Revisiting Russell's Troodontid: Autecology, Physiology, And

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Canadian Journal of Earth Sciences

Revisiting Russell’s troodontid: autecology, physiology, and speculative tool use

Journal: Canadian Journal of Earth Sciences

Manuscript ID cjes-2020-0184.R1

Manuscript Type: Article

Date Submitted by the 12-Jan-2021 Author:

Complete List of Authors: Varricchio, David; Dept of Earth Sciences Hogan, Jason; Dept of Earth Sciences Freimuth, William; North Carolina Museum of Natural Sciences, Paleontology; North Carolina Community College System, Biological Sciences Draft Keyword: Dinosaurs, Traces, Paleobiology, Troodontids, Troodon, gastric pellets

Is the invited manuscript for consideration in a Special Tribute to Dale Russell Issue? :

3 Revisiting Russell’s troodontid: autecology, physiology, and speculative tool use 4

6 D. J. Varricchio, J. D. Hogan, and W. J. Freimuth

8 D.J. Varricchio and J.D. Hogan. Earth Sciences, Montana State University, Bozeman, MT

9 USA 59717, [email protected], [email protected]

10 W.J. Freimuth. [1] Paleontology, North Carolina Museum of Natural Sciences, 11 W Jones St, 11 Raleigh, NC USA 27601 and [2] DepartmentDraft of Biological Sciences, North Carolina 12 State University, 100 Brooks Ave., Raleigh, NC USA 27607 [email protected]

13 Corresponding author: David Varricchio (e-mail: [email protected]), 406-994-6907, fax 406-

14 994-6923.

1 © The Author(s) or their Institution(s) Canadian Journal of Earth Sciences Page 2 of 65

24 Abstract: Dale Russell described the osteology, morphology, and ecology of the small theropod

25 “Stenonychosaurus inequalis” in two papers, speculating on its life habits, brain-power, vision,

26 movement, feeding and hand capabilities. Russell even pondered a tool-using dinosauroid, the

27 hypothetical troodontid descendant if the lineage survived the K/Pg extinction. We revisit the life

28 habits of the North American troodontids, Troodon formosus and Latenivenatrix mcmasterae, by,

29 in part, reviewing various trace fossils of T. formosus discovered in Montana. These include egg

30 clutches, a nest, and recently discovered regurgitalites. We also ruminate on the possibility of

31 dinosaur tool use. Troodon likely constructed earthen nests as ratites and other birds create their

32 nesting scrapes, through backward hindlimb kicks. The more complex clutch architecture

33 suggests dexterous movement of the eggs, potentially requiring manual manipulation.

34 Functionally, reproductive traces supportDraft elevated body temperatures and a metabolic output that

35 approached but did not equal that of modern birds. Brooding would require very high energy

36 investment from the adult. The regurgitalites largely contain multi-individual aggregations of the

37 marsupialiform Alphadon and support Russell’s hypotheses of troodontids as nocturnal,

38 intelligent, small game hunters with elevated metabolism and enhanced vision. Tool use in a few

39 crocodilians and widely among extant birds suggests a reasonable possibility of this behavior in

40 non-avian dinosaurs. Whether avian-comparable encephalization quotient and freed forelimbs

41 would make North American troodontids good candidates to exhibit such behavior remains an

42 open and speculative question. However, given the minimal modification made to tools by

43 modern archosaurs, recognition of fossil tools poses a challenging problem.

45 Keywords: Troodon, troodontid, reproduction, encephalization quotient, regurgitalites, gastric

46 pellets, trace fossils, tool use, physiology

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47 Introduction

48 Dale Russell summarized the osteology, morphology, and ecology of the troodontid

49 dinosaur “Stenonychosaurus inequalis” in two papers (Russell 1969; Russell and Séguin 1982).

50 The first paper (Russell 1969) describes several troodontid specimens collected in the Upper

51 Cretaceous beds of Alberta, Canada from what at the time were considered part of the Oldman

52 Formation. In “Reconstruction of the small Cretaceous theropod and a hypothetical

53 dinosauroid,” Russell and Séguin (1982) document their building of a three-dimensional model

54 of the dinosaur and the reasoning behind the proportions and shape of their reconstruction. In

55 conjunction with this project, they also speculate on its life habits including brain-power, vision, 56 movement, hand capabilities, and feedingDraft (topics also covered in Russell 1969) (Fig. 1). 57 Additionally, and somewhat surprisingly, they ponder what the descendants of this dinosaur

58 might have looked like if they had survived the K/Pg extinction event.

59 Here we revisit the life habits of the North American troodontids, Troodon formosus (a

60 senior synonym of S. inequalis, see below) and Latenivenatrix mcmasterae, by reviewing the

61 various trace fossils discovered in Montana over the last 40 years. These include egg clutches, a

62 nest, and regurgitalites (fossil regurgitates) that have implications for troodontid ecology,

63 feeding, hand use, and metabolism. Finally, with a nod to the ruminations of Russel and Séguin

64 (1982), we speculate on possible tool use in Mesozoic dinosaurs.

65 In 1969, small theropods of any clade, from anywhere, were exceedingly rare;

66 surprisingly, the year saw osteological description of three important taxa: “Stenonychosaurus

67 inequalis” (Russell 1969), Dromaeosaurus albertensis (Colbert and Russell 1969), and

68 Deinonychus antirrhopus (Ostrom 1969). These descriptions were important contributions to the

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69 revitalization of the dinosaur origins of birds and in the re-thinking of Mesozoic dinosaurs as

70 active, intelligent and complex vertebrates (Russell 1969; Ostrom 1969).

71 Russell (1969) identifies his “Oldman” troodontid material as Stenonychosaurus

72 inequalis, a taxon named by Sternberg (1932) on a foot and additional associated material.

73 However, in 1993, the upper portion of the Oldman Formation was recognized as a distinct unit,

74 the Dinosaur Park Formation (Eberth and Hamlin 1993) and Russell (1969) includes specimens

75 from both the Oldman and Dinosaur Park Formations. Since 1969, there have been several

76 taxonomic revisions of S. inequalis. Currie (1987) synonymizes S. inequalis into the earlier

77 named Troodon formosus from the Judith River Formation of Montana. Although Currie (2005)

78 introduces a new combination, Troodon inequalis in 2005, T. formosus has largely remained in

79 use since 1987. More recently, van der ReestDraft and Currie (2017), abandon the earlier

80 synonymization of Currie (1987) and recognize two species within T. formosus of Currie (1987):

81 S. inequalis and the newly named Latenivenatrix mcmasterae for troodontids of the lower and

82 upper portion of the Dinosaur Park Formation, respectively. Russel’s 1969 description of “S.

83 inequalis” thus incorporates specimens representative of both taxa. Varricchio et al. (submitted)

84 argue, as Russell (1969) also notes, that T. formosus has priority, and thus is the proper name for

85 S. inequalis as defined by van der Reest and Currie (2017), a usage we follow here.

86 Russell (1969) documents a number of taxonomically and likely functionally important

87 osteological features in troodontids. Among these are a sizeable brain with large cerebral

88 hemispheres, spacious orbits with a strong anterior orientation, bowed ulna, a semilunate carpal

89 with a mesocarpal wrist articulation, long hind limb proportions, fused calcaneum and astragalus,

90 and an arctometatarsalian and highly asymmetric metatarsus. Based on these observations,

91 Russell (1969, 1981; Russell and Séguin 1982) proposes several hypotheses concerning the

92 physiology, behavior, and intelligence of these Late Cretaceous troodontids of Alberta and

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93 Mongolia. These include: 1) a brain with an avian level of intelligence and organization

94 requiring a high metabolism with potentially endothermy (Béland and Russell 1979), 2) excellent

95 vision with stereoscopic and nocturnal capabilities, 3) mobile lower arm, 4) an opposable and

96 grasping manual digit III providing manual dexterity, 5) rapid and agile gait, 6) occupation of

97 terrestrial environments distal from depositional centers, and 7) predation upon small crepuscular

98 to nocturnal mammals (Fig. 1). Noting that Late Cretaceous troodontids possess a large brain,

99 stereoscopic vision, opposable digits, and a bipedal gait, attributes also found within the earliest

100 hominids (Jones et al. 1995a), Russell and Séguin (1982) speculate on the course of evolution for

101 these theropods if the lineage survived the end-Cretaceous extinction. They propose that

102 selection would favor an ever-increasing brain size, tool-use, live birth, and a rather hominid-like

103 body plan in the subsequent “dinosauroid”.Draft

104 A number of these hypotheses of Russell were more fully demonstrated by later research

105 and proved to be important in the re-imagining of dinosaurs as more active and endothermic

106 vertebrates. For example, recognition of the large brain and brain to body size ratio in “S.

107 inequalis” (Russell 1969; Russell and Séguin 1982; Russell and Dong 1993) figured prominently

108 in subsequent discussions on the evolution of brain size in dinosaurs and its implications for

109 endothermy (Hopson 1977, 1980). Further, the cerebral expansion and elaboration of visually

110 associated brain regions within troodontids and related theropods remain important links to the

111 development of an avian brain and bird origins (Balanoff et al. 2013; Xu et al. 2014). Even the

112 suggestion that the “optic lobes were probably shifted ventrolaterally as in birds” (Russell 1969,

113 p. 598) has been demonstrated by three-dimensional reconstructions of troodontid endocasts

114 (Balanoff et al. 2013). Visually, Stevens (2006) corroborates binocular vision in Troodon with a

115 binocular field matching or exceeding those of extant raptorial birds, and the abundance of

116 Troodon in high latitude assemblages of Alaska may reflect its visual acuity in low-light

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117 conditions (Fiorillo and Gangloff 2001; Fiorillo 2008) as originally suggested by Russell (1969;

118 Russell and Séguin 1982). Furthermore, subsequent discoveries (Russell and Dong 1993;

119 Varricchio 1997) and analyses (Carrano 1999; Persons and Currie 2016) clearly demonstrate the

120 cursorial limb proportions of troodontids consistent with the rapid and agile gait previously

121 envisioned on relatively sparse material (Russell 1969).

122 In contrast, other hypotheses remain untested or contradicted by more recent discoveries.

123 For example, the dexterity of the antebrachium and manus of troodontids remains an open

124 question, in part due to a lack of articulated material from North America. Senter (2006a) shows

125 the radius to sit immobile against the ulna in the dromaeosaurids, Deinonychus and Bambiraptor,

126 restricting supination and pronation. However, he proposes an opposable digit III in Bambiraptor

127 based on the twisting shaft of phalanx III-3Draft which repositions the ungual in opposition to that of

128 digit I (Senter 2006a). Russell (1969) suggests a different mechanism for opposability with

129 metacarpal III in “S. inequalis” being independently mobile of the other metacarpals. However,

130 several more recently discovered Asian specimens preserve articulated hands with inter-braced

131 metacarpals (Barsbold et al. 1987; Currie and Dong 2001; Gao et al. 2012) that would preclude

132 independent movement of metacarpal III as noted in Sinornithoides youngi by Russell and Dong

133 (1993). Thus, an opposable digit III is unlikely if North American troodontids share a similar

134 metacarpal morphology with Asian taxa.

135 Russell (1969, p. 611) suggests “the extreme rarity of Stenonychosaurus and

136 Dromaeosaurus in the Oldman Formation may very likely be due to their strong preference for

137 purely terrestrial surroundings, which are not well represented among the freshwater

138 environments of deposition in this stratigraphic unit.” Certainly, North American troodontids

139 continue to remain very rare, with a known record largely of isolated teeth (White et al. 1998)

140 and their taxonomy still often relying on isolated elements (van der Reest and Currie 2017;

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141 Evans et al. 2017). Taphonomic surveys, however, suggest they were regular components of the

142 floodplain fauna, their underrepresentation likely reflecting their small and more fragile

143 skeletons (White et al. 1998; Brown et al. 2013).

144 Finally, in contrast to Russell (1969) but consistent with Béland and Russell (1979),

145 associations of numerous shed Troodon teeth with baby hadrosaur elements in sites in both

146 Alberta and Montana suggest Late Cretaceous troodontids of North America may have favored a

147 broad array of small prey, not just mammals (Horner 1994; Ryan et al. 1998). This is further

148 supported by troodontid tarsal and pedal morphology (Fowler et al. 2011) and biomechanical

149 models of troodontid teeth (Torices et al. 2018) that suggest morphological adaptations well-

150 suited for capturing and processing relatively small prey.

151 The infamous dinosauroid continuesDraft to live on long after it first ‘evolved’ (Russell and

152 Séguin 1982) inspiring a number of science-fictional reconstructions (Carey and Kirkland 2000;

153 Baxter 2003; Leigh and Miller 2004). But the dinosauroid has also influenced those vigorously

154 contemplating the existence and form of extraterrestrial intelligence (Harrison 1993; Ashkenazi

155 2017), evolutionary development in a universal sense (Smart 2019), and the role of contingency

156 versus determinism in the evolution of life here on earth (Morris 2003; Losos 2017).

157 Here we first review the reproductive traces for T. formosus and then follow this by

158 examining some recently discovered mammal-rich regurgitalites from Egg Mountain in

159 Montana. We consider the locomotor and physiologic implications of these traces and what they

160 may say about the ecology, sensory capabilities, dexterity and metabolism of the North

161 American troodontids, T. formosus and L. mcmasterae (See Table 1 for list of specimens). Given

162 that modern birds and crocodilians are now known to use and even build tools (e.g., Lefebvre et

163 al. 2002; Dinets et al. 2013), this behavior might have existed in some dinosaur groups as well.

164 We finish by first pondering the intelligence of these troodontids and then the possibility of and

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165 in what ways Mesozoic tools might have been used, and how such artifacts or behaviors might

166 be represented in the fossil record.

167 168 Reproductive traces

169 Reproductive traces for Troodon formosus include numerous egg clutches (Horner 1982,

170 1984, 1987; Hirsch and Quinn 1990; Zelenitsky and Hills 1996) and a nest structure (Varricchio

171 et al. 1997, 1999). The physical construction and reproductive function of these traces has

172 implications for both the locomotor capabilities and metabolism of this dinosaur.

173

174 Construction 175 The only well-preserved nest, MuseumDraft of the Rockies (MOR) 963 consisted of a bowl- 176 shaped depression with an internal area of approximately 1 m2 surrounded by a distinct rim

177 (Varricchio et al. 1999). A clutch of 24 tightly-placed eggs sat in the center and both nest and

178 clutch show bilateral symmetry about a north–south axis. The trace occurs within a moderately

179 well-developed micritic paleosol. A physically and chemically distinct mudstone originally

180 covered the nest and represented overbank deposition. The external dimensions for the structure

181 measure 1.6 m north–south by 1.7 m east–west externally (Fig. 2). Most of the nest perimeter is

182 marked by a distinct rim that forms a large "U" enclosing an arc of around 270° about the clutch.

183 For most of its length, the raised rim stands 10 cm high and 21 cm wide. A lower, straighter, and

184 less distinct rim closes the remaining northern portion of the nest, and the clutch sits closest to

185 this low north rim. The U-shaped portion of the rim has a steeper interface with a slope of

186 approximately 40° and a gentler exterior face angled at 27°. Between 15 and 40 cm separate the

187 internal edge of the rim to the clutch perimeter and the nest floor slopes gently down from rim to

188 clutch at approximately 15° (Varricchio et al. 1999).

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189 Egg clutches show a consistent pattern. The elongate and asymmetric T. formosus eggs

190 are placed narrow end down in the ground, steeply plunging and angled away from the clutch

191 center such that the upper blunt ends are closely spaced to touching, whereas the narrow ends

192 radiate away (Horner 1987; Hirsch and Quinn 1990; Varricchio et al.1997). Egg-pairing is

193 suggested by egg spacing, trends, and plunges in some clutches and is statistically supported in

194 one (MOR 363) (Varricchio et al. 1997).

195 The sub circular clutches may have up to 24 eggs (Horner 1987; Varricchio et al. 1999)

196 In some clutches, a lithologic transition occurs approximately two-thirds of the distance up from

197 the small pole of the egg (Horner 1987). For example, excavation of MOR 963 revealed the

198 bottom portions of most eggs as preserved in a micritic bioturbated limestone, whereas fissile

199 mudstone surrounded the upper one-thirdDraft of the eggs (Varricchio et al. 1999).

200 The nest and clutches clearly represent the works of Troodon formosus, but how did they

201 excavate and build the earthen nest and how did they construct the clutch with its tight egg

202 spacing and unusual egg orientation? The T. formosus nest structure appears most similar to the

203 scrapes generated by a variety of birds for the incubation of their eggs. Nesting scrapes occur

204 among galliforms (pheasants, grouse, partridge), anseriforms (various ducks), Charadrii (e.g.,

205 coursers, killdeer) and short-eared owl (Asio flammeus), with the largest, the product of ratites

206 including ostrich (Struthio camelus), greater rhea (Rhea americana), and emu (Dromaius

207 novaehollandiae) (Davies 2002; Goodfellow 2011). Male ostrich and greater rhea create their

208 scrapes by kicking backward with their feet. The ostrich adopts a lying pose and pushes the soil

209 out behind him, whereas the greater rhea may crouch and slowly rotate. Its movement helps

210 shape the nest and generate a low mound at the perimeter (Davies 2002).

211 Although megapodes construct more complex nests than scrapes, they too use their feet

212 to either rake material into mounds (e.g., Australian brush-turkey, Alectura lathami) or to scratch

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213 out burrows (e.g., Malleefowl, Leipoa ocellata; Maleo, Macrocephalon maleo). Typically, they

214 scratch several times with one leg before shifting to the other (Jones et al. 1995b). Even those

215 birds that rely on their bills to break ground when digging their nest burrows still employ their

216 feet to clear any loosened debris (Goodfellow 2011; Hansell 2000). Crocodilians and some

217 turtles similarly excavate and build their nesting burrows and mounds with their hindlimbs (Ross

218 1989; Fowler and Hall 2011). Thus, it seems reasonable that a bipedal animal like T. formosus,

219 would, like ratites, employ their relatively robust hindlimbs and feet in the principal excavation

220 and movement of earth in their nest construction. Whether this could account for the sharper rim

221 of the Troodon nest remains to be determined.

222 The emplacement of elongate eggs at a steep angle and perhaps 10 cm deep into a soil

223 horizon seems like a more challenging taskDraft than the earth-moving of nest construction. Two

224 possible scenarios might explain how a clutch of 24 eggs was constructed with eggs laid

225 iteratively two at a time, over multiple days. In the first scenario, an adult T. formosus would

226 loosen a patch of ground, freeing the soil of binding vegetation and breaking up clods of earth.

227 This might be done by either hands or feet. Hands using a clawing action might be better suited

228 for this purpose, since the goal would not be earth removal, but simply disaggregation.

229 Hindlimbs and feet seem better suited for dispersion and movement of earth as with ratite nest

230 builders or pronghorns and canids making “spuds”, territorial marking scrapes (Halfpenny 2008).

231 An alternative scenario would be more constructive with the adult beginning by

232 excavating a bowl; the low north rim of the T. formosus nest could reflect this. Within in this

233 space, the adult would then build a small mound. Eggs would then be layered around this mound

234 with additional dirt in an iterative fashion.

235 In either scenario of nest construction the most challenging aspect, in terms of dexterity,

236 would be the actual emplacement of the eggs. Potentially, eggs might be arranged during laying

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237 by deft positioning of the hindlimbs and cloaca. Egg orientations would then simply reflect the

238 act of ovipositing. Potential challenges to this emplacement hypothesis would be whether the

239 adult could accurately straddle a growing clutch and generate enough push to place the egg into

240 the soil. The postures preserved in specimens of Sinornithoides and Mei long might support this

241 squatting action (Russell and Dong 1993; Gao et al. 2012). Alternatively, eggs could be

242 manipulated into the proper position by either the hands or mouth. The elongate shape and ~ 67

243 mm diameter of the eggs would seem to make them relatively easy to grasp with the manus, even

244 if all digits were simply flexing. Senter (2006a) shows that Deinonychus, an animal fairly similar

245 in size and form, could likely have flexed its digits sufficiently to comfortably grasp an egg.

246 Whereas both Gishlick (2001) and Carpenter interpreted grasping forelimbs in Deinonychus,

247 Senter (2006a) considered the theropod Draftincapable of scratch digging and one-handed prehension

248 by curling the digits around an object due to pronation issues and complications of feathers,

249 respectively. The more distantly related Struthiomimus altus may also have had good flexion

250 capabilities (and pectoral girdle maneuverability), even if it lacked a specialized grasping

251 function(Nicholls and Russell 1985). Alternatively, T. formosus might have been able to grasp an

252 egg with its mouth as observed in numerous crocodilians (Ross 1989). This would perhaps only

253 require a gape of 70 mm to grasp effectively. Although hindlimb use in nest construction seems

254 likely given the habits of modern birds, the role of hands, mouth, and feet in egg arrangement

255 remains more problematic. Functional analysis of more complete troodontid forelimbs could help

256 resolve this issue.

257

258 Function

259 The functional implications of Troodon formosus reproductive traces have ramifications

260 for overall energetics as well as body temperature. The statistically significant paired egg

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261 arrangement found in a complete T. formosus clutch, a pattern commonly seen in oviraptorosaur

262 clutches, was used to argue for monoautochronic ovulation (Varricchio et al. 1997), the process

263 where two eggs are produced and deposited at daily or greater intervals (Smith et al. 1973). The

264 subsequent discovery of oviraptorosaur adults each with an associated pair of eggs corroborates

265 this type of egg production in pennaraptoran theropods (Sato et al. 2005; Jin et al. 2020). These

266 paired eggs represent a measure of metabolic output, and a pair of T. formosus eggs at 312 g each

267 (Varricchio et al. 2013) represents 58% of the mass of a single egg predicted for a bird of

268 equivalent adult body mass (50 kg) (Blueweiss et al. 1978). This suggests a somewhat similar

269 metabolic output for each egg-laying iteration. However, the key missing variable is time, the

270 time between egg-laying episodes and hence the time available to generate the egg pair. Birds

271 commonly produce eggs at daily intervals,Draft but larger birds with more massive eggs may require

272 multiple days to generate an egg. For example, megapodes require 4 to 8 days to produce their

273 eggs, whereas ratites, penguins and large raptors need 3 to 5 days (Gill 1989). So, if the rate of

274 egg production was similar to that found in birds, then T. formosus reproductive output would

275 have been 58% of that for modern birds, but any extended gaps between egg laying could alter

276 this significantly. Potentially, the rate of eggshell formation, based on the microstructure form

277 and orientation, might provide a means for quantifying at least this portion of egg formation.

278 The functional significance of the nesting trace has been discussed in detail elsewhere,

279 with the main interpretation being that contact incubation (brooding) is supported by the shape of

280 the nesting trace, the absence of organic matter in the overlying sediment, the clutch

281 configuration with eggs partially exposed in the nest, consistent vertical changes in lithology

282 associated with this and other clutches, and an unhatched egg clutch associated with a partial

283 adult skeleton (Varricchio et al. 1997, 1999, 2002). Low porosity and gas conductance values

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284 further support the partial burial of eggs and incubation by a brooding T. formosus adult

285 (Varricchio et al. 2013).

286 For maniraptorans, some authors favor crocodilian-like nest guarding (Wesolowski 2004;

287 Deeming 2006; Jones and Geist 2012) over any form of contact incubation. Others support a

288 more avian style incubation involving some form of contact incubation (Norell et al. 1995;

289 Varricchio et al. 2013, 2018). Contact incubation is a crucial piece of modern bird reproduction,

290 but it is unclear whether this behavior can be traced back to their dinosaur ancestors. It is

291 suggested that contact incubation may be problematically inefficient when paired with a partially

292 buried clutch (Ruben et al. 2003). Partial burial of eggs is extremely rare among modern

293 vertebrates (Grellet-Tinner et al. 2006), and so comparative physiology is not of much use.

294 Actualistic experiments into the Draftfeasibility of contact incubating partially buried eggs

295 argue that the two behaviors are not mutually exclusive (Hogan and Varricchio 2021). Eggs,

296 incubated half submerged in sediment, maintained temperatures much closer to surrogate than

297 ambient. This was true for experiments in both controlled indoor and fluctuating temperature

298 outdoor scenarios. Furthermore, daily caloric expenditure was approximately equivalent to that

299 of brooding emus (Buttemer and Dawson 1989; Hogan and Varricchio 2021) suggesting that the

300 experiment itself was not unrealistically energy efficient.

301 Two further implications of brooding include 1) an elevated body temperature, sufficient

302 to raise clutch temperatures beyond ambient conditions and 2) a sustained parental investment

303 through the incubation period that carries with it an energetic cost. An elevated body temperature

304 is additionally implied by the function of the complexly arranged but iteratively produced egg

305 clutch. From a construction perspective, the more central eggs would appear to be those first laid.

306 But for this clutch arrangement to function well, given precocial young, one would presume that

307 eggs in the center of the clutch could not hatch earlier than those at the periphery.

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308 In most modern birds with large clutches and precocial young, adults refrain from

309 incubating eggs until completion of the clutch (Gill 1989; Stoleson and Beissinger 1995; Hébert

310 2002). Thus, embryos in earlier laid eggs remain at ambient temperatures and in developmental

311 stasis until brooding begins. Brooding begins with the completion of the clutch, raising the

312 embryos to incubation temperatures and synchronizing hatching of the precocial young (Gill

313 1989). The implication from the trace is then, that the attending adult T. formosus has a body

314 temperature elevated above ambient conditions. Based on incremental growth lines in the teeth

315 of T. formosus embryos, the incubation period was approximately 74 days, substantially shorter

316 than that predicted for a reptilian egg of similar mass (Varricchio et al. 2018). This further

317 implies elevated incubation temperatures.

318 Regardless of whether elevated incubationDraft temperatures are a product of special

319 behaviors by an ectotherm or normal conditions of an endotherm, the energetics of brooding a

320 clutch of relatively large eggs (312 g each) would be significant. Large pythons such as the

321 Indian python (Python moluru) and the Australian king python (Morelia spilotes) incubate their

322 eggs by muscular shivering that elevates their body temperatures. Rates of oxygen consumption

323 can be as much as 20 times greater than a non-brooding individual at the same temperature (Van

324 Mierop and Barnard 1978; Harlow and Grigg 1984). Further, females fast during the

325 development of eggs (3 months) and then through brooding (2 more months), so that in cold

326 climates, the energetic costs are so high that breeding is restricted to every second year (Harlow

327 and Grigg 1984). Energetic costs for brooding birds can also be high. Emus have been measured

328 to expend between 645 and 813 kcal/day while incubating and incubation may take 56 days

329 (Buttemer and Dawson 1989). Thus, simply the act of brooding a clutch would demand a

330 significant energetic investment from the incubating T. formosus.

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331 Trace fossils have been described simply as “fossil behavior” (Seilacher 1967). If our

332 interpretation of the function of these traces is correct, then they provide insight into the body

333 temperature and energetics of T. formosus, and potentially useful constraints to be tested by other

334 lines of investigation. The metabolic output as represented by producing an egg pair as well as

335 the incubation capabilities of brooding both appear to approach, but importantly, not match the

336 condition in modern birds.

337

338 Feeding traces

339 Russell (1969) first posited Late Cretaceous troodontids as active hunters of small, 340 crepuscular mammals based on a suite ofDraft morphological adaptations including a large brain 341 within enhanced cerebral hemispheres, large eyes with some degree of binocular capabilities,

342 powerful and agile hindlimbs, and dexterous forelimbs (Fig. 1). These ideas were elaborated

343 upon and further demonstrated in the life reconstruction of “S. inequalis” (Russell and Séguin

344 1982). The predatory adaptations, behaviors, and ecological inferences for troodontids have been

345 supported by subsequent morphological and taphonomic analyses. Moreover, regurgitalites

346 (fossilized regurgitates or gastric pellets) potentially attributable to Troodon formosus from the

347 Upper Cretaceous Two Medicine Formation lend additional support to the inferences of diet and

348 behavioral ecology postulated by Russell (1969) and Russell and Séguin (1982).

349 Two examples of regurgitalites from the Egg Mountain locality of the Upper Cretaceous

350 (Campanian) Two Medicine Formation of Montana are described in Freimuth (2020; Freimuth et

351 al. in press) (Fig. 3A–B, Table 1). One specimen (MOR 10912) contains three individuals of the

352 marsupialiform Alphadon halleyi preserved within a <100 cm2 area (Fig. 3A). A second (MOR

353 10913) comprises eleven individuals, including ten A. halleyi and an indeterminate lizard skull,

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354 contained within <300 cm2 (Fig. 3B). The close association of multiple individuals in a confined

355 area combined with the inferred depositional setting (Freimuth and Varricchio 2019; Panascí and

356 Varricchio 2020) are unlikely for an abiotic origin of these deposits, and a lack of a phosphatic or

357 mineralized ground mass in both specimens precludes their assignment as coprolites (Freimuth

358 2020; Freimuth et al. in press; Gordon et al. 2020). Both specimens are characterized by high

359 proportions of paired crania and indigestible tooth-bearing elements, prevalent disarticulation,

360 extensive breakage of crania and postcrania, and periosteal corrosion attributable to digestion,

361 features which closely match prey remains in gastric pellets of extant diurnal raptors

362 (Accipitriformes and Falconiformes), such as hawks, harriers, and kestrels (Andrews 1990;

363 Montalvo and Fernández 2019; Freimuth 2020; Freimuth et al. in press) (Fig. 3).

364 Troodon formosus is the best candidateDraft as the producer of Alphadon-bearing

365 regurgitalites based on: 1) abundant nesting evidence, suggesting extended occupation at the

366 locality; 2) abundant shed teeth, suggestive of active feeding behavior; 3) teeth and postcrania

367 suited for small prey items; and 4) inferred derived ability of troodontids and avialans to

368 routinely expel gastric pellets (see Freimuth 2020 for discussion). Accordingly, these

369 regurgitalites pose several implications for the behavioral ecology of T. formosus, including

370 ecological role, vision capabilities and diel patterns, hand use, and metabolism. These are

371 expanded upon the original observations and ecological inferences made by Russell (1969) and

372 Russell and Séguin (1982).

373

374 Troodontid prey selection and ecological role

375 Russell (1969) first noted morphological features of the cranium that suggested Late

376 Cretaceous troodontids were adapted for small mammalian prey, compared to the relatively

377 robust cranium of dromaeosaurids which were better adapted for prey closer to their own body

16 © The Author(s) or their Institution(s) Page 17 of 65 Canadian Journal of Earth Sciences

378 size. Subsequent taphonomic and morphological studies further support this initial distinction.

379 An exceptional Velociraptor–Protoceratops association is perhaps the best evidence for larger

380 prey strategies amongst dromaeosaurids (Carpenter 1998), whereas the association of numerous

381 shed Troodon teeth at a hadrosaur nesting ground suggest a small (albeit non-mammalian) prey

382 preference (Ryan et al. 1998). Fowler et al. (2011) suggest the stout metatarsus and ginglymous

383 articulations of dromaeosaur pedal elements were better adapted for handling larger prey, while

384 the slender arctometatarsalian metatarsals and ball-like articulation of mt-I of T. formosus was

385 better adapted for small prey. Using finite element analyses, Torices et al. (2018) demonstrate

386 that Troodon teeth fail at suboptimal bite angles, suggesting a small or soft prey diet in contrast

387 to the more robust teeth of tyrannosaurids and dromaeosaurids which were suitable for larger or

388 struggling prey. Regurgitalites from EggDraft Mountain, if produced by T. formosus, offer the best

389 available evidence of a small mammalian diet, supporting original inferences of troodontid

390 dietary preference by Russell (1969).

391 The relationship between predator body mass and prey body mass is a significant factor

392 in modern terrestrial ecosystems, where larger carnivores tend to prefer proportionally larger

393 prey compared to smaller carnivores (Vézina 1985). Carbone et al. (1999) additionally

394 demonstrate that predators under 21.5 kg will favor proportionally smaller prey, and a similar

395 pattern (~16–32 kg) is hypothesized for dinosaurian communities (Codron et al. 2013). By these

396 models, a ~50 kg adult T. formosus (Varricchio 1993; ~45 kg “S. inequalis” Russell 1969)

397 appears too large to consistently prey upon small mammals. However, a number of larger

398 modern predators regularly incorporate small-bodied mammals in their diet, including Komodo

399 dragons (Varanus komodoensis, 35–59 kg; Auffenberg 1981) and pumas (Puma concolor, (29–

400 120 kg; Montalvo et al. 2007). Small-bodied mammals are also dietary components of

401 omnivorous maned wolves (Chrysocyon brachyurus, 30 kg; Aragona and Setz 2001);

17 © The Author(s) or their Institution(s) Canadian Journal of Earth Sciences Page 18 of 65

402 omnivorous to herbivorous habits have been previously discussed for T. formosus (Holtz et al.

403 1998), although some degree of faunivory is likely (Larson et al. 2016; Torices et al. 2018;

404 Cullen et al. 2020). The body mass of a small juvenile T. formosus from Egg Mountain (MOR

405 430) is calculated as ~2.4 kg (after Campione et al. 2014, eq 7) or ~3.0 kg (with developmental

406 mass extrapolation of Erickson and Tumanova 2000), and a larger juvenile from elsewhere in the

407 Two Medicine Formation (MOR 563) is calculated as ~12.9 kg (after Campione et al. 2014, eq

408 7) or ~18.0 kg (with developmental mass extrapolation of Erickson and Tumanova 2000) (Table

409 1). These estimates fall within the mass ranges of many extant owls and mammalian carnivores,

410 respectively, frequent predators of small-bodied mammals (Andrews 1990). Combined with

411 abundant nesting evidence at Egg Mountain and the morphological features noted above and by

412 Russell (1969), immature T. formosus mayDraft be good candidates as hunters (and regurgitators) of

413 small-bodied mammals.

414 The role of troodontids amongst other theropods in Late Cretaceous ecosystems remains

415 a somewhat open question, and their scarcity (first noted by Russell 1969) in Late Cretaceous

416 deposits further complicates broad ecological inferences (White et al. 1998; Brown et al. 2013).

417 Nonetheless, the presence of troodontid material over a vast geographic (present day Utah to

418 Alaska) and temporal (Campanian through Maastrichtian, ~20 Ma) range suggests they were

419 regular components of floodplain fauna in the Late Cretaceous of North America (Fiorillo 2008;

420 Zanno et al. 2011). Among contemporaneous theropods, the partitioning of different food

421 sources is supported by analyses of dental and ecomorphological disparity (Larson et al. 2016),

422 and stable isotope analysis (Frederickson et al. 2018). However, the precise nature of these

423 apparent niches is poorly understood (Larson et al. 2016). Mounting morphological and

424 taphonomic evidence for a small prey preference (discussed above) combined with possible T.

18 © The Author(s) or their Institution(s) Page 19 of 65 Canadian Journal of Earth Sciences

425 formosus regurgitalites offer a more nuanced predatory niche for troodontids with potential to

426 guide future studies of theropod ecologies in the Late Cretaceous of the Western Interior.

427 428 A messy eater? Evaluating prey processing

429 Russell (1969) also notes the robustness of the forelimbs in troodontids and posits they

430 were adaptations for predation in conjunction with the enlarged raptorial pedal digit and

431 hindlimb proportions suited for agility. The taphonomic features of the Egg Mountain

432 regurgitalites may support these functional inferences. Prey remains in modern gastric pellets

433 reflect the feeding processes of broad predator groups (Terry 2007). For example, owls

434 (Strigiformes) tend to swallow prey whole, producing prey remains in gastric pellets with more 435 equal representation of crania versus postcrania,Draft fewer broken elements, and less digestive 436 corrosion (Andrews 1990; Terry 2007; Montalvo and Fernández 2019). In contrast, diurnal

437 raptors (Accipitriformes and Falconiformes) will stabilize prey with their feet and tear chunks of

438 flesh with their beak; this results in regurgitated prey remains that display greater element

439 breakage, and in turn greater digestive corrosion and a greater representation of crania and tooth-

440 bearing elements (Andrews 1990; Terry 2007; Montalvo and Fernández 2019). The similarities

441 between prey in gastric pellets of diurnal raptors and the features of Egg Mountain regurgitalites

442 suggest T. formosus manipulated or processed prey during feeding prior to consumption and

443 regurgitation (Fig. 3C). Similar feeding behaviors are inferred for deinonychosaurs, where the

444 feet and hypertrophied digit II were used to pin and grasp prey items (Fowler et al. 2011).

445 Though first suggested by Russell (1969), it is unlikely that troodontids would have manipulated

446 prey with opposable digits given updated views of metacarpal morphology (Russell and Dong

447 1993). Nonetheless, the forelimbs may have played a role in food acquisition in other

448 maniraptoriforms (Nicholls and Russell 1985), and specifically deinonychosaurs (Carpenter

19 © The Author(s) or their Institution(s) Canadian Journal of Earth Sciences Page 20 of 65

449 2002), including potential digit opposability and grasping functionality (Senter 2006a). The

450 functionality of T. formosus or other troodontids forelimbs remains to be tested. The taphonomic

451 features of Egg Mountain regurgitalites evoke questions of troodontid manual and pedal

452 dexterity and their utilization in predatory behaviors, ideas first conveyed by Russell (1969).

453

454 Sensory capabilities

455 “S. inequalis” possesses an orbital diameter estimated at 52 mm with a forward slope of

456 40° (Russell 1969), and both Russell (1969) and Russell and Séguin (1982) remark on the large

457 eye size and binocular capabilities likely contributing to acute visual senses. Using the

458 reconstructed “S. inequalis” model of Russell and Séguin (1982), Stevens (2006) predicts a

459 binocular field of view of 55-60°, comparaDraftble to owls and other predatory raptorial birds but less

460 than many mammalian carnivores (Heesy 2004). Russell and Séguin (1982) conservatively

461 estimate an eye size of 44 mm and discussed the large sclerotic ring and likely crepuscular to

462 nocturnal habits of “S. inequalis” and other Late Cretaceous troodontids. Similar analyses using

463 sclerotic ring morphology predict nocturnal lifestyles for many small theropods (Schmitz and

464 Motani 2011; but see Hall et al. 2011), and many Mesozoic mammals, including metatherians,

465 are hypothesized as nocturnal (e.g., Kielan-Jaworowska et al. 2004; Heesy and Hall 2010; Maor

466 et al. 2017). It is possible that the presumed Alphadon–Troodon relationship records a nocturnal

467 feeding interaction, supporting Russell’s original ecological hypotheses (Russell 1969; Russell

468 and Séguin 1982). If T. formosus and other troodontids were indeed nocturnal, this offers a

469 potential mode of ecological separation of troodontids from other small- to medium-sized

470 theropods in the Late Cretaceous.

471 Russell (1969; Russell and Séguin 1982) notes that the braincase of derived troodontids

472 accommodated enlarged cerebral hemispheres and would have provided an “avian level” of

20 © The Author(s) or their Institution(s) Page 21 of 65 Canadian Journal of Earth Sciences

473 intelligence, suitable for preying upon similarly encephalized mammals. Indeed, the estimated

474 encephalization quotient (EQ) for Russell’s “S. inequalis” ranges from 0.24 to 0.34 (Russell and

475 Séguin 1982), comparable to extant opossums (0.24–0.27 in Didelphis virginiana) and some

476 stem marsupials (Macrini et al. 2007). The relationship between predator–prey brain size appears

477 to hold true in some cases, where larger-brained prey is selected by proportionally larger-brained

478 predators (Kondoh 2010). Encephalization has been noted to increase amongst organisms that

479 occupy relatively higher trophic positions, including dinosaurs (Hopson 1977; Russell 1981). For

480 carnivorous mammals, Gittleman (1986) likens an increased brain size to greater sensory

481 function necessary for seeking and procuring prey. This pattern is seen in birds, where eye size

482 and brain size appear to have coevolved in response to nocturnality and prey capture

483 (Garamszegi et al. 2002). In troodontids,Draft the proportionately large orbit and optic lobes of the

484 brain may reflect a similar relationship.

485

486 Efficient eater: implications for metabolic processes

487 Given the above features—large brain, large eyes and binocular vision, dexterous

488 forelimbs, powerful and agile hindlimbs—Russell (1969) posits an active, mobile lifestyle for

489 troodontids, which would have required a greater metabolism than the “reptilian” condition. Egg

490 Mountain regurgitalites support these claims, in addition to histological analyses (Varricchio

491 1993) and reproductive traits (Varricchio and Jackson 2004; see above). In a broader

492 evolutionary context, the ability of the large-bodied, non-volant T. formosus to regurgitate gastric

493 pellets supports the hypothesis that avian-style regurgitation may have evolved within non-avian

494 dinosaurs as a means to increase digestive efficiency and accommodate increased physiological

495 processes in groups closely related to modern birds, rather than as a mechanism directly related

496 to flight (O’Connor et al. 2019; O’Connor and Zhou 2019). As such, in addition to nesting and

21 © The Author(s) or their Institution(s) Canadian Journal of Earth Sciences Page 22 of 65

497 incubating behaviors, a homeothermic metabolism approaching the avian condition may have

498 been beneficial for T. formosus feeding ecology as well.

499

500 Summary of troodontid feeding ecology

501 More than fifty years since their publication, Russell’s (1969; Russell and Séguin 1982)

502 inferences of Late Cretaceous troodontid predatory ecology largely hold true. Mammal-bearing

503 regurgitalites from the Egg Mountain locality of the Two Medicine Formation are potentially

504 attributable to T. formosus (Freimuth 2020; Freimuth et al. in press), and together with additional

505 taphonomic (Ryan et al. 1998) and morphological evidence (Fowler et al. 2011; Torices et al.

506 2018) suggest a diet of primarily small, and in some instances, mammalian prey, first suggested

507 by Russell (1969). Egg Mountain regurgitalitesDraft closely resemble prey remains in gastric pellets

508 of modern diurnal raptors and may suggest a similar prey processing style, either with the hands

509 or feet, supporting Russell’s (1969) original anatomical observations. Combined, these features

510 suggest an active lifestyle for troodontids (Russell 1969), and the ability to regurgitate

511 indigestible prey may increase digestive efficiency to accommodate an enhanced, near avian-

512 grade metabolism (O’Connor and Zhou 2019). The integration of feeding trace fossils with

513 modern morphological analyses support Russell’s (1969) original work and ground future studies

514 regarding T. formosus and other theropod feeding behavior and ecology.

515

516

517 Intelligence and tool use

518 Intelligence is a difficult attribute to measure in animals, but even rough estimates can be

519 useful for interpreting behavior and ecology. Calculation of encephalization quotients (EQ) has

22 © The Author(s) or their Institution(s) Page 23 of 65 Canadian Journal of Earth Sciences

520 become a standard metric for approximating animal intelligence. EQ is a value derived by

521 comparing an animal’s actual brain mass to a hypothetical brain mass predicted by its body mass

522 (Jerison 1973, 1985). Animals with higher EQs have higher actual brain mass than predicted

523 brain mass, and theoretically this extra brain mass corresponds to greater intelligence. Brain

524 mass can be derived from brain volume at a 1:1 ratio (historically 9:10, see below), and brain

525 volume can often be reliably estimated from endocasts—physical or digital (Iwaniuk and Nelson

526 2002; Early et al. 2020). The EQ of Russell’s troodontid is calculated at 0.24-0.34 (1969;

527 Hopson 1980; Russell and Séguin 1982) using Jerison’s (1973) general relationship, a range that

528 indicates fairly high intelligence from a reptilian perspective but low from a mammalian one.

529 Currie and Zhao (1993) reexamine a troodontid EQ using measurements from a more complete

530 braincase (Table 1). Their reconstructedDraft endocast provides additional useful details, including

531 several major nerve locations and evidence for enlarged floccular lobes. They arrive at a brain

532 volume of 45 cm3, with a mass of 41 g using the older 9:10 mass to volume ratio (resulting in an

533 EQ of 0.27 with Jerison’s general relationship). This 41 g mass is used in subsequent studies

534 (Hurlburt 1996; Hurlburt et al. 2013), however it has not been appropriately updated to reflect

535 more current brain mass estimates and EQ formulas. Hurlburt (1996) calculates a significant list

536 of fossil animal EQs and also proposes several new EQ formulas to more accurately reflect EQs

537 for reptiles, birds, and various extinct fauna. His research makes a compelling case for

538 comparing theropod EQs along an avian curve (BEQ) instead of a mammalian (MEQ) or

539 reptilian (REQ) one. This new equation returns an EQ of 0.630 (Hurlburt 1996) for the Troodon

540 formosus braincase described by Currie and Zhao (1993).

541 However, it should be noted that Hurlburt (1996) mistakenly cites 41 cm3 as the volume

542 of the troodontid brain. Currie and Zhao considered the mass of the brain to be 90% of the

543 volume, but more recent EQ calculations consider the volume and brain mass to be identical

23 © The Author(s) or their Institution(s) Canadian Journal of Earth Sciences Page 24 of 65

544 (Hurlburt 1996; Hurlburt et al. 2013). Hurlburt (1996) makes this correction for many taxa but

545 misses the distinction in T. formosus. Therefore, the mass of the troodontid brain ought to be

546 considered 45 g, since 45 cm3 is the original volume cited (Currie and Zhao 1993). Furthermore,

547 as stated by Currie and Zhao (1993), this volume is quite conservative considering that the

548 floccular lobes are excluded and part of the braincase shows noticeable crushing. Still, 45 g is

549 close to Russell’s (1969) initial brain volume estimates from specimen Canadian Museum of

550 Nature (CMN) 12340, the type for L. mcmasterae. When an updated brain mass and avian

551 formula are used to recalculate the EQ of Russell’s troodontid, the range is approximately 0.64-

552 0.80. The lower end of the EQ range was calculated assuming a body mass of 60 kg (using

553 methods described by Campione et al. 2014, eq 7) and the upper end a body mass of 41 kg

554 (according to Anderson et al. 1985, eq 9).Draft Russell (1969) suggests that the troodontid’s brain was

555 perhaps comparable to that of extant ratites. Hurlburt’s (1996) research supports this hypothesis

556 as his calculated troodontid EQ exceeded that of all tested large ratites except for Darwin’s rhea

557 (Rhea pennata).

558 Most current dinosaur body mass estimates require a femoral circumference (Anderson et

559 al. 1985; Campione et al. 2014), and since EQ calculations require a body mass then an

560 appropriate specimen for EQ analysis must include material that can provide approximations of

561 both brain mass and femoral circumference. In the case of Currie and Zhao (1993) the troodontid

562 braincase does not have an associated femur, and so their EQ relies on body mass derived from

563 other sources. The calculation is still valuable but should be considered cautiously due to the lack

564 of association. However, even with appropriately associated material EQ estimates can vary

565 enormously. Dinosaur body mass assessments are heavily dependent upon the method used for

24 © The Author(s) or their Institution(s) Page 25 of 65 Canadian Journal of Earth Sciences

566 calculation. Table 2 shows several troodontid EQ solutions that vary based on class curve and

567 mass calculation.

568 Hurlburt et al. (2013, table 6.3) compare the EQ of several small theropod dinosaurs

569 including Currie and Zhao’s (1993) troodontid. The BEQs of an Ornithomimus (0.739) and

570 Bambiraptor (0.669) both surpass that of the troodontid. However, using the corrected troodontid

571 brain mass of 45 g, from Currie and Zhao (1993), results in a troodontid EQ of 0.69, slightly

572 above that of Bambiraptor. A juvenile Bambiraptor, with a comparatively staggering 1.263

573 BEQ, is also included. This example serves to illustrate why adult specimens are preferable for

574 the consistent and accurate EQ results, although some solutions to ontogenetic mass

575 discrepancies can be solved through the use of developmental mass extrapolation (examples

576 shown in Erickson and Tumanova 2000Draft as well as Brassey et al. 2015). The high end of the

577 corrected BEQ range for Russell’s troodontid, 0.80, puts the troodontid Latenivenatrix

578 mcmasterae (specimen CMN 12340) as the highest calculated adult EQ to date for any non-avian

579 dinosaur. Although Russell’s troodontid has not yet been dethroned as the record non-avian

580 dinosaur EQ, a prediction from Russell and Séguin (1982), its EQ is not bizarrely high among

581 small theropod dinosaurs (Russell and Séguin 1982; Hurlburt et al. 2013).

582 Despite its popularity, the accuracy of EQ as a measurement of cognitive ability among

583 extant animals is debated. For some groups total brain size appears to better track cognitive

584 ability than EQ (Deaner et al. 2007). Additionally, raw neuron count seems to correlate strongly

585 with cognitive ability (Herculano-Houzel 2017) and may be a better indicator of overall

586 intelligence. Olkowicz et al. (2016) show that bird brains, despite their relatively small size, are

587 extremely neuron dense, with avian forebrains having neuron counts comparable to many

588 primates. Recent experimentation with ravens (Corvus corax) suggests they have advanced

589 physical and social cognitive skills, on par with great apes (Pika et al. 2020). Other research

25 © The Author(s) or their Institution(s) Canadian Journal of Earth Sciences Page 26 of 65

590 demonstrates that carrion crows (Corvus corone) exhibit sensory consciousness (Nieder et al.

591 2020), a feature previously reserved for the mammalian cerebral cortex—primates in particular.

592 These advances in avian neurology and cognition indicate that bird intelligence may

593 generally be underestimated when inferred via EQ. Hurlburt’s (1996) revised EQ formulas work

594 to correct this, but bird intelligence estimations by this method are still problematic. Relatedly,

595 troodontids might have been even more intelligent than Russell predicted given what we now

596 know about neuronal organization in avian brains (Olkowicz et al. 2016; Herculano-Houzel

597 2017) and troodontids’ phylogenetic proximity to birds. Although many similarities exist

598 between avian and non-avian maniraptoran brains (Larsson et al. 2000; Balanoff et al. 2013;

599 2014; Gaetano et al. 2017) it is difficult to parse through analogy and homology. Additionally, it

600 is still unknown whether or not maniraptoranDraft dinosaur brains had avian-like neuronal

601 organization, but perhaps continuing advancement in avian paleoneurology (Knoll and Kawabe

602 2020) will elucidate the issue. Although neuron counts and behavioral tests may be better than

603 EQ as indicators of animal intelligence (Herculano-Houzel 2017), they are difficult to apply to

604 paleontological specimens and EQ is likely to remain the preferred method for now. Even though

605 EQs are highly dependent on derivation methods, they are still useful for comparison if

606 calculated in the same manner.

607 Russell (1981) discusses the expensive nature of encephalization and suggests that large

608 brains are best supported by predatory, endothermic organisms. Because of the raw caloric

609 requirements of high encephalization, it seems infeasible to maintain such a costly organ with a

610 reptilian metabolism (Russell 1981). Contrary to longstanding prior opinion, and hypothesized

611 by Béland and Russell (1979), current research shows that many non-avian dinosaurs were likely

612 endothermic, theropods in particular (Barrick and Showers 1994; Fricke and Rogers 2000; Amiot

613 et al. 2006; Eagle et al. 2011; Dawson et al. 2020). Body temperatures for oviraptorosaurs, a

26 © The Author(s) or their Institution(s) Page 27 of 65 Canadian Journal of Earth Sciences

614 group closely related to troodontids, are estimated at 35-40°C (Amiot et al. 2017). Both

615 phylogenetic and histological evidence (Varricchio 1993), indicates that T. formosus was

616 probably endothermic as well. However, body temperatures remain unknown, with recent

617 research showing a possible range from 28-38°C (Dawson et al. 2020). Regardless of the exact

618 body temperature, troodontid metabolism would most likely map better with warm-bloodedness

619 than cold-bloodedness. This endothermic interpretation of troodontids fits with Russell’s

620 suggested requirements for encephalized, intelligent life.

621 Animal intelligence may also be deduced through observation. Tool use is commonly

622 thought to be a behavioral indicator of relatively high animal intelligence, though the relationship

623 is complicated and not entirely predictive (Hansell 2000; Emery and Clayton 2009). Russell and

624 Séguin (1982) make several mentions ofDraft tool use, though only in regard to the hypothetical

625 dinosauroid. This behavior is depicted as an adaptation that could take place along the

626 evolutionary trajectory to a more ape-like form. Russell and Séguin (1982) propose that the

627 upright posture of the dinosauroid would allow it to make use of tools, but it has since been

628 observed that a humanoid bauplan is unnecessary for the competent manipulation of tools.

629 Although originally associated with primates, tool use is documented among a wide variety of

630 animals including elephants (Chevalier-Skolnikoff and Liska 1993; Hart et al. 2001) dolphins

631 (Smolker et al. 1997; Krützen et al. 2005), fish (Jones et al. 2011; Bernardi 2012; Harborne and

632 Tholan 2016), octopus (Finn et al. 2009), birds (Lefebvre et al. 2002), and even crocodilians

633 (Dinets et al. 2013). These last two are particularly striking since, as noted by Dinets et al.

634 (2013), they phylogenetically bracket dinosaurs.

635 What qualifies as tool use in the animal world is heavily debated. In general, tool use

636 occurs when an animal employs an object from its environment to alter the state of another

637 object or organism to the animal’s benefit (Shumaker et al. 2011). However, there is not

27 © The Author(s) or their Institution(s) Canadian Journal of Earth Sciences Page 28 of 65

638 consensus on any one definition. Some disagreement involves intent, replicability, and the nature

639 of the purported tool, such as whether or not a tool must be detached from the environment. A

640 bird dropping a rock on a shelled food item would be tool use, but how about a bird dropping a

641 shelled food item onto a hard surface? Some authors differentiate between true tools and proto-

642 tools (Parker and Gibson 1977), and Lefebvre et al. (2002) investigate accounts of both true and

643 proto-tool use in birds. Their results indicate that, in general, true tool users have proportionally

644 larger brains than those that use proto-tools. Furthermore, their work suggests that tool use has

645 evolved independently many times in Aves, seemingly accompanying encephalization (Lefebvre

646 et al. 2002).

647 Hansell (2000) suggests that researchers are perhaps overly fascinated with tool use as an

648 indication of animal intelligence. He pointsDraft out that bird nests are often arbitrarily excluded

649 when discussing animal tools, though they fit most definitions of tool use. Nests may be

650 excluded due to their presumed genetically programmed origin, ubiquity, or the fact that they

651 adhere to a substrate of some sort. Nevertheless, nests illustrate birds’ great manipulative

652 capacity. Also, if nest-building can be explained by genetic programming, then why not tool use

653 too? Hansell (2000, p. 92) worries that human obsession with tool-use may be “wilful

654 anthropomorphism,” and insists that it is birds’ manipulative skills and capacity to learn that are

655 remarkable, not necessarily that these are used to employ tools. Nevertheless, tool use remains

656 popular as a marker of possible animal intelligence and is likely an indicator that will be used for

657 years to come.

658

659 Avian tool use

660 Lefebvre et al. (2002) document tool use in over a hundred species of birds, indicating

661 that the behavior is far more widespread than previously believed. The authors mention that tool

28 © The Author(s) or their Institution(s) Page 29 of 65 Canadian Journal of Earth Sciences

662 use was only ascribed to a single avian species in the 1960s (Thomson 1964), the woodpecker

663 finch (Camarhynchus pallidus). The woodpecker finch is still famous for its tool-tuned foraging

664 behavior, and studies have since focused on how the behavior is learned (Tebbich et al. 2001;

665 Tebbich et al. 2012), specific problem-solving capabilities (Tebbich and Bshary 2004), and tool

666 selection using unfamiliar materials (Sabine et al. 2012). Corvids, now celebrities of avian

667 intelligence, have also become well known for tool use. They have been observed physically

668 altering objects to create more suitable tools for complex problem-solving (Hunt 1996), and even

669 performing comparable to great apes on abstract planning tasks that necessitate tool use

670 (Kabadayi and Osvath 2017). Parrots are similarly known for their intelligence and have been

671 observed using tools on numerous occasions (Borsari and Ottoni 2005; Auersperg et al. 2011;

672 Lambert et al. 2015). Additionally, researchDraft shows that some birds can easily learn to use tools

673 even if the behavior does not naturally occur in the wild (van Horik and Emery 2016). This

674 suggests that tool use is not always simply genetic and that it can be driven by experience and

675 intelligence, perhaps emerging from encephalization as suggested by Lefebvre et al. (2002).

676 Although the woodpecker finch, corvids, and parrots are well known, many other birds make use

677 of a diverse array of tools. Some examples include baiting prey (Ardeola, Butorides, Ceryle,

678 Eurypya, Larus, Milvus), using rocks to break open or acquire food sources (Corvus,

679 Hamirostra, Neophron, Numenius), using grass to extract termites (Bradornis), and even using

680 various materials to sponge up water for effective liquid transport (Ciconia, Cyanocitta,

681 Euphagus) (Lefebvre et al. 2002).

682

683 Crocodilian tool use

684 Some crocodilians have been recorded exhibiting behaviors that were previously

685 associated with mostly endothermic tetrapods. This includes cooperative hunting (Dinets 2015)

29 © The Author(s) or their Institution(s) Canadian Journal of Earth Sciences Page 30 of 65

686 and possible tool use (Dinets et al. 2013). For the latter, Mugger crocodiles (Crocodylus

687 palustris) and American alligators (Alligator mississippiensis) are reported to balance sticks on

688 their face and snout as lures in an effort to capture prey (Dinets et al. 2013). Stick-displaying is

689 systematically examined in American alligators (Dinets et al. 2013), and the behavior is thought

690 to specifically attract birds seeking out nesting materials. When the birds get close to the

691 displayed sticks, the alligators attempt to attack them. Furthermore, this stick-displaying

692 appeared to coincide with the nest building season in nearby rookeries (Dinets et al. 2013).

693 The positioning and use of environmental assets as lures to capture prey would fall into

694 the category of true tool use, but there is debate over the intentionality and exhibition of the

695 behavior. Rosenblatt and Johnson (2020) reexamine tool use in American alligators using

696 controlled experiments and captive specimens.Draft They introduced sticks into alligator ponds at

697 several sites, some near active rookeries. Stick-displaying increased universally, and stick-

698 displaying lasting more than 10 minutes was only seen at sites with rookeries. However, outside

699 of these long displays the behavior was actually more common at sites without a nearby rookery.

700 The authors acknowledge the significance of the longer episodes of stick-displaying but conclude

701 that ultimately their evidence suggests the behavior is more random than intentional and that

702 alligators generally did not alter their behavior to include more stick-displaying depending on the

703 environment. Although Rosenblatt and Johnson’s (2020) test did not support alligators’ ability to

704 engage in spontaneous tool use, it seems unlikely that an alligator would display open-ended

705 problem-solving skills similar to its more encephalized avian relatives.

706

707 Tool use in non-avian dinosaurs?

30 © The Author(s) or their Institution(s) Page 31 of 65 Canadian Journal of Earth Sciences

708 Tool use in extinct fauna is rarely discussed outside the realm of human ancestors. Nevertheless,

709 due to widespread tool use in modern animals outside of primates it seems possible that extinct

710 fauna could have displayed similar behaviors. Unfortunately, convincing description of such

711 tools could be extremely problematic.

712 No dinosaurian tools have been described from the fossil record, and it would be quite

713 difficult to do so. However, given the variety of modern tool users and dinosaurs’ 160 Ma reign,

714 vast diversity, and phylogenetic bracketing of modern tool users it seems likely that some non-

715 avian dinosaurs would have employed tools. Russell and Séguin (1982) do not mention tool use

716 with regards to their described troodontid, but it is considered along with the dinosauroid. There

717 seems to be an assumption that tools would have been manipulated with the dinosauroid’s hands.

718 Due to the bipedal nature of most theropodDraft dinosaurs, it is tempting to speculate on how they

719 may have employed their freed-up forelimbs.

720 Although the vast majority of known theropod dinosaurs were bipedal, their forelimb

721 capabilities are still unclear. Birds, the most common modern bipedal organisms, have forelimbs

722 largely dedicated to flight. While there are a significant number of modern flightless bipeds, their

723 forelimb morphology still differs greatly from non-avian theropods. Nicholls and Russell (1985)

724 provide a detailed comparison of Struthiomimus altus forelimbs and pectoral girdle to those of

725 several modern animals. Their work shows that S. altus appeared to have great forereach and a

726 substantial range of motion, quite similar to chameleons (Chamaeleonidae). Chameleons, though

727 quadrupedal, have pectoral and forelimb anatomy which, in many ways, mirrors that of theropod

728 dinosaurs (Peterson 1973; Bakker 1975; Nicholls and Russell 1985). The combination of reach

729 and range could have made maniraptoran forelimbs well suited for object manipulation.

730 More recently, Philip Senter has led a variety of analyses investigating dinosaurian

731 forelimbs with regard to range of motion and possible behavior (Senter 2005; Senter and Robins

31 © The Author(s) or their Institution(s) Canadian Journal of Earth Sciences Page 32 of 65

732 2005; Senter 2006a; Senter 2006b; Senter and Sullivan 2019). These tests serve as important

733 anchors for interpreting theropod forelimb use, especially considering the dearth of appropriate

734 modern comparisons. This research has not covered troodontids specifically, but it has included

735 several members of Dromaeosauridae (Senter 2006a). Anatomical investigation reveals that

736 Bambiraptor and Deinonychus forelimbs had considerable range of motion, especially compared

737 to larger theropods. These dinosaurs were likely able to bring an object from their forelimbs to

738 their mouths, could clutch an object between their hands (fingers or palms), and could hold an

739 object to their chest. Additionally, Senter (2006a) reconstructs Bambiraptor with opposable

740 digits, similar to how Russell and Séguin (1982) reconstruct T. formosus. Hypothesized

741 opposable digits in theropods have been around for at least a century (Osborn 1916). Dinosaurs

742 with opposable digits may have been ableDraft to precisely manipulate objects, perhaps even for tool

743 use. However, while the Bambiraptor reconstruction remains plausible, Osborn’s hypothesis of

744 opposable S. altus digits has been refuted (Ostrom 1969; Nicholls and Russell 1985). Similarly,

745 the opposability of T. formosus digits appears questionable. Russell and Dong (1993) describe a

746 troodontid that definitively lacks opposable digits, and its manus morphology closely matches

747 that of Russell’s troodontid.

748 Senter (2006a) points out that, given the presence and orientation of forelimb feathers, it

749 may have been difficult for a maniraptoran to use its hands to interact with objects on the ground.

750 Since it seems that the hand could not pronate through wrist movement, the forelimb feathers

751 might contact the ground first and hinder attempts to grasp objects. Still, it is possible that the

752 hand could pronate through arm movement thus allowing for a grasping surface that is parallel

753 with the ground. Finally, even if grabbing an object on the ground was problematic, conceivably

754 it could first be plucked from the ground by mouth before being transferred to the hands.

32 © The Author(s) or their Institution(s) Page 33 of 65 Canadian Journal of Earth Sciences

755 Potentially some theropod dinosaur could have manipulated a tool using its forelimbs,

756 but fixation on handheld tools may be overly anthropocentric. In extant fauna, tool use does not

757 necessitate specialized morphology. As discussed above, the behavior extends across groups and

758 anatomies. Dexterous hands, while useful, are not necessary for competent object manipulation.

759 A tool-wielding theropod might have used its mouth or feet for manipulation, just as modern

760 birds do. Figure 4 illustrates some speculative methods of theropod tool use. Russell and Séguin

761 (1982) reserved tool use for the dinosauroid, but the troodontid they describe might have been a

762 perfectly competent tool user without any further modifications.

763

764 Tools and traces

765 A fossilized tool, being an interactionDraft of an organism on its environment, would be

766 considered a trace fossil itself. However, identifying such an object in the fossil record would be

767 immensely challenging. Many modern birds do not markedly modify their tools, they select

768 objects that are already of the desired form (Lefebvre et al. 2002). Even discarded tools that had

769 been modified would be troublesome to recognize in the modern world, and identification of

770 fossilized examples is even more daunting. Some of the most advanced tool use by modern day

771 animals can be seen among the spear-wielding chimpanzees of Senegal (Pruetz and Bertolani

772 2007). Perhaps this is the sort of tool Russell and Séguin (1982) envision for the dinosauroid,

773 tools that “obviate the need for bodily armament (p 27).” Even these manufactured tools, as

774 impressive as they are, would be difficult to identify among other fallen or broken branches. The

775 sticks can be identified as spears mostly because researchers witnessed them being crafted and

776 employed by chimpanzees.

777 If an isolated stick or stone tool would be problematic to identify, evidence of tool use

778 might also be preserved as a more classic trace fossil, i.e., marks in substrate. An animal using a

33 © The Author(s) or their Institution(s) Canadian Journal of Earth Sciences Page 34 of 65

779 tool might inflict a trace upon its environment or prey. Traces left by animal tools have not been

780 well described, and a better understanding would aid in the identification of similar marks in the

781 fossil record. However, paleontologists could potentially benefit from familiarizing themselves

782 with the research of their archaeologist kin. Humans have left an extensive record of traces,

783 many specific to tool use. For instance, mammoth remains have been uncovered with wounds

784 and marks inflicted by tools (Nikolskiy and Pitulko 2013; Pitulko et al. 2016; Wojtal et al. 2019).

785 Tool-wielding dinosaurs seems like something off the shelves of science-fiction, indeed

786 Diane Carey and James Kirkland’s Star Trek First Frontier (1995) depicts an Earth ruled by

787 highly intelligent dinosaurs. Stephen Baxter’s 2003 novel Evolution even describes a

788 hypothetical group of tool-using Cretaceous troodontids. However speculative it may seem,

789 given current knowledge dinosaur tool useDraft seems to be within the realm of possibility. Short of a

790 spectacularly obvious discovery (skewered prey item, clutched object among articulated skeletal

791 elements, distinctly altered rock), evidence will be tough to extract from the fossil record.

792 Although troodontids never physically evolved to be like Russell and Séguin’s (1982)

793 dinosauroid, perhaps they still could have exhibited increased intelligence or tool use.

794

795 Conclusions

796 • Troodon likely constructed its earthen nest in the same manner employed by ratites and

797 other birds to create their scrapes through backward kicks of the hindlimb. However, the

798 architecture of the egg clutch is more difficult to explain, but likely required dexterous,

799 manual manipulation of the eggs.

800 • Functionally, the reproductive traces indicate iterative laying of two eggs and brooding,

801 consistent with elevated body temperatures and a metabolic output that approaches but

34 © The Author(s) or their Institution(s) Page 35 of 65 Canadian Journal of Earth Sciences

802 does not equal that of modern birds. Brooding a clutch of eggs to hatching would require

803 a very high energy investment from the adult.

804 • Two regurgitalites from the Egg Mountain locality of Montana are represented by multi-

805 individual, crania-dominated specimens, primarily of the marsupialiform Alphadon

806 halleyi. Abundant nesting evidence and shed teeth at the locality favor Troodon formosus

807 as the responsible predator.

808 • Combined with recent morphological (Fowler et al. 2011; Torices et al. 2018) and

809 taphonomic studies (Ryan et al. 1998), these regurgitalites corroborate hypotheses first

810 broached by Russell (1969; Russell and Séguin 1982) of a preference for small

811 mammalian prey, potential manual and pedal functionality in predation and feeding, and

812 an active, possibly nocturnal, predatoryDraft ecology for Late Cretaceous troodontids.

813 • Reproductive and feeding traces from the Two Medicine Formation of Montana

814 corroborate a number of the hypotheses of Russell (1969) and Russell and Séguin (1982)

815 for troodontids such as a more avian-like level of intelligence, high metabolism with

816 potential endothermy, excellent vision with stereoscopic and nocturnal capabilities, a

817 mobile lower arm with some grasping capabilities, and predation upon small crepuscular

818 to nocturnal mammals (Fig. 1).

819 • Tool use is widespread among modern birds (Lefebvre et al. 2002) and occurs even in

820 some crocodilians (Dinets et al. 2013). It does not require a humanoid or dinosauroid

821 bauplan and the archosaurian phylogenetic bracketing suggests a reasonable possibility of

822 this behavior occurring in at least a few non-avian dinosaurs.

823 • Small theropod dinosaurs, like Troodon formousus and Latenivenatrix mcmasterae, had

824 fairly high EQs with perhaps avian levels of intelligence. But the functional capabilities

35 © The Author(s) or their Institution(s) Canadian Journal of Earth Sciences Page 36 of 65

825 of their forelimbs has yet to be examined from an anatomical or biomechanical

826 perspective and whether any troodontid used tools remains an interesting but highly

827 speculative question at this time.

828 • Given the limited modification made to tools by modern vertebrates (Lefebvre et al.

829 2002), recognition of one in the fossil record would likely be very challenging. But

830 conceivably, a tool or tool originated mark could one day be found in the Mesozoic fossil

831 record.

832

833 Acknowledgements 834 We thank Dale Russell for his scientificDraft contributions, inspiration, and generous 835 personality. We thank the organizers of this special volume for considering our submission and

836 our hopefully not too random discussion as well as the Museum of the Rockies, Beatrice R.

837 Taylor Paleontological Resource Area, Jack Horner, and John Scannella for permission and

838 support to excavate Egg Mountain. Thanks also A. van der Reest and D. Evans for their helpful

839 reviews.

840

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1279

1280 Figure 1. Russell’s troodontid predictions. Russell’s hypotheses for Laurasian Late

1281 Cretaceous troodontids included A) a brain with an avian level of intelligence and organization

1282 requiring a high metabolism with potentiallyDraft endothermy (Béland and Russell 1979), B)

1283 excellent vision with stereoscopic and nocturnal capabilities, C) mobile lower arm, D) an

1284 opposable and grasping manual digit III providing manual dexterity, E) rapid and agile gait, F)

1285 occupation of terrestrial environments distal from depositional centers, and G) predation upon

1286 small crepuscular to nocturnal mammals. Brain reconstruction (A) adapted from Currie and Zhao

1287 (1993, fig. 3).

1288

1289 Figure 2. Reproductive nesting traces for Troodon formosus including the nesting trace as

1290 photographed at an earlier (A), then later (B) stage of excavation and egg clutch, MOR 963 (C).

1291 The egg clutch, still largely covered with a mudstone, is represented by the oval area at the

1292 center of the nest in A and by the white plaster jacket in B. Comparable areas in A and B are

1293 marked by t for a portion of the rim truncated by earlier excavation and k for the knob-like

1294 termination of the rim and the other side. Mudstone (ms) still covers a portion of the rim in A.

1295 (C) Egg clutch MOR 963 in dorsolateral view showing the near upright position of the eggs

1296 within the sediments. Clutch contains 24 eggs in total. (D) Behavioral interpretation of the

1297 nesting and clutch traces showing an adult T. formosus in brooding posture. Illustration by D.

1298 Anduza. Scale bars are 20 cm in A, B, and D and 10 cm in C.

1299

1300 Figure 3. Visual summary of regurgitalites from the Egg Mountain locality with comparison to

1301 modern diurnal raptor gastric pellets. (A) MOR 10912, regurgitalite consisting of three Alphadon

1302 halleyi represented largely by cranial elements and broken, digested postcrania. (B) MOR 10913,

1303 regurgitalite including ten A. halleyi and an indeterminate lizard, also represented

1304 disproportionately by broken cranial elements. (C–E) A. halleyi in regurgitalites share many

1305 features with prey items in extant diurnalDraft raptor gastric pellets, including high relative abundance

1306 of crania compared to postcrania (C), extensive breakage (D), and observable digestive corrosion

1307 (E). These features are in part product of prey processing in modern raptors, and T. formosus

1308 may have fed similarly. Relative abundance of (C) compiled from Andrews (1990) and Montalvo

1309 and Fernández (2019) (Freimuth 2020; Freimuth et al. in press); extant mouse opossum

1310 (Thylamys pallidior) maxilla (D) from Fernández et al. (2012); extant mouse (Mus spretus) ulna

1311 (E) from Souttou et al. (2012). (D–E) not to scale.

1312 1313 1314 Figure 4 - Examples of tool use have been observed among both modern archosaur groups that

1315 bracket non-avian dinosaurs (A). This, coupled with the repeated evolution and sheer abundance

1316 of tool users in Aves, might suggest that some non-avian dinosaurs were also capable of wielding

1317 tools. Modern birds tend to interact with objects using their feet or mouths, but some small

1318 theropods appear to have had forelimbs suitable for grasping and manipulation. (B) Depiction of

1319 speculative methods of theropod tool use. They may have used their mouths (I), as seen in the

1320 woodpecker finch and several modern corvids. Alternatively, an object might have been

1321 manipulated using their feet (II), although perhaps theropod feet may have been ill-suited for the

1322 task. Lastly, due to their bipedal nature, it is intriguing to consider how a theropod may have

1323 used its hands for tool use (III). Bambiraptor has been reconstructed with an opposable digit.

1324 Perhaps some dinosaurs employed opposable digits for precise object manipulation or tool use.

1325 Research by Senter (2006a) suggests that some maniraptorans would have had difficulty holding

1326 an object in a curled grip due to finger flexion putting insufficient pressure on the palm. The size

1327 of the object would be a significant consideration for this grip. Senter (2006a) also shows that

1328 grasping an object between two hands, against either the fingers or palms, would have been

1329 possible as well.

1330 Draft

1331 Table 1. Troodon formosus (upper) and Latenivenatrix mcmasterae (lower) specimens discussed

1332 in this paper.

1333 1334 1335 Table 2. Troodontid EQ results for specimens described by Russell (1969) and Currie and Zhao

1336 (1993). EQ varies depending on estimated body mass and chosen class curve. Class curves were

1337 created by Hurlburt (1996) to better approximate EQs of non-mammalian animals, especially

1338 extinct taxa. Since Russell’s troodontid had both braincase and femoral specimens, the EQ is

1339 fairly accurate for the individual. The estimated brain volume was 49 cm3, which corresponds to

1340 a mass of about 49 g (updated from Russell’s 45 g value). Body mass estimates were based on a

1341 femoral circumference of 96 mm (CMN 12340). The higher body mass was retrieved using

1342 methods described by Campione et al. (2014, eq 7) while the lower mass with methods from

1343 Anderson et al. (1985, eq 9). Currie and Zhao’s troodontid specimen had a well-preserved

1344 braincase (volume at least 45 cm3), but no associated femur. Since Anderson et al. (1985)

1345 provided a popular mass estimation technique for the time, the mass suggested by Currie and

1346 Zhao is used as the low metric. A proportionally higher mass (as one that might be returned

1347 using methods from Campione et al. if a femur were available) was used for comparison. EQs

1348 derived from the bird class curve are likely the most appropriate (Hurlburt 1996; Hurlburt et al.

1349 2013) and are bolded for emphasis.

1350 1351

1352

Draft

Figure 1. Russell’s troodontid predictions. Russell’s hypotheses for Laurasian Late Cretaceous troodontids included A) a brain with an avian level of intelligence and organization requiring a high metabolism with potentially endothermy (Béland and Russell 1979), B) excellent vision with stereoscopic and nocturnal capabilities, C) mobile lower arm, D) an opposable and grasping manual digit III providing manual dexterity, E) rapid and agile gait, F) occupation of terrestrial environments distal from depositional centers, and G) predation upon small crepuscular to nocturnal mammals. Brain reconstruction (A) adapted from Currie and Zhao (1993, fig. 3).

181x134mm (300 x 300 DPI)

Draft

Figure 2. Reproductive nesting traces for Troodon formosus including the nesting trace as photographed at an earlier (A), then later (B) stage of excavation and egg clutch, MOR 963 (C). The egg clutch, still largely covered with a mudstone, is represented by the oval area at the center of the nest in A and by the white plaster jacket in B. Comparable areas in A and B are marked by t for a portion of the rim truncated by earlier excavation and k for the knob-like termination of the rim and the other side. Mudstone (ms) still covers a portion of the rim in A. (C) Egg clutch MOR 963 in dorsolateral view showing the near upright position of the eggs within the sediments. Clutch contains 24 eggs in total. (D) Behavioral interpretation of the nesting and clutch traces showing an adult T. formosus in brooding posture. Illustration by D. Anduza. Scale bars are 20 cm in A, B, and D and 10 cm in C.

181x126mm (300 x 300 DPI)

Draft Figure 3. Visual summary of regurgitalites from the Egg Mountain locality with comparison to modern diurnal raptor gastric pellets. (A) MOR 10912, regurgitalite consisting of three Alphadon halleyi represented largely by cranial elements and broken, digested postcrania. (B) MOR 10913, regurgitalite including ten A. halleyi and an indeterminate lizard, also represented disproportionately by broken cranial elements. (C–E) A. halleyi in regurgitalites share many features with prey items in extant diurnal raptor gastric pellets, including high relative abundance of crania compared to postcrania (C), extensive breakage (D), and observable digestive corrosion (E). These features are in part product of prey processing in modern raptors, and T. formosus may have fed similarly. Relative abundance of (C) compiled from Andrews (1990) and Montalvo and Fernández (2019) (Freimuth 2020; Freimuth et al. in press); extant mouse opossum (Thylamys pallidior) maxilla (D) from Fernández et al. (2012); extant mouse (Mus spretus) ulna (E) from Souttou et al. (2012). (D–E) not to scale.

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Figure 4 - Examples of tool use have been observed among both modern archosaur groups that bracket non-avian dinosaurs (A). This, coupled with the repeated evolution and sheer abundance of tool users in Aves, might suggest that some non-avian dinosaurs were also capable of wielding tools. Modern birds tend to interact with objects using their feet or mouths,Draft but some small theropods appear to have had forelimbs suitable for grasping and manipulation. (B) Depiction of speculative methods of theropod tool use. They may have used their mouths (I), as seen in the woodpecker finch and several modern corvids. Alternatively, an object might have been manipulated using their feet (II), although perhaps theropod feet may have been ill-suited for the task. Lastly, due to their bipedal nature, it is intriguing to consider how a theropod may have used its hands for tool use (III). Bambiraptor has been reconstructed with an opposable digit. Perhaps some dinosaurs employed opposable digits for precise object manipulation or tool use. Research by Senter (2006a) suggests that some maniraptorans would have had difficulty holding an object in a curled grip due to finger flexion putting insufficient pressure on the palm. The size of the object would be a significant consideration for this grip. Senter (2006a) also shows that grasping an object between two hands, against either the fingers or palms, would have been possible as well.

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Table 1. Troodon formosus (upper) and Latenivenatrix mcmasterae (lower) specimens discussed in this paper.

Femur Formation, Body-Mass Specimen Length, Specimen Geographic Locality Estimates Reference no. Circumference Location (kg) (mm)

Two Medicine, Egg Mountain Varricchio et MOR 363 egg clutch - - Montana TM-006 al. 1997

clutch and Two Medicine, Egg Mountain Varricchio et MOR 963 - - nest Montana TM-006 al. 1999 small Two Medicine, Egg Mountain 2.41,1.72, MOR 430 126, 30 - juvenile Montana TM-006 3.03

large Two Medicine, 12.91, 9.02, MOR 563 - 230*, 55 - juvenile Montana 18.03 1 48.5 , adult with Two Medicine, MOR 748 - 320, 89 52.62, - eggs Montana 48.5**

formosus Two Medicine, Jack’s Varricchio MOR 553 bonebed - - T. MontanaDraft Birthday Site 1995 MOR Two Medicine, Egg Mountain Freimuth et al. regurgitalite - - 10912 Montana TM-006 in review

MOR Two Medicine, Egg Mountain Freimuth et al. regurgitalite - - 10913 Montana TM-006 in review

Currie and

Zhao 1993; RTMP Dinosaur Dinosaur braincase - - van der Reest 86.36.457 Park, Alberta Provincial and Currie Park 2017

RTMP Dinosaur Red Deer Currie and skull roof - - 79.8.1 Park, Alberta River Zhao 1993 Russell 1969; CMN Dinosaur Red Deer van der Reest adult ??, 96 601 12340 Park, Alberta River and Currie L. mcmasterae 2017

1 Body-mass estimate using Campione et al. (2014, eq 7). 2 Body-mass estimate using Anderson et al. (1985, eq 9). 3Body-mass estimate using DME (Erickson and Tumanova 2000). *length estimate based on comparable MOR 553 **adult body-mass estimate for DME using result of Campione et al. (2014)

Table 2. Variable troodontid encephalization quotients based on body mass and class curve.

Russell’s troodontid Currie and Zhao’s troodontid L. mcmasterae T. formosus

Mass high (60 kg) Mass low (41 kg) Mass high (66 kg) Mass low (45 kg) Reptilian EQ 7.2 8.9 6.5 7.6 Bird EQ 0.64 0.80 0.55 0.69 Mammalian EQ 0.23 0.30 0.19 0.26

Note: Troodontid EQ results for specimens described by Russell (1969) and Currie and Zhao

(1993). EQ varies depending on estimated body mass and chosen class curve. Class curves were

created by Hurlburt (1996) to better approximate EQs of non-mammalian animals, especially

extinct taxa. Since Russell’s troodontid had both braincase and femoral specimens, the EQ is fairly accurate for the individual. The estimatedDraft brain volume was 49 cm3, which corresponds to a mass of about 49 g (updated from Russell’s 45 g value). Body mass estimates were based on a

femoral circumference of 96 mm (NMC 12340). The higher body mass was retrieved using

methods described by Campione et al. (2014: eq 7) while the lower mass with methods from

Anderson et al. (1985: eq 9). Currie and Zhao’s troodontid specimen had a well preserved

braincase (volume at least 45 cm3), but no associated femur. Since Anderson et al. (1985)

provided a popular mass estimation technique for the time, the mass suggested by Currie and

Zhao is used as the low metric. A proportionally higher mass (as one that might be returned

using methods from Campione et al. if a femur were available) was used for comparison. EQs

derived from the bird class curve are likely the most appropriate (Hurlburt 1996; Hurlburt et al.

2013) and are bolded for emphasis.