Feeding behaviour and bone utilization by theropod dinosaurs

DAVID W. E. HONE AND OLIVER W. M. RAUHUT

Hone, D.W.E. & Rauhut, O.W.M. 2010: Feeding behaviour and bone utilization bytheropod dinosaurs. Lethaia, Vol. 43, pp. 232–244.

Examples of bone exploitation by carnivorous theropod dinosaurs are relatively rare,representing an apparent waste of both mineral and energetic resources. A review of theknown incidences and possible ecological implications of theropod bone use concludesthat there is currently no definitive evidence supporting the regular deliberate ingestionof bone by these predators. However, further investigation is required as the small bonesof juvenile dinosaurs missing from the fossil record may be absent as a result of thero-pods preferentially hunting and consuming juveniles. We discuss implications for bothhunting and feeding in theropods based on the existing data. We conclude that, likemodern predators, theropods preferentially hunted and ate juvenile animals leading tothe absence of small, and especially young, dinosaurs in the fossil record. The traditionalview of large theropods hunting the adults of large or giant dinosaur species is thereforeconsidered unlikely and such events rare. h Behaviour, carnivory, palaeoecology, preda-tion, resource utilization.

David W. E. Hone [dhone@ivpp.ac.cn], Institute of Vertebrate Paleontology & Paleoanthro-pology, Xhizhimenwai Dajie 142, Beijing 100044, China; Oliver W. M. Rauhut[o.rauhut@lrz.uni-muenchen.de], Bayerische Staatssammlung fur Palaontologie und Geolo-gie and Department fur Geo- und Umweltwissenschaften, Ludwig-Maximilians-UniversitatMunich, Richard-Wagner-Str. 10, 80333 Munich, Germany; manuscript received on18 ⁄ 01 ⁄ 2009; manuscript accepted on 20 ⁄ 05 ⁄ 2009.

Tetrapod bone can provide an important source ofessential elements, such as calcium, phosphorus andpotassium, and sustenance (due to their fat, bloodand bone marrow content, Haynes 1980; Kardong2002) for a predatory animal. Extant carnivorousmammals exploit bone extensively, even in situationswhere the prey item is large and provides energy-richmuscle and organ tissue (e.g. elephants, buffalo,Haynes 1980). Large- and small-bodied opportunistsconsume available bones (e.g. hyenas and jackals), asdo primary carnivores (e.g. felids and hunting dogs,van Valkenburgh 1996). Extant crocodiles (Fisher1981; Naju & Blumenschine 2006) and birds (Dodson& Wexler 1979) also regularly consume the bones oftheir prey.

Given both their large body sizes (up to 14 m inlength and 6–7 tonnes in weight) and hypercarnivo-rous habits (Holtz & Osmolska 2004), it might beexpected that at least some non-avian theropod dino-saurs would have actively utilized prey, or scavenged,bone. However, direct evidence for predator-damagedbones in the dinosaur fossil record is rare and suchremains occur less frequently than in the mammalrecord (Fiorillo 1991). Moreover, most examples oftheropod predation damage appear to represent acci-dental contact between teeth and bone rather thandeliberate attempts to consume bone. Recovereddinosaur bones rarely exhibit the modifications associ-ated with osteophagy in extant taxa (Chure et al.

2000): for example, they generally lack the spiral frac-tures, splintered long bones and deep tooth puncturemarks that result from the attentions of living bone-eating taxa. This lack of evidence leads to the surpris-ing conclusion that theropods either did not utilizebone in their diets or consumed bones and left nodirect evidence of this behaviour (perhaps due tosome feature of their digestive physiology; Mellett1983).

Here, we intend to re-assess the evidence for osteo-phagy in non-avian carnivorous theropod dinosaursand explore the possible ecological implications of thisinferred behaviour (or lack thereof). Multiple lines ofevidence are available, but, although most of thesehave been discussed separately with regard to thero-pods, they have not been evaluated collectively. Directevidence is available from predator-damaged bones,preserved stomach contents and coprolites. Indirectevidence from craniodental morphology and theinferred ecology of theropod dinosaurs also contrib-utes to our picture of theropod diets. Comparisonswith extant analogues, including birds, crocodiliansand mammals, are informative and help to constrainspeculation on the digestive and functional morpho-logical repertoires of their extinct relatives (the ExtantPhylogenetic Bracket, Witmer 1995). We have focusedon those theropods thought to have a strictly carnivo-rous diet: several theropod clades, such as Ornithomi-mosauria and Therizinosauroidea, were probably not

10.1111/j.1502-3931.2009.00187.x � 2009 The Authors, Journal compilation � 2009 The Lethaia Foundation

primarily carnivorous (Kobayashi and Lu 2003; Bar-rett 2005) and are therefore excluded fromconsideration.

Tyrannosaurs – the exceptions thatprove the rule?

Tyrannosaurs deserve special mention in any paperdealing with theropod osteophagy. Large tyrannosaurs(e.g. Tyrannosaurus, Albertosaurus and Daspletosaurus)have repeatedly been interpreted as the only non-aviantheropods capable of damaging large prey bones onthe basis of direct evidence (tooth puncture marks, Er-ickson & Olson 1996), the gross morphology of theskull and post-cranium (Holtz 2004), biomechanicalanalyses of cranial strength and biting performance(Rayfield 2004) and direct evidence of bone consump-tion from coprolites (Chin 1997).

Throughout this paper, reference is made to largetheropods. These often include animals of similar sizeto tyrannosaurs (e.g. Carcharodontosaurus, Saurophag-anax, Ceratosaurus) and some might have actuallybeen significantly larger (e.g. Giganotosaurus, Spino-saurus; see Dal Sasso et al. 2005). Size is therefore nota key component of bone crushing (although largebones can still be exploited by large animals by swal-lowing them whole) and instead we must focus on theapparent numerous adaptations of tyrannosaurs forbone crushing (Barrett & Rayfield 2006). However,the capability to damage and bite through boneshould not be considered synonymous with the actualactivity of consuming bone for nutritional reasons(i.e. ability does not necessarily equal behaviour).Bone may be consumed simply because it is easierthan not doing so (i.e. an inability to separate bonefrom flesh on a carcass) or it may be consumed acci-dentally (e.g. when biting off the distal part of the tail).However, it is probably impossible to distinguishamong these potential behavioural aspects of boneconsumption and so instead we will focus on the con-sumption of bone by tyrannosaurids based on theirapparent ability to crush and break even large bonesor bone complexes (e.g. the sacrum; see Erickson &Olson 1996).

Direct evidence – bone modification

Bones that exhibit damage resulting from tooth–bonecontact represent the primary evidence for osteo-phagy. Such damage is relatively easy to distinguishfrom ‘trample’ marks, transport-induced breaks andother taphonomic alterations (Fiorillo 1987).

Theropod feeding traces typically consist of eithertooth scratches on the bone surface (produced as theteeth are drawn across a bone to deflesh it or toremove the cortex) or puncture wounds (resultingfrom teeth piercing and entering the cortex). Thelength, depth and spacing of scratches can be used toattribute the marks to a potential trace maker (e.g.Chure et al. 2000). Similarly, the outlines of puncturewounds, or casts of moulds taken from within thewounds, reveal the dental morphology of the predatorand thereby provide information on its identity (e.g.Erickson & Olson 1996; Carpenter et al. 2005; Fig. 1).

The rarity of bones that display obvious damageinflicted by theropod teeth implies that theropodswere not habitually osteophagous (Chure et al. 2000).Known examples (Table 1) typically consist of one ormore scratch marks or puncture wounds on a singleelement of a particular prey item. This observationalso suggests that the few feeding traces available areprimarily accidental in nature, with the predator ⁄ scav-enger biting bone while feeding on the surroundingtissue or attempting to dismember the carcass. This ishighlighted by the fact that most predator damageconsists of scratches (created by tearing and pulling)rather than punctures (created by impact). Evenwhere conspicuous puncture wounds are present, theyusually represent isolated bites, rather than a patternconsistent with repeated feeding activity across anentire specimen (Jacobsen 1998). One exception tothis is a Triceratops pelvis that bears numerous punc-ture wounds, presumably from the same attacker,which was most probably a Tyrannosaurus (Fig. 1,Table 1).

Studies on the occurrence of predator-damagedbones within accumulations, such as species-specific

Fig. 1. Triceratops sacrum with bite marks (black arrows) attrib-uted to Tyrannosaurus. The lower right section has actually beenbitten off. Moulds taken from the scores and punctures replicatethe teeth of Tyrannosaurus (Erickson & Olson 1996). Image: copy-right G.M. Erickson.

LETHAIA 43 (2010) Theropod feeding behaviour 233

bone beds, suggest that while feeding traces are notcommon, they may be more frequent than generallyrealized. In some accumulations, approximately 4% ofthe elements have been modified by predators (Fioril-lo 1991). A similar figure was obtained from a surveyof multiple neoceratopsian bonebeds and up to 14%of bones are damaged in some hadrosaur accumula-tions (Jacobsen 1998). However, this last figure mayhave been inflated artificially by the presence of largetyrannosaurs inflicting more damage than would benormal compared with other large theropod commu-nities (see below). The relative proportion of damagedbones seems to be higher in isolated bones than inmass assemblages (Fiorillo 1991). Mass death eventsmay have isolated and buried the carcasses and thusprevented scavenging, or alternatively with the largenumber of bodies available, scavengers may have beencapable of preferentially consuming meat and thusavoiding bones.

Broken, gnawed and tooth-marked bones are com-mon in the mammalian fossil and sub-fossil record(Haynes 1980) suggesting common bone feedingbehaviour; in fact, it is noticeable higher than seen fordinosaurs (Farlow 1976). Clearly, if this behaviour wasfrequent among theropods, it would be recorded withfar greater frequency than is observed in extant mam-malian predators (Carlson & Pickering 2003) andcrocodiles (Naju & Blumenschine 2006). On the basisof direct bite-mark evidence, it can be concluded thattheropods (with the possible exception of the largertyrannosaurs) did not deliberately attack and consumebone (although the pattern may be obscured, seeErickson & Olson 1996).

Feeding apparatus

It has been suggested that the skulls and teeth oftheropods were poorly adapted for trituration or

crushing of bone and that the lack of evidence for os-teophagy reflects the inability of these animals to pro-cess this food source (Fiorillo 1991). Theropods couldnot chew bones in a conventional mammalian man-ner with lateral jaw movements (although this is lim-ited in many carnivores) but could presumably biterepeatedly on a bone in the jaws if they wished. Thebone fragments seen in the coprolite referred to atyrannosaur suggest the possibility of very high levelsof oral processing (Andrews & Fernandez-Jalvo 1998)giving credibility to this interpretation (in tyranno-saurs at least). Clearly, theropods could also drag theirteeth across bones without sustaining injury or dam-age to the teeth and this could be done repeatedly toweaken or damage bones (e.g. as with the Camarasau-rus ilium, see Chure et al. 2000). However, apart fromoccasional scrape marks on bones there is no directevidence for either of these behaviours.

Smaller bones (e.g. distal caudal vertebrae and pha-langes) could probably have been swallowed whole bymany theropods. Some medium-sized bones (e.g. ver-tebrae and ribs) could be bitten through or at leasthave parts removed relatively easily (e.g. neuralarches) by large theropods. Even those genera that donot appear to be well adapted to biting on bone couldprobably have broken a neural spine that was only afew millimetres thick.

It has been suggested that the feeding strategy oftheropods involved careful avoidance of any tooth–bone contact (Chure et al. 2000) and may have beenaimed at avoiding damage to the teeth. Teeth in mosttheropods probably represented important tools forprey capture as well as feeding, and thus significantdamage or loss might have severely impeded theirsurvival. While this may well have been true for smalltheropods with fine, fragile teeth (e.g. dromaeosaurids)and these could also be more delicate in theirfeeding on larger bones, it seems doubtful for thelarger carnivores. Even so, there are scrape marks and

Table 1. Examples of notable injuries to dinosaur and other archosaur remains attributable to theropod dinosaurs.

Description Attributed bite maker Source

Triceratops pelvis exhibiting multiple tooth punctures Tyrannosaurus Erickson & Olson (1996)Bitten off horn and scratch marks in a Triceratops skull Tyrannosaurus Happ (2008)Healed bite mark on Edmontosaurus neural spine Tyrannosaurus Carpenter (2000)Allosaurus pubic boot with one side bitten through Torvosaurus or Ceratosaurus Chure et al. (2000)Stegosaurus cervical plate that has been bitten through Allosaurus Carpenter et al. (2005)Camarasaurus ilium showing tooth drag marks Allosaurus Chure et al. (2000)Hypacrosaurus fibula with a tooth embedded in it Tyrannosaurus Chin (1997)Edmontosaurus phalanx with tooth punctures Tyrannosaurus Erickson & Olson (1996)Damaged Apatosaurus bones Allosaurus Matthew (1908)Various damaged sauropod bones (including long bones, sacra, etc.) Various large Jurassic theropods Hunt et al. (1994)Various dinosaur bones including sauropods and Majungasaurus Majungasaurus Rogers et al. (2004)Teeth scratch and puncture marks on skulls of Sinraptor and tyrannosaurids Sinraptor and tyrannosaurids Tanke & Currie (2000)Pterosaur vertebra with tooth embedded in it Spinosaurid Buffetaut et al. (2004)Pterosaur tibia with tooth embedded in it Dromaeosaurid Currie & Jacobsen (1995)

234 D. W. E. Hone & O. W. M. Rauhut LETHAIA 43 (2010)

even a tooth embedded in bone attributable todromaeosaurid predators (Currie & Jacobsen 1995)showing that even these animals produced strongtooth–bone contacts and even broke teeth duringfeeding.

The ‘carnosaurs’ with relatively thin teeth (e.g. car-charodontosaurids) might have risked damage to theirteeth if they impacted on bone, and the slightly curvedor sinusoidal shape of their crowns (see Fig. 2) leavesthem vulnerable to bending forces during heavy com-pressive pressure compared with a straight tooth.However, these teeth were still relatively robust (com-pared with those of smaller theropods, in addition tobeing absolutely more robust), and although not mo-lariform, they are much bigger in absolute size thanthe teeth of many mammals capable of bone-crackingbehaviour. Thus, the risk is unlikely to be as high asmight otherwise be inferred compared with mammalscapable of cracking large bones. Furthermore, bitingin these animals was probably strictly orthal, in whichcase the bite force is transmitted directly from the tipof the tooth to the base, so that the lateral flattening ofthe tooth plays only a minor role. Indeed, biomechan-ical studies have shown both the ability of theropodskulls (Rayfield et al. 2001; Rayfield 2005) and teeth(Mazzetta et al. 2004) to withstand large bite forces.In addition, the constant replacement of teeth intheropods means that there is overall relatively little

harm to an individual in losing or breaking a few teethif this leads to gaining a vital meal. Even modern andrecently extinct mammals that cannot replace teethcan show high incidences of broken canines and carn-assials (van Valkenburgh 1988, 2009) that would pre-sumably have more serious consequences for themthan for a theropod that could replace its damagedteeth.

At least some large non-tyrannosaur theropodswere capable of exerting bone-crunching bites onbones (presumably without tooth damage) asobserved by the bitten-through Allosaurus pubic bootand Stegosaurus armour plate (see Table 1). There arealso records of theropods inflicting significant damageon conspecifics through cranio-facial biting behav-iours in both tyrannosaurids and allosauroids (Tanke& Currie 2000). Clearly, theropods were willing toengage in behaviour that risked damage to their ownteeth, jaws and skull in circumstances that would pre-sumably involve more risk than static feeding on acorpse.

While some theropod teeth were dislodged by bit-ing bone (e.g. Hypacrosaurus fibula with embeddedtooth, see Fig. 3), this may represent the loss of looseor old teeth in which the root was already partially orfully resorbed (wear on theropod teeth is actually notuncommon but has mainly been described for tyran-nosaurs; see Farlow & Brinkman 1994; Schubert &

Fig. 2. Theropod lateral tooth, Carcharodontosaurus sp., mid-Cretaceous, Kem Kem, Morocco; BSPG 1993 IX 1, in mesial (left), (?) lingual(middle) and distal (right) views. Note the slight sinusoidal curve of the tooth in distal view. Note the small wear facet at the tip, especiallyvisible in mesial view. Scale bar with 10- and 1-mm divisions.

LETHAIA 43 (2010) Theropod feeding behaviour 235

Ungar 2005) and is not necessarily an indication ofhabitually loosely socketed teeth in theropods. In fact,tooth roots in theropods are actually quite strong,being typically at least twice as long as the crowns andsomewhat expanded; so, the teeth were not looselyattached in a living animal (O.W.M.R., personalobservation). Tooth loss in many fossil theropodskulls is thus the result of the degradation of the softtissues holding the teeth in place after the death of theanimal, which is also seen in modern crocodiles andmany mammals (O.W.M.R., personal observation).When alive, theropod teeth were weakened in theirsockets by the development of replacement teeth andthe roots of the tooth in the mouth having alreadybeen reabsorbed and thus weakly held in the jaw, andeasily dislodged. Coyotes and foxes are capable of leav-ing gnaw marks on large Bos and Bison bones (Fiorillo1991); so, it is reasonable to expect an allosaur to becapable of grating on some large bones without losingfully functional teeth.

Teeth may also have been shed during hunting orfeeding regardless of tooth–bone contact. Once theroot has been resorbed, theropod teeth seem to beshed with remarkable ease and this may have been ahabitual (or at least very frequent) part of feeding.Shed teeth are found with great frequency and areoften unworn (Fiorillo & Currie 1994), suggesting thatthey were shed or lost without having gone throughmuch use before their replacement (or were not sub-jected to heavy wear). The classic Tenontosaurus ⁄ Dein-onychus associations (Maxwell & Ostrom 1995),amongst others (e.g. Buffetaut & Suteethorn 1989;Ryan et al. 1998), show very high numbers of shedteeth, suggesting that this was a common occurrence.A distinction should be made, however, between teeththat are being shed anyway (because it is simply theirtime to be replaced) and are shed during feeding, and

those teeth that become unusable due to extensivedamage. The implications are that teeth were not sub-jected to much wear but rather were lost regularly as aresult of feeding but without significant tooth–bonecontact. The latter is common in theropods that haveconstant tooth replacement and simply depends onreplacement rates and only secondarily on the forcesexerted on the tooth (as the root is already reabsorbedwhen they are lost). Thus, the potential loss of teethcannot account for theropods avoiding tooth–bonecontact as it is unlikely that it would have had any sig-nificant detrimental effect on the animal or its health.

Stomach contents

There are a number of well-preserved and articulatedlarge theropod specimens that are known fromaround the world (e.g. Allosaurus, Albertosaurus andTarbosaurus). It is rare for both large and small thero-pods to be preserved with bony stomach contents ofprevious meals, although a few are known, and inthese, bones of considerably smaller prey than thepredator seem to have been swallowed whole (e.g.Baryonyx, Compsognathus and Sinosauropteryx). Sometyrannosaurids have been found with juvenile orni-thischians as part of the stomach contents (Varricchio2001) and bone was found in coprolites attributed totyrannosaurs (Chin 1997, and see below). Therefore, iftheropods were regularly consuming large pieces ofbone, one would expect to find many more specimens(especially the tyrannosaurs) with preserved bonemass in their chest cavities.

In large living crocodiles at least (that habituallyconsume large quantities of unprocessed bone), theeffect of stomach acids is such that no recognizablebone fragments are passed from the body (Andrews &

Fig. 3. A partial Hypacrosaurus fibula (MOR 549) in lateral view (left) and in cross-section (right). It shows a deep tooth score mark (left,indicated by white arrow) and an embedded partial tyrannosaur tooth (right, indicated by white arrow). Scale bar is 10 mm. For details, seeChin (1997).

236 D. W. E. Hone & O. W. M. Rauhut LETHAIA 43 (2010)

Fernandez-Jalvo 1998). This is also true of some otherectothermic animals, such as large amphibians(Mellett 1983). Even if consumed bones weresubjected to considerable oral processing and weremaintained in the high-acid environment of the stom-ach for extended periods of time, one would expect tosee some bone preserved occasionally when an animaldied soon after feeding before the process of digestionhad acted fully on the consumed bone. Even a largetyrannosaurs feeding on the bones of a juvenile animal(with probably incomplete ossification) with extensiveoral processing and a long digestion time (againassumed based on the size of the animal) identifiablepieces can be identified from the coprolites resultingfrom this; so, stomach contents should be recoveredon occasion, especially for individually large bones orbone pieces if ingested. The quality of preservation ofsome complete specimens is such that even small bonefragments in the stomach should be recovered occa-sionally.

However, even in largely articulated specimens, theribcage is often broken open and prey bone fragmentsmight have been scattered outside the ribcage. Thus,they may simply have gone unnoticed or unreportedin the past as unrecognizable and undiagnostic bonefragments, if collected at all, are often not studied inany detail during the study of a fossil. Intensive searchfor acid-etched or tooth-marked bone fragments inmuseum collections of material excavated at theropodsites might thus reveal additional evidence for boneconsumption by theropods, but such a survey isbeyond the scope of this paper.

The abilities of birds (Dodson & Wexler 1979;Housten & Copsey 1994), crocodiles (Fisher 1981)and large varanids that can digest heavy bone loadseffectively (Auffenberg 1981) suggest that if theropodswere consuming very large amounts of bone, or verylarge pieces of bones, then some should still survivelong enough to be found in stomach contents (asindeed they survive to be recovered in coprolites atleast on some occasions). In crocodiles, little survivesthe digestive process and even enamel can be strippedfrom teeth, although bones and bone fragments canbe passed out in faeces (Fisher 1981). Crocodiles typi-cally break bones prior to ingestion, including thosethat are not ultimately consumed (Naju & Blumens-chine 2006) a process that leaves distinctive marks,which cannot be confused with mammalian bite andbreak traces (Naju & Blumenschine 2006). In birds,little is known outside of studies of owls, which habit-ually consume small mammals whole and then regur-gitate undigested material. Nevertheless, they arecapable of digesting more than 50% of the bones con-sumed (Dodson & Wexler 1979) and this points to astrong digestion despite minimal oral processing and

reduced time in the digestive tract. A similar figure of50% for bone digestion was also found for thebearded vulture after consuming ribs from largemammals without any form of mechanical processing(Housten & Copsey 1994).

In the theropod Baryonyx stomach contentsincluded scales attributed to the fish Lepidotes (Charig& Milner 1997), which have a very thick layer of gano-in and should thus be very resistant to acid wear.These scales, however, show serious acid damage(P.M. Barrett, personal communication), and thisprovides evidence that theropods had very acidicstomach environments. Large theropods would havehad long digestion times due to the length of theirgut, and there is evidence that at least in the stomachthere was a highly destructive acid environment (Chinet al. 1998; Varricchio 2001). While this might permitthem to digest large pieces of bone effectively, thepresence of fragments of bones from juvenile animalsin the coprolites of even the largest tyrannosaurs(Chin et al. 1998; Varricchio 2001) suggest thatcomplete elimination of large bones would be verydifficult.

Coprolites

If theropods were consuming bone regularly, theircoprolites should be common (Bradley 1946), butinstead they are rare (Chin 1997), although this is trueof coprolites of terrestrial vertebrates in general. Thelow number of theropod coprolites could be a resultof unfavourable conditions for preservation, behavio-ural factors (e.g. defecation in water) or they may behard to diagnose, with or without high bone content.However, the basic observation is that theropod copr-olites of any kind are rare. Coprolites attributable toherbivores are also infrequent and, although thesewould be far less favoured for preservation over amineral-rich bone-based coprolite, the sheer size andnumber of herbivorous dinosaurs should producemany more coprolites than are currently known.Thus, the apparent rarity of theropod coprolites maysimply be due to preservational or collection bias andshould be considered as equivocal evidence withrespect to bone consumption by theropods. Further-more, as with crocodiles (see above) consumed bonemay simply have been degraded and digested to thepoint where even bone fragments are absent from fae-ces (which seems unlikely as discussed above),although the additional minerals should still be pres-ent which would enhance the chances of preservation.

Overall, the lack of any form of bone fragments inthe stomach contents of well-preserved specimens (seeabove), the rarity of coprolites, and the presence of

LETHAIA 43 (2010) Theropod feeding behaviour 237

fragments of bones from juveniles in the few copro-lites suggest three possible explanations:

1. theropods selectively consumed meat and werecareful to avoid any contact with bones duringfeeding;

2. theropods habitually consumed medium- or evenlarge-sized bones (with or without oral processing)and these were rapidly and totally digested andthus left no traces; or

3. theropods consumed only small bones (in com-parison with the predator’s body size; e.g. fromjuvenile animals, which would also be less mineral-ized) and these were digested fully leaving little orno trace.

Each explanation has arguments in its favour asdescribed above, but only the third alternative hasgood supporting evidence from the fossil record(stomach contents and coprolites contain the remainsof juveniles, not adults). Furthermore, the first andsecond alternatives both conflict with available evi-dence – there are signs of damage on fossil bones fromfeeding, suggesting that tooth–bone contact was notavoided, and while admittedly negative evidence, thereis no suggestion of large quantities of partly digestedbones from adults known in either stomach contentsor coprolites.

Discussion

The fundamental conclusion of the above review isthat although the apparent extent of bone exploitationby large theropods remains low, its true extentremains unknown. However, we are still in a positionto make a number of predictions about both huntingand feeding behaviours based on the available evi-dence, and comparisons with extant taxa, both withinthe extant phylogenetic bracket and with other large-bodied carnivores. Future analyses or discoveries maytip the balance towards or away from bone use, andthis will favour one or the other of the following pre-dictions which may then become open to further test-ing and analysis.

Feeding habits

Although their gross morphology is unlike anythingalive today, one can assume that theropods hunted ina broadly similar manner to modern predators. Preywould have been pursued until it was tired and ⁄ orinjured through numerous small wounds, or wouldhave suffered a devastating injury through a singlewound inflicted from an ambush (McDonald 1994).

The large size and presumed relatively slow speed ofmany adult dinosaurian herbivores would have madea mammalian style ‘pursuit and trip’ exceptionally dif-ficult for theropods to perform, although it remains apossible tactic for animals hunting smaller ornitho-pods or juveniles. (A ‘trip’ approach would be prob-lematic against large and heavy prey, and it would bedifficult for a bipedal theropod to try and trip a qua-drupedal prey species with a relatively higher instabil-ity of the former when trying to perform such amanoeuvre, and large graviportal quadrupeds wouldbe hard to trip). In large theropods, the risk of injury(e.g. Farlow et al. 1995) and relatively slow maximumspeeds (e.g. Hutchinson & Garcia 2002) make anambush tactic most likely, in which a crippling bite isinflicted after a short run. Such a behavioural patternhas already been proposed by Paul (1987) and Molnar& Farlow (1990), and is consistent with skull biome-chanics (Rayfield et al. 2001; Rayfield 2004) and thelittle direct evidence there is for predatory behaviour(Carpenter 2000). Although there is some evidence forfrontal encounters between tyrannosaurids and cera-topsians (Happ 2008), this was probably the exceptionrather than the rule (see also Holtz 2008).

Both modern predators and scavengers eat quicklyas they risk being displaced from the kill by largercompetitors or groups of competitors. Only some sol-itary cats (e.g. tigers and leopards) that can removethe kill to a place of safety have the luxury of time toprocess the food without any form of competition(from other species or conspecifics). Even pack hunt-ers will face competition for food from other groupmembers despite tight social hierarchies.

This is an important point as an animal which israpidly trying to consume as much food as possiblein the shortest time is unlikely to show a delicatetouch in avoiding contacting bone with its teeth (themore delicate felids still break their teeth duringhunting or feeding; van Valkenburgh 2009). This isespecially so with theropods, which do not have therange of motion in the jaw (especially laterally) thatmammals can demonstrate, nor the specialized carn-assials of most carnivorans for processing meat.Therefore, unless large amounts of meat were ordi-narily available for theropods, or their overall popula-tion density was very low, it is very unlikely thattheropods could have afforded to have been fussy eat-ers and taken extreme care to avoid biting on bonewhile feeding on the surrounding tissue. Bite marks,while rare, show that tooth–bone contact did occurand we do see some relatively robust bones bittenthrough at least on occasion (see Table 1). The objec-tive of a carnivore or scavenger at a kill is generally toconsume the maximum amount of food in the short-est possible time.

238 D. W. E. Hone & O. W. M. Rauhut LETHAIA 43 (2010)

However, this assumes that theropods were bring-ing down prey, which represented a significant frac-tion of their mass (i.e. greater than half). Most adultherbivorous dinosaurs were of similar or substantiallygreater mass than individual theropods that probablypreyed on them. In the case of diplodocoid sauropodsfor example, if a small pack of allosauroids killed anadult, the latter would probably weigh more than thewhole group combined. In this case, there would be avery large quantity of meat available, and avoidingbone would neither be particularly difficult, nor costlyin terms of time or effort. This scenario, despite itsaesthetic appeal is, however, unlikely. Theropodswould almost certainly have avoided healthy adultscompletely and instead targeted easier prey – juveniles(Farlow & Holtz 2002; see also Hummel & Clauss2008).

While there is, of course, significant variation pres-ent in extant organisms, few modern predators makeactive selection of prey that is potentially difficult ordangerous to handle. Predators select for the young,the old and the weak or injured (Palmqvist et al.1996), or at least their presence greatly enhances theability of predators to hunt successfully (Temple1987). Modern and recent mammalian predators(Kruger et al. 1999; Husseman et al. 2003; Steele2004) and birds (Donazar & Ceballos 1989; Boshoffet al. 1994; Rohner & Krebs 1996) certainly preferthese kinds of sub-optimal fitness prey. Small prey ofa given species is also typically preferred over largerindividuals by such diverse predators as leopards(Hayward et al. 2006), hunting dogs (Fuller & Kat1993), bluefish (Scharf et al. 1998) and several inverte-brates (Barbeau & Scheibling 1994) or simply smallprey in general (e.g. Webb et al. 1991; Gotmark &Post 1996; Turesson et al. 2002).

The huge infant mortality seen in almost all verte-brate taxa (as described above) would also suggest thatthis is indeed normal for just about all predator ⁄ preysystems that have been studied. The requirements ofgrowth in juveniles and their inexperience at foragingnecessitates that they forage for longer periods (Carey& Moore 1986; Marchetti & Price 1989; Weathers &Sullivan 1989; Arenz & Leger 2000) and it has beenshown in a variety of vertebrate taxa that foragingmakes individuals more vulnerable to predation (Ca-rey & Moore 1986; Krause & Godin 1996), and thatpredators will preferentially attack foraging or unwaryprey (Krause & Godin 1996), thus making juveniles apreferred target of predators for multiple overlappingreasons. Finally, learned anti-predator responses arecommon in vertebrates after predatory encounters(Fuiman 1993; Kelley & Magurran 2003; Quinn &Cresswell 2004), which highlights the vulnerability ofjuveniles which are naive with respect to predators.

(Note that the citations above are limited by the nat-ure of laboratory studies, which tend to focus on smallspecies and especially fish, and wild studies that tendto focus on birds).

Active predators are vulnerable to starvation follow-ing an injury and will not pursue a prey individual (orspecies) that is easily capable of escaping the predatoror causing it serious injury if an easier alternative isavailable. Given the large size of adult dinosaurs andtheir apparent longevity, there may have been a strongnumerical and therefore biomass bias towards healthyadults in a dinosaurian population (Paul 1994; Erick-son et al. 2001; Hummel & Clauss 2008). However,specimens of young dinosaurs are notably rare exceptin mass death assemblages (Richmond 1965). This isnot likely to be a size or collection bias as many largedinosaur-bearing formations are replete with bones ofsmall tetrapods (pterosaurs, crocodilians, squamates,etc.), yet juvenile remains are still rare. Furthermore,although juvenile bones are less mineralized andtherefore less likely to fossilize, some very young dino-saurs and embryos are known from nests (Carpenter1999) suggesting that their rarity cannot entirely beexplained by this factor and that they may genuinelybe rare. Other biases may exist (juveniles may avoidareas favourable to preservation or suffer fromdestruction or damage during sorting) and ultimatelythese may be hard, if not impossible, to separate fromselective feeding by theropods (and clearly both maybe important factors).

The obvious conclusion is that like vertebratestoday, many juvenile dinosaurs, without the protec-tion of large size, adults, herds and ⁄ or experience,were especially vulnerable to predation by theropods.If we assume that juvenile dinosaurs were vulnerablein the same way for the same reason, this may explainthe apparent creche behaviour of some dinosaur spe-cies (Zhao et al. 2007; Varricchio et al. 2008) evenwhere adults are thought to be solitary (Mathews et al.2009) as a way of providing the natural protection ofa group, reducing the change of a given individualbeing attacked and providing additional animals tolook for danger.

Dinosaurs tended to lay eggs in large numbers rela-tive to their body size (Janis & Carrano 1992; Paul1994) and thus produced large numbers of offspring,yet the adult populations of many dinosaurs wouldhave been limited due to their large size (e.g. Burnesset al. 2001), indicating very high rates of infant mor-tality. Modern tetrapods also reflect this pattern ofpopulation structure with large numbers of veryyoung juveniles (i.e. between 1 and 2 years of age),low numbers of more mature juveniles and subadultsand then a large standing population of adults. Thejuvenile part of this population is, of course, transient

LETHAIA 43 (2010) Theropod feeding behaviour 239

as they age and become subadults and adults and arereplaced by new births. The subadult population islow and thus despite the high number of births, fewjuveniles make it to subadulthood or adulthood –juveniles obviously suffer from very high mortalityrates, and this is especially as a result of predation (e.g.see Anders et al. 1997). This pattern has been shownin animals as diverse as lions (Creel & Creel 1997),passerines (Sullivan 1989), various African herbivores(Galliard et al. 1998), seals (Baker & Thompson2007), and crocodiles (Webb et al. 2000) and so it canbe concluded that theropods habitually ate juveniledinosaurs and that this is at least partly reflected inthe fossil record. It has already been noted that at leastsome herbivores suffered very high juvenile mortalityas deduced from their population structure of massmortality events (e.g. Varricchio et al. 2008 and refer-ences therein).

In those K-selected taxa (e.g. elephants) with a lowbirth rate, long development times and a high invest-ment in offspring (typically large-bodied taxa) juvenilemortality is obviously lower. However, dinosaurs wereboth large and r-selected as egg layers (Janis & Carr-ano 1992; Paul 1994) and parental care would havebeen limited beyond the nest (Horner 2002). Certainlysome dinosaurs hatched precocial young (Horner2002). Thus, dinosaurs, despite the large size of manyspecies, would have contributed very large numbers ofjuveniles to the population providing prey for popula-tions of very large theropods at a rate beyond that seenin comparable faunas consisting of large mammals.Indeed, r-strategy in combination with large adult sizemight have been one of the secrets of the success ofdinosaurs (Janis & Carrano 1992).

As juveniles had both smaller bones (in terms ofabsolute size) and these were probably weaker (lessossified, and not fused at, e.g. the sacrum and neuralarches) their bones would have been far easier fortheropods to both bite and consume. They would alsohave been easier to digest, and probably left less tracesin the stomach contents or coprolites due to the lowermineral content and lower absolute volume of bone,and they would have been easier to break up duringfeeding than large adult bones. Therefore, betweenpreferential feeding on juveniles and their increasedability to both consume and digest bones of juveniles,theropods were perhaps capable of preventing the vastmajority of juvenile dinosaurs from entering in thefossil record just as is seen in modern vertebrates. Thismay also explain the apparent unwillingness of thero-pods to exploit large bones of killed or scavengedadult carcasses: there would have been sufficient bonein their diets already from juveniles consumed whole,and the opportunity to feed on large adults may havegenerally been a relatively rare event.

The little direct evidence there is from stomach orcoprolite contents is consistent with this idea. Thesmall theropods Compsognathus and Sinosauropteryxare known with remains of much smaller prey itemsin their stomach region, which were obviously swal-lowed whole, including the bones. Concerning largetheropods, remains of a juvenile Iguanodon have beenfound in the rib cage of the type specimen of Baryonyx(Charig & Milner 1997). The fact that bones of allregions of the skeleton were found (see Charig & Mil-ner 1997, appendix B) indicates that most of the preywas probably swallowed whole. Likewise, Varricchio(2001) reported remains of a juvenile hadrosaur asstomach contents of a Daspletosaurus, and boneremains of juvenile dinosaurs were also found in acoprolite attributed to Tyrannosaurus (Chin et al.1998). Thus, there is some direct evidence that smallor juvenile animals might have constituted an impor-tant part of a theropod’s diet. If these smaller preyitems were swallowed whole or in larger chunks, littletooth-inflicted damage to bone would be expected.This does not necessarily mean that bone might nothave been physically damaged prior to digestion, asthere is some evidence for the presence of a musculargizzard in theropods (Varricchio 2001), and stomachstones were reported in at least one large theropoddinosaur (Mateus 1998).

Smaller theropods (or juveniles of large species)would have been unable to kill large adult prey speciesbut, by scavenging on the kills made by larger preda-tors, would presumably attempt to exploit any avail-able nutrition and thus leave traces of their activitieson fossil bones (as with Fiorillo 1991). As previouslysuggested, juvenile theropods might have had dietscompletely different from those of adults and couldhave fed on even smaller, non-dinosaurian prey oreven insects as a form of niche partitioning such as ispracticed by crocodiles (Tucker et al. 1996). However,small bones could be consumed whole and small indi-viduals could be more delicate in their feeding actionsand may simply have lacked the jaw power, or toothstrength to tackle bones and so no marks would be left(and small animals would simply not be capable oftackling large bones). Most, if not all, traces are attrib-uted to larger (and presumably) adult theropods, butno analysis has yet attempted to correlate bone markswith likely trace maker size.

This does not rule out attacks by theropods on largeadult animals. There are at least some records of theseattacks having occurred (e.g. Carpenter 2000; Happ2008), although we maintain that these would be rare.These attacks could have been made by young andinexperienced theropods themselves and may not berepresentative of ‘normal’ adult predation behaviour.This is supported by the fact that both of these

240 D. W. E. Hone & O. W. M. Rauhut LETHAIA 43 (2010)

reported instances were obviously unsuccessful, as thebite marks show signs of healing, despite the injuriesreceived by the victims. The very fact that unsuccessfulattacks occur on adults may thus reflect that adultswere a difficult animal to attack relative to juveniles(though age or illness would have made even largeadults a target for predators).

Future research

While this paper is intended as a review of the avail-able evidence and the theoretical implications of the-ropod feeding behaviour, the possibilities for testingthese ideas should at least be discussed here. Testingthe possible extent of theropod bone use is difficult –as described above there are numerous plausible fac-tors or combinations of factors that can explain bothheavy and light bone exploitation by theropods basedon the limited evidence available. The completedestruction of bone through oral processing andstomach acids may mean that theropods habituallyexploited some bone but left little or no trace of hav-ing done so. Equally, however, the lack or traces mayresult from a simple lack of use, or from theropodslacking access to the majority of skeletons recovered ifthey were buried before scavenging could occur.

As mentioned above, a possible test of the idea thattheropods consumed but not necessarily broke boneprior to consumption (although possibly through theuse of a gastric mill after ingestion) might be a carefulsurvey of unidentifiable bone fragments found in asso-ciation with skeletal remains of theropod dinosaurs,and including careful searches for acid-etched bonewhen excavating or preparing theropod dinosaurspecimens. Even in less-than-perfect conditions, itmight thus be possible to tell just a fragmented boneof the specimen at hand from a possible partiallydigested bone by looking for traces of chemicaldecomposition due to stomach acids (e.g. Charig &Milner 1997; Varricchio 2001). Further study of signsof stomach acids on bone in recent predators wouldbe very helpful in order to provide a series of compari-sons.

Another, related test would be to determine iftheropods exploited only small bones, i.e. if they con-sumed those small enough to swallow with minimalor no oral processing. This is difficult to determine asfew fossil specimens would be suitable for analysis,and maximal bone size to be swallowed whole, ofcourse, depends on the size of the predator. In mostcases, it would be virtually impossible to tell theabsence of small bones due to predation from theabsence due to taphonomic processes, such as hydrau-lic sorting or preferential preservation of large ele-ments. Complete, articulated specimens that were

presumably buried soon after death and not subjectedto any form of feeding must be excluded. Those ani-mals (apparently) buried as a result of flooding orsimilar ‘instant’ mortality situations must also be dis-regarded – completely disarticulated specimens orthose with much missing cannot be assessed withoutthe assumption that small missing parts are a result oftaphonomy or mechanical action on the carcass beforeburial ⁄ preservation (and or subsequent erosion).Poorly preserved fossil bone will also be hard to assessfor possible damage. Mass mortality graves are alsounsuitable as these would either have not been avail-able for predators to feed on or, if they remainedexposed before burial, have supplied so much meatthat bones could be avoided if desired. Suitable speci-mens are those that either show obvious damage orare relatively complete, articulated and well preserved.The absence of evidence is, however, not evidence ofabsence. Small bones might be consumed without anyform of oral processing, but also their small size wouldmake them prone to disarticulation during scavengingby smaller theropods, or they might not preserve at alleven if they were present. Even modern herbivoresand omnivores (including small rodents) occasionallyexploit bone for mineral content and leave observabledamage.

Even allowing for the conditions of death and bur-ial, possible damage through mechanical action, ero-sion and quality of preservation (given the very largenumber bones available), if bones were regularlyexploited by theropods of any size, there would be farmore evidence of damage to them and large bonespresent in stomach contents, or evidence of adultbones in coprolites, and perhaps far more damagedtheropod teeth known. There are large numbers oftooth-damaged bones known from the mammalianfossil record; so, despite these heavy constraints, evi-dence should be available if dinosaur bones were regu-larly used (Fiorillo 1991) and would be significantlyhigher than the current typical figures of around 5%that are observed (Jacobsen 1998).

However, analysis of multiple large bone bedsmight still reveal patterns of bone use by theropodsbeyond the base counts of bone damage by Fiorillo(1991) and others. Bones can be graded by absolutesize with the assumption that smaller bones will beexploited more easily and therefore more often thanlarger ones. Despite the possible taphonomic biasagainst smaller bones, if theropods were actively con-suming bones whole, this should be detectable bycareful statistical analyses of several localities. Environ-ments suitable for preserving small tetrapods and frag-ile bones such as skulls and gastralia should not bebiased against ribs and tarsals; so, if certain elementsare consistently underrepresented in the samples, their

LETHAIA 43 (2010) Theropod feeding behaviour 241

preferential ingestion by predators would be a proba-ble explanation. Multitaxon bonebeds might be espe-cially suited for such an analysis, as they usuallyrepresent attritional mortality rather than catastrophicdeath events and thus presumably give a variety ofpredators more opportunity to feed on the carcasses.

The theropods themselves might also provide addi-tional data. Both shed teeth and those still in place inthe jaws can be examined for wear, breakages and mi-crowear that may indicate their use on bones (as seenin carnivorans – van Valkenburgh 2009). In the jawsespecially, if theropods were attempting to breakbones, they would use the posterior teeth most oftenas this provides the best concentration of force duringbiting and thus these teeth should most often showbreaks or damage.

Conclusions

The current evidence on bone consumption by thero-pods is equivocal and no one available hypothesis canbe especially favoured. Previous analyses of tooth-marked bones strongly indicate that bone crushingand break-up was much less common in theropodsthan it is in modern mammalian and crocodilian pre-dators. However, preferential consumption of smalland ⁄ or juvenile prey and ingestion and subsequentdigestion of whole bones is consistent with the avail-able evidence and might explain the scarcity of juve-nile dinosaurs in the fossil record. Although this ideais supported by the little direct evidence there is fromstomach and coprolite contents, it should be notedthat it is currently largely based on negative evidence.Further detailed analysis of both theropod feedingmechanics and a review of possibly exploited skeletons(especially of non-adults) might yet shed light on howtheropods fed on available carcasses. Extensive work isalready being carried out on the former by severalresearch groups worldwide with impressive results,and on the basis of our interpretations here we wouldappeal to researchers to be vigilant when preparingnew theropod finds in looking for possible stomachcontents. Analyses of existing collections from dino-saur bearing horizons combined with studies of theeffects of acid on bones in extant taxa can provide cor-roborating evidence for the ideas proposed here andso, while the conclusions of this paper are somewhatequivocal, there is a strong foundation for furtherwork that can elucidate much about theropod feedingand digestion.

It must be considered a strong probability thatalthough living biomass of dinosaurs was biasedtowards large adults, juvenile animals may have beensystematically the primary prey of choice for the

majority of theropods (see Hummel & Clauss 2008).This is backed up by both the fossil record of juveniledinosaurs and the population structure of modern tet-rapods and the behaviour of predators. This factorshould be considered in subsequent analyses of dino-saurian population ecology and is an important, andso far ignored, component of hypothesized theropodhunting and feeding behaviour.

Acknowledgements. – Special thanks are due to Paul Barrett fornumerous long discussions and feedback on this manuscript, andalso Zhijie Jack Tseng for discussions on carnivoran biology andSterling Nesbitt on taphonomy. Two anonymous referees arethanked for their helpful comments, which improved the manu-script. Thanks are due to Corwin Sullivan for suggestions toimprove the manuscript and assistance in formatting the figures.We thank Greg Erickson for the photograph used in Figure 1 andChris Brochu for Figure 4. G. Janssen took the photographs forFigure 2. DWEH is funded by grants awarded to Xu Xing by theChinese Academy of Sciences and the IVPP.

References

Anders, A.D., Dearborn, D.C., Faaborg, J. & Thompson, F.R. 1997:Juvenile survival in a population of neotropical migrant birds.Conservation Biology 11, 698–707.

Andrews, P. & Fernandez-Jalvo, Y. 1998: Palaeobiology: 101 usesfor fossilized feces. Nature 393, 629–630.

Arenz, C.L. & Leger, D.W. 2000: Antipredator vigilance of juvenileand adult thirteen-lined ground squirrels and the role of nutri-tional need. Animal Behaviour 59, 535–541.

Auffenberg, W. 1981: The Behavioural Ecology of the Komodo Moni-tor, 406 pp. University Press, Gainsville.

Baker, J.D. & Thompson, P.M. 2007: Temporal and spatial varia-tion in age-specific survival rates of a long-lived mammal, theHawaiian monk seal. Proceedings of the Royal Society of London,B 274, 407–415.

Barbeau, M.A. & Scheibling, R.E. 1994: Behavioral mechanisms ofprey size selection by sea stars (Asterias vulgaris Verrill) andcrabs (Cancer irroratus Say) preying on juvenile sea scallops(Placopecten magellanicus (Gmelin)). Journal of ExperimentalMarine Biology and Ecology 180, 103–136.

Barrett, P.M. 2005: The diet of ostrich dinosaurs (Theropoda: Or-nithomimosauria). Palaeontology 48, 347–358.

Barrett, P.M. & Rayfield, E.J. 2006: Ecological and evolutionaryimplications of dinosaur feeding behaviours. Trends in Ecologyand Evolution 21, 217–224.

Boshoff, A.F., Palmer, N.G., Vernon, C.J. & Avery, G. 1994: Com-parison of the diet of crowned eagles in the Savanna and ForestBiomes of south-east South Africa. South African Journal ofWildlife Research 24, 26–31.

Bradley, W.H. 1946: Corpolites from the Bridger Formation ofWyoming: their composition and microorganisms. AmericanJournal of Science 244, 215–239.

Fig. 4. A complete theropod tooth (Tyrannosaurus rex) showingthe crown and large root. Total length of the tooth is 300 mm, ofwhich approximately 100 mm is crown and 200 mm is root. Therelative proportions are typical of theropod teeth.

242 D. W. E. Hone & O. W. M. Rauhut LETHAIA 43 (2010)

Buffetaut, E. & Suteethorn, V. 1989: A sauropod skeleton associ-ated with theropod teeth in the Upper Jurassic of Thailand:remarks on the taphonomic and palaeoecological significance ofsuch associations. Palaeogeography, Palaeoclimatology, Palaeoe-cology 73, 77–83.

Buffetaut, E., Martill, D. & Escuillie, F. 2004: Pterosaurs as part of aspinosaur diet. Nature 430, 33.

Burness, G.P., Diamond, J. & Flannery, T. 2001: Dinosaurs, drag-ons, and dwarfs: the evolution of maximal body size. Proceedingsof the National Academy of Sciences 98, 14518–14523.

Carey, H.V. & Moore, P. 1986: Foraging and predation risk in yel-low-bellied marmots. American Midland Naturalist 116, 267–275.

Carlson, K.J. & Pickering, T.R. 2003: Intrinsic qualities of primatebones as predictors of skeletal element representation in modernand fossil carnivore feeding assemblages. Journal of Human Evo-lution 44, 431–450.

Carpenter, K. 1999: Eggs, Nests and Dinosaur Babies: A Look atDinosaur Reproduction, 338 pp. Indiana University Press,Bloomington.

Carpenter, K. 2000: Evidence for predatory behavior by carnivo-rous dinosaurs. Gaia 15, 135–144.

Carpenter, K., Sanders, F., McWhinney, L. & Wood, L. 2005: Evi-dence for predator–prey relationships: example for Allosaurusand Stegosaurus. In Carpenter K. (ed.). The Carnivorous Dino-saurs, 325–350. Indiana University Press, Bloomington.

Charig, A.J. & Milner, A.C. 1997: Baryonyx walkeri, a fish-eatingdinosaur from the Wealden of Surrey. Bulletin of the NaturalHistory Museum 53, 11–70.

Chin, K. 1997: What did dinosaurs eat? Coprolites and other directevidence of dinosaur diets. In Farlow J.O. & Brett-Surman M.K.(eds): The Complete Dinosaur, 371–382. Indiana UniversityPress, Bloomington.

Chin, K., Tokaryk, T.T., Erickson, G.M. & Calk, L.C. 1998: A king-sized theropod coprolite. Nature 393, 680–682.

Chure, D.J., Fiorillo, A.R. & Jacobsen, R. 2000: Prey bone utiliza-tion by predatory dinosaurs in the Late Jurassic of North Amer-ica, with comments on prey bone use by dinosaurs throughoutthe Mesozoic. Gaia 15, 227–232.

Creel, S. & Creel, N.M. 1997: Lion density and population struc-ture in the Selous Game Reserve: evaluation of hunting quotasand offtake. African Journal of Ecology 35, 83–93.

Currie, P.J. & Jacobsen, A.R. 1995: An azhdarchid pterosaur eatenby a velociraptorine theropod. Canadian Journal of Earth Sci-ences 32, 922–925.

Dal Sasso, C., Maganuco, S. & Buffetaut, E. 2005: New informationon the skull of the enigmatic theropod Spinosaurus, withremarks on its size and affinities. Journal of Vertebrate Paleontol-ogy 25, 888–896.

Dodson, D. & Wexler, P. 1979: Taphonomic investigation of owlpellets. Palaeobiology 5, 292–296.

Donazar, J. & Ceballos, O. 1989: Selective predation by eagle owlsBubo bubo on rabbits Oryctolagus cuniculus: age and sex prefer-ences. Ornis Scandinavica 20, 117–122.

Erickson, G.M. & Olson, K.H. 1996: Bite marks attributable toTyrannosaurus rex: preliminary description and implications.Journal of Vertebrate Paleontology 16, 175178.

Erickson, G.M., Curry Rogers, K. & Yerby, S.A. 2001: Dinosauriangrowth patterns and rapid avian growth rates. Nature 412, 429–433.

Farlow, J.O. 1976: A consideration of the trophic dynamics of aLate Cretaceous large-dinosaur community (Oldman Forma-tion). Ecology 57, 841–857.

Farlow, J.O. & Brinkman, D.L. 1994: Wear surfaces on the teeth oftyrannosaurs. In Rosenberg, G.D. & Wolberg, D.L. (eds): DinoFest, 165–175, Paleontological Society Special Publication 7.University of Tennessee, Knoxville.

Farlow, J.O. & Holtz, T.R. 2002: The fossil record of predation indinosaurs. Paleontological Society Special Papers 8, 251–265.

Farlow, J.O., Smith, M.B. & Robinson, J.M. 1995: Body mass, bone‘strength indicator’, and cursorial potential of Tyrannosaurusrex. Journal of Vertebrate Paleontology 15, 713–725.

Fiorillo, A.R. 1987: Significance of juvenile dinosaurs from CarelessCreek Quarry (Judith River Formation), Wheatland DountyMontanna. In Currie, P.J. & Foster, K. (eds): Fourth Symposiumon Mesozoic Terrestrial Ecosystems, Short Papers. 3, 88–95 Occa-sional Papers of the Tyrrell Musuem, Canada.

Fiorillo, A.R. 1991: Prey bone utilisation by predatorydinosaurs. Palaeogeography, Palaeoclimatology, Palaeoecology 88,157–166.

Fiorillo, A.R. & Currie, P.J. 1994: Theropod teeth form the JudithRiver Formation (Upper Cretaceous) of south-central Montana.Journal of Vertebrate Paleontology 14, 74–80.

Fisher, D.C. 1981: Crocodilian scatology, microvertebrate concen-trations, and enamel-less teeth. Paleobiology 7, 262–275.

Fuiman, L. 1993: Development of predator evasion in Atlantic her-ring, Clupea harengus L. Animal Behaviour 45, 1101–1116.

Fuller, T.K. & Kat, P.W. 1993: Hunting success of African wilddogs in southwestern Kenya. Journal of Mammology 74, 464–467.

Galliard, J.-M., Festa-Bianchet, M. & Yoccoz, N.G. 1998: Popula-tion dynamics of large herbivores: variable recruitment withconstant adult survival. Trends in Ecology and Evolution 13, 58–63.

Gotmark, F. & Post, P. 1996: Prey selection by sparrowhawks,Accipiter nisus: relative predation risk for breeding passerinebirds in relation to their size, ecology and behaviour. Philosophi-cal Transactions of the Royal Society B 351, 1559–1577.

Happ, J. 2008: An analysis of predator–prey behavior in a head-to-head encounter between Tyrannosaurus rex and Triceratops. InLarson P. & Carpenter K. (eds): Tyrannosaurus rex the TyrantKing, 355–370. Indiana University Press, Bloomington, IN.

Haynes, G. 1980: Evidence of carnivore gnawing on Pleistoceneand Recent mammalian bones. Paleobiology 6, 341–351.

Hayward, M.W., Henschel, P., O’Brien, J., Hofmeyr, M., Balme, G.& Kerley, I.H. 2006: Prey preferences of the leopard (Pantherapardus). Journal of Zoology 27, 298–313.

Holtz, T.R. 2004: Tyrannosauroidea. In Weishampel, D.B., Dod-son, P. & Osmolska, H. (eds): The Dinosauria, 2nd edn, 111–136. California University Press, Berkeley, CA.

Holtz, T.R. 2008. A critical reappraisal of the obligate scavenginghypothesis for Tyrannosaurus rex and other tyrant dinosaurs. InLarson, P. & Carpenter, K. (eds): Tyrannosaurus rex the TyrantKing, 371–396. Indiana University Press, Bloomington, IN.

Holtz, T.R. & Osmolska, H. 2004: Saurischia. In Weishampel, D.B.,Dodson, P. & Osmolska, H. (eds): The Dinosauria, 2nd edn,2124. California University Press, Berkeley, CA.

Horner, J.R. 2002: Dinosaur behaviour. In Encyclopedia of LifeSciences, vol. 5, 468–472. John Wiley & Sons, Chichester.

Housten, D.C. & Copsey, J.A. 1994: Bone digestion and intestinalmorphology of the bearded vulture. Journal of Raptor Research28, 73–78.

Hummel, J. & Clauss, M. 2008: Megaherbivores as pacemakers ofcarnivore diversity and biomass: distributing or sinking trophicenergy? Evolutionary Ecology Research 10, 925–930.

Hunt, A.P., Meyer, C.A., Lockley, M.G. & Lucas, S.G. 1994:Archaeology, toothmarks and sauropod dinosaur taphonomy.Gaia 10, 225–231.

Husseman, J.S., Murray, D.L., Power, G., Mack, C., Wenger, C.R.& Quigley, H. 2003: Assessing differential prey selection patternsbetween two sympatric large carnivores. Oikos 1, 591–601.

Hutchinson, J.R. & Garcia, M. 2002: Tyrannosaurus was not a fastrunner. Nature 415, 1018–1021.

Jacobsen, A.R. 1998: Feeding behavior of carnivorous dinosaurs asdetermined by tooth marks on dinosaur bones. Historical Biology13, 17–26.

Janis, C.M. & Carrano, M.T. 1992: Scaling or reproductive turn-over in archosaurs and mammals: why are large terrestrial mam-mals so rare? Annales Zoologica Fennica 28, 201–216.

Kardong, K.V. 2002: Vertebrates: Comparative Anatomy, Function,Evolution, 3rd edn. McGraw-Hill, Boston.

Kelley, J.L. & Magurran, A.E. 2003: Learned predator recognitionand antipredator responses in fishes. Fish and Fisheries 4, 216–226.

LETHAIA 43 (2010) Theropod feeding behaviour 243

Kobayashi, Y. & Lu, J.C. 2003: A new ornithomimid dinosaur withgregarious habits from the Late Cretaceous of China. ActaPalaeontologica Polonica 48, 235–259.

Krause, J. & Godin, J.J. 1996: Influence of prey foraging posture onflight behavior and predation risk: predators take advantage ofunwary prey. Behavioural Ecology 7, 264–271.

Kruger, S.C., Lawes, M.J. & Maddock, A.H. 1999: Diet choiceand capture success of wild dog (Lycaon pictus) in Hluhluwe-Umfolozi Park, South Africa. Journal of Zoology 248, 543–551.

Marchetti, K. & Price, T. 1989: Differences in the foraging of juve-nile and adult birds: the importance of developmental con-straints. Biological Reviews of the Cambridge Philosophical Society64, 51–70.

Mateus, O. 1998: Lourinhasaurus antunesi, a new Upper Jurassic al-losauroid (Dinosauria: Theropoda) from Lourinha, Portugal.Memorias da Academia das Ciencias de Lisboa 37, 111–124.

Mathews, J.C., Brusatte, S.L., Williams, S.A. & Henderson, M.D.2009: The first Triceratops bonebed and its implications for gre-garious behaviour. Journal of Vertebrate Paleontology 29, 286–290.

Matthew, W. 1908: Allosaurus, a carnivorous dinosaur, and itsprey. American Museum Journal 8, 3–5.

Maxwell, W.D. & Ostrom, J.A. 1995: Taphonomy and paleobiolog-ical implications of Tenontosaurus–Deinonychus associations.Journal of Vertebrate Paleontology 15, 707–712.

Mazzetta, G.V., Christiansen, P. & Farina, R.A. 2004: Giants andbizarres: body size of some southern South American CretaceousDinosaurs. Historical Biology 16, 71–83.

McDonald, D.W. 1994: Carnivores. In McDonald, D.W. (ed.) TheEncyclopedia of Mammals, 2nd edn, 18–25. Oxford UniversityPress, Oxford.

Mellett, J.S. 1983: Dinosaurs, mammals, and Mesozoic taphonomy.Acta Palaeontologica Polonica 28, 209–213.

Molnar, R.E. & Farlow, J.O. 1990. Carnosaur paleobiology. In Wei-shampel, D.B., Dodson, P. & Osmolska, H. (eds): The Dinosauri-a, 210–224. University of California Press, Berkeley.

Naju, J.K. & Blumenschine, R.J. 2006: A diagnosis of crocodilefeeding traces on larger mammal bone, with fossil examplesfrom the Plio-Pleistocene Olduvai Basin, Tanzania. Journal ofHuman Evolution 50, 142–162.

Palmqvist, P., Martinez-Navarro, B. & Arribas, A. 1996: Prey selec-tion by terrestrial carnivores in a Lower Pleistocene paleocom-munity. Paleobiology 22, 514–534.

Paul, G.S. 1987. Predation in the meat eating dinosaurs. In Currie,P.J. & Koster, E.H. (eds): Fourth Symposium on Mesozoic Terres-trial Ecosystems, Short Papers, 173–178. Tyrrell Museum of Pale-ontology, Drumheller.

Paul, G.S. 1994: Dinosaur reproduction in the fast lane: implica-tions for size, success and extinction. In Carpenter, K., Hirsch,K. & Horner, J.R. (eds): Dinosaur Eggs and Babies, 244–255.Cambridge University Press, Cambridge.

Quinn, J.L. & Cresswell, W. 2004: Predator hunting and prey vul-nerability. Journal of Animal Ecology 73, 143–154.

Rayfield, E.J. 2004: Cranial mechanics and feeding in Tyrannosau-rus rex. Proceedings of the Royal Society, Series B 271, 1451–1459.

Rayfield, E.J. 2005: Aspects of comparative cranial mechanicsin the theropod dinosaurs Coelophysis, Allosaurus andTyrannosaurus. Zoological Journal of the Linnean Society 144,309–316.

Rayfield, E.J., Norman, D.B., Horner, C.C., Horner, J.R., Smith,P.M., Thomason, J.J. & Upchurch, P. 2001: Cranial design andfunction in a large theropod dinosaur. Nature 409, 1033–1037.

Richmond, N.D. 1965: Perhaps Juvenile dinosaurs were alwaysscarce. Journal of Vertebrate Paleontology 39, 503–505.

Rogers, R.R., Krause, D.W., Curry Rogers, K., Rasoamiaramanana,A.H. & Rahantrisoa, L. 2004: Paleoenvironment and paleoecol-ogy of Majungasaurus crenatissimus (Theropoda: Abelisauridae)from the Late Cretaceous of Madagascar. In Sampson, S.D. &Krause, D.W. (eds): Majungasaurus crenatissimus (Theropoda:

Abelisauridae) from the Late Cretaceous of Madagascar, 21–31.Journal of Vertebrate Paleontology. Memoir 8.

Rohner, C. & Krebs, C.J. 1996: Owl predation on snowshoe hares:consequences of antipredator behaviour. Population Ecology 108,303–310.

Ryan, M.J., Currie, P.J., Gardner, J.D., Vickaryous, M.K. & Lavigne,J.M. 1998: Baby hadrosaurid material associated with an unusu-ally high abundance of Troodon teeth from the Horseshoe can-yon formation, Upper Cretaceous, Alberta, Canada. Gaia 15,123–133.

Scharf, F.S., Buckel, J.A., Juanes, F. & Conover, D.O. 1998: Preda-tion by juvenile piscivorous bluefish (Pomatomus saltatrix): theinfluence of prey to predator size ratio and prey type on preda-tor capture success and prey profitability. Canadian Journal ofFisheries and Aquatic Science 55, 1695–1703.

Schubert, B.W. & Ungar, P.S. 2005: Wear facets and enamel spall-ing in tyrannosaurid dinosaurs. Acta Palaeontologica Polonica 50,93–99.

Steele, T.E. 2004: Variation in mortality profiles of red deer (Cervuselaphus) in Middle Palaeolithic assemblages from western Eur-ope. International Journal of Osteoarchaeology 14, 307–320.

Sullivan, K.A. 1989: Predation and starvation: age-specific mortal-ity in juvenile juncos (Junco phaenotus). The Journal of AnimalEcology 58, 275–286.

Tanke, D.H. & Currie, P.J. 2000: Head biting behaviour in thero-pod dinosaurs: paleopathological evidence. Gaia 15, 167–184.

Temple, S.A. 1987: Do predators always capture substandard indi-viduals disproportionately from prey populations? Ecology 68,669–674.

Tucker, A.D., Limpus, C.J., McCallum, H.I. & McDonald, K.R.1996: Ontogenetic dietary partitioning by Crocodylus johnstoniduring the dry season. Copeia 1996, 978–988.

Turesson, H., Persson, A. & Bronmark, C. 2002: Prey size selectionin piscivorous pikeperch (Stizostedion lucioperca) includes activeprey choice. Ecology of Freshwater Fish 11, 223–233.

van Valkenburgh, B. 1988: Incidence of tooth breakage amonglarge, predatory mammals. The American Naturalist 131, 291–302.

van Valkenburgh, B. 1996: Feeding behavior in free-ranging, largeAfrican carnivores. Journal of Mammalogy 77, 240–254.

van Valkenburgh, B. 2009: Costs of carnivory: tooth fracture inPleistocene and Recent carnivorans. Biological Journal of the Lin-nean Society 96, 68–81.

Varricchio, D.J. 2001: Gut contents from a Cretaceous tyrannosau-rid: implications for theropod dinosaur digestive tracts. Journalof Paleontology 75, 401–406.

Varricchio, D.J., Sereno, P.C., Zhao, X., Tan, L., Wilson, J.A. &Lyon, G.H. 2008: Mud trapped herd captures evidence of dis-tinctive dinosaur sociality. Acta Palaeontologica Polonica 53,567–578.

Weathers, W.W. & Sullivan, K.A. 1989: Juvenile foraging profi-ciency, parental effort, and avian reproductive success. EcologicalMonographs 59, 223–246.

Webb, G.J.W., Hollis, G.J. & Manolis, S.C. 1991: Feeding, growth,and food conversion rates of wild juvenile saltwater crocodiles(Crocodylus porosus). Journal of Herpetology 25, 462–473.

Webb, G.J.W., Britton, A.R.C., Manolis, S.C., Ottley, B. & Stirrat,S. 2000: The recovery of Crocodylus porosus in the Northern Ter-ritory of Australia: 1971–1998. In Proceedings 15th WorkingMeeting of the IUCN-SSC Crocodile Specialist Group. Varadero,Cuba 17–20 January 2000, 196–235. IUCN, Gland.

Witmer, L.M. 1995: The Extant Phylogenetic Bracket and theimportance of reconstructing soft tissues in fossils. In Thomp-son, J.J. (ed): Functional Morphology in Vertebrate Paleontogy,19–33. Cambridge University Press, New York.

Zhao, Q., Barrett, P.M. & Eberth, D. 2007: Social behaviour andmass mortality in the basal ceratopsian dinosaur Psittacosaurus(early Cretaceous, People’s Republic of China). Palaeontology 50,1023–1029.

244 D. W. E. Hone & O. W. M. Rauhut LETHAIA 43 (2010)