Palaeogeography, Palaeoclimatology, Palaeoecology 311 (2011) 38–47

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Trace fossils on dinosaur bones from Upper Cretaceous eolian deposits in Mongolia:Taphonomic interpretation of paleoecosystems in ancient desert environments

Mototaka Saneyoshi a,⁎, Mahito Watabe a, Shigeru Suzuki a, Khishigjav Tsogtbaatar b

a Center for Paleobiological Research, Hayashibara Biochemical laboratories, Inc., 1-2-3 Shimoishii, Kita-ku, Okayama 700-0907, Japanb Mongolian Paleontological Center, Mongolian Academy of Sciences, Ulaanbaatar 210351, Mongolia

⁎ Corresponding author.E-mail address: m-saneyoshi@hayashibara.co.jp (M.

0031-0182/$ – see front matter © 2011 Elsevier B.V. Adoi:10.1016/j.palaeo.2011.07.024

a b s t r a c t

a r t i c l e i n f o

Article history:Received 5 August 2010Received in revised form 5 June 2011Accepted 18 July 2011Available online 31 July 2011

Keywords:Trace fossilsDinosaur carcassesNitrogen cycleDjadokhta and Barun Goyot FormationsGobi desert

The formation processes of trace fossils – including shallow to deep pits, notches, borings (tunnels), andchannels, particularly at the limb joints – observed on the surfaces of Velociraptor, Protoceratops, ankylosaurid,and Bagaceratops skeletons from Upper Cretaceous eolian deposits in the Gobi desert, Mongolia wereinvestigated. The median diameters of these structures ranged from 5.25 to 7.68 mm. These structures werelikely created by insects scavenging on dinosaur carcasses. This interpretation is corroborated by the presenceof burrows of a size similar to the trace fossils observed on the dinosaur bone surfaces at the same locality.Broad borings (about 32 mm in diameter) created by small Mesozoic mammals have also been discovered onthe ribs and scapulae of a Protoceratops skeleton. Dinosaur skeletons found at two localities, Tugrikin Shirehand Khermeen Tsav, and two formations, the Djadokhta Formation and Barun Goyot Formation, exhibited thesame type of damage to the limb joints. The high frequency of trace fossils at the limb joints suggests thatsmall animals targeted the collagen in the joint cartilage of dried dinosaur carcasses as a source of nitrogen,which was relatively scarce in the eolian environments of the Gobi desert during the Late Cretaceous.

Saneyoshi).

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© 2011 Elsevier B.V. All rights reserved.

1. Introduction

Damage to fossilized bones in terrestrial environments hasbeen studied by many researchers (e.g., Behrensmeyer, 1978;Haynes, 1983; Jhonson, 1983; Fiorillo, 1988; Lyman and Fox, 1989;Vasileiadou et al., 2009), and a number of theoretical models of bonescavenging activity by insects and mammals have been proposed.Watson and Abbey (1986) postulated that insects targeted bonecollagen as a source of nitrogen, and Fejfar and Kaiser (2005) sug-gested the same possibility regarding bone borings made by Oli-gocenemammals fromDetan, northwest Bohemia. This phenomenonis a characteristic problem in nitrogen-poor subtropical carbonatiticsoils. Thus, elucidating the formation processes of trace fossils onbone surfaces could provide insight into ancient insect and mam-malian behavior, and assist in the reconstruction of paleoenviron-ments and paleoecosystems (Chin and Gill, 1996; Hasiotis et al.,1999; West and Hasiotis, 2007).

In taphonomic studies, damage to dinosaur bone, particularly boneborings, has been used to elucidate the scavenging and pupatingbehaviors of insects in flood plain environments (e.g., Hasiotis andBown, 1992; Paik, 2000; Paik et al., 2001; Britt et al., 2008). Rogers(1992) documented occurrences of macro-borings on the surfaces ofProsaurolophus bones from the Upper Cretaceous of northwestern

Montana, and suggested that these borings were created by scaveng-ing carrion beetles. Previously, bone borings on dinosaur bones fromflood plain environments have been interpreted as pupation chambersmade by insects (e.g., Martin and West, 1995; Hasiotis et al., 1999).Trace fossils on dinosaur bones from eolian deposits, though they haveonly been briefly described (e.g., Jerzykiewicz et al., 1993; Kirklandet al., 1998), have also been interpreted as traces of pupation cham-bers made by insects (Kirkland and Bader, 2010). However, detaileddescriptions of trace fossils preserved on dinosaur bones from eoliandeposits are rare, and the formation processes of trace fossils areunclear. To develop a better understanding of Cretaceous paleoeco-systems in continental desert environments, the formation processesof trace fossils preserved on dinosaur remains from continental eoliandeposits were investigated.

The Upper Cretaceous sediments of Mongolia's Gobi desert areone of the world's most important dinosaur localities (Berky andMorris, 1927; Norell et al., 1994). Upper Cretaceous eolian and fluvio-lacustrine deposits are widely distributed throughout the Gobi desert(Gradzinski et al., 1977; Jerzykiewicz and Russel, 1991; Eberth, 1993;Fastovsky et al., 1997). Many dinosaur specimens from the Gobidesert are well preserved, allowing for detailed observation of struc-tures on the bone surfaces and enabling a good understanding of theprocesses of trace fossil formation. The present study focuses on tracefossils associated with fully articulated Velociraptor, Protoceratops andBagaceratops skeletons, and the skull and cervical vertebrae of anankylosaurid specimen from Upper Cretaceous eolian deposits in theGobi desert.

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2. Geological setting of dinosaur localities

The dinosaur skeletons with trace fossils used in the present studywere from the Djadokhta and Barun Goyot Formations, which arewidely distributed throughout Upper Cretaceous dinosaur localities inthe Gobi Desert (Lefield, 1971; Gradzinski et al., 1977; Jerzykiewicz,2000). The dinosaur remains used in the present study were collectedat Tugrikin Shireh and Khermeen Tsav (Fig. 1), which are located inthe central to southwestern part of the Gobi desert.

The Djadokhta Formation crops out at Tugrikin Shireh. The for-mation is composed of middle to fine, white to pale yellow cementedsand made up predominantly of quartz grains (Fastovsky et al., 1997).The sand beds in the locality exhibit large-scale trough cross bedding(Fig. 2A; Saneyoshi and Watabe, 2008a). The Djadokhta Formation atthis locality consists predominantly of eolian deposits (Fastovskyet al., 1997; Watabe et al., 2010). In previous studies, various kinds oftrace fossils have been described from eolian deposits at TugrikinShireh (Fastovsky et al., 1997; Saneyoshi and Watabe, 2008b; Seikeet al., 2010). Natural casts of pupal chambers of an unknown insectwere collected by the Japan–Mongolian Paleontological Joint Expedi-tion (JMPJE) in 2007 (Fig. 2B). The age of the formation at TugrikinShireh has been determined to be Middle Campanian (Jerzykiewiczand Russel, 1991; Jerzykiewicz, 2000).

The Barun Goyot Formation, cropping out in the northern part ofKhermeen Tsav, is subdivided, from lower to upper, into the LowerWhite Bed and the Red Bed, as proposed by a Polish expedition in the1960s (Gradzinski et al., 1977). The Red Bed, which includesfossiliferous beds containing dinosaur remains, consists of well-sortedmedium to fine, reddish to pale orange cemented sand beds andmassive mud beds with conglomerates of gravel-sized clasts (Watabeet al., 2010). The sediments in the reddish sand beds exhibit large-scale trough cross-bedding (Fig. 2C). The sedimentary environmentsof the Red Bed in this locality consist predominantly of eolian andfluvio-lacustrine deposits (Saneyoshi et al., 2007). The eolian depositshave yielded trace fossils (Watabe and Suzuki, 2000c); however,detailed descriptions of Red Bed trace fossils are lacking. The age ofthe Red Bed has been determined to be Middle to Late Campanian

Fig. 1. Map showing locations of the dinosaur specimens used in this study

(Gradzinski et al., 1977; Jerzykiewicz and Russel, 1991; Jerzykiewicz,2000).

3. Material in the present study

Five dinosaur specimens (Fig. 3) – one Velociraptor, two Protocera-tops, one ankylosaurid and one Bagaceratops – were collected fromUpper Cretaceous eolian deposits in the Gobi desert. Of these, in 1993,1994 and 1998, JMPJE collected articulated the Velociraptor (MPC-D100/54), both Protoceratops specimen (MPC-D 100/533 and MPC-D100/534) and the ankylosaurid specimen (MPC-D 100/1337) from theDjadokhta Formation at Tugrikin Shireh (Watabe and Suzuki, 2000a,2000b, 2000d). In 1993, JMPJE collected the articulated Bagaceratopsskeleton (MPC-D 100/535) from the Barun Goyot Formation atKhermeenTsav (Watabe andSuzuki, 2000a). Trace fossilswereobservedon all of these articulated skeletons (e.g. Watabe and Fastovsky, 1999;Mastumoto and Saneyoshi, 2010).

Institutional abbreviations — MPC, Mongolian PaleontologicalCenter, Ulaanbaatar, Mongolia

4. Results

4.1. Weathering stage of dinosaur skeletons

Modifications of fossilized bones are caused by several processes,including scavenging by other vertebrates (Hone and Watabe, 2010),transportation causing breakage of bones (Fiorillo, 1991), weathering(Behrensmeyer, 1978), chemical damage (Fiorillo, 1998) and smallanimal activity (Rogers, 1992). Dinosaur skeletonswith trace fossils inthis taphonomic study were collected from eolian deposits, and hadbeen kept in an articulated portion (Fig. 3). This evidence suggeststhat dinosaur carcasses may have been quickly buried in eoliandeposits (Fastovsky et al., 1997; Loope et al., 1998). Therefore, damagecaused by vertebrate scavengers and transportation processes can beexcluded in the case of present study. In addition, corrosion was notobserved on all dinosaur specimens in the present study (Fig. 3). Onthe other hand, bone weathering is an important indication of

(after Jerzykiewicz, 2000). TS, Tugrikin Shireh; KhT, Khermeen Tsav.

Fig. 2. Photographs of outcrops of eolian deposits in the Gobi desert, Mongolia, andnatural casts of pupal chambers. (A) Eolian deposits with large-scale cross-stratifications at Tugrikin Shireh. Outcrop is about 8.0 m high. (B) Natural casts ofpupal chambers from Tugrikin Shireh. These casts were discovered by the JapanMongolian Paleontological Joint Expedition (JMPJE) in 2007. (C) Eolian deposits withlarge-scale cross-stratifications at Khermeen Tsav. Outcrop is about 9.0 m high.

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modification processes in arid conditions (Behrensmeyer, 1978), andmust be involved in the depositional processes of dinosaur carcasses.

All skeletons used in the present study appeared to be well pre-served, with good articulation (Fig. 3). The specimens from TugrikinShireh (Velociraptor, both Protoceratops and the ankylosaurid) hadsmall, shallow cracks, but no fracturing of the bone surfaces (Fig. 3AtoD). Shallow crackswere generallyfilledwith eolian sandmatrix. Bonesurfaces of the Bagaceratops skeleton showed longitudinal cracking ofthe outer cortical bone (Fig. 3E), and the surfaces of the skull andischium were beginning to flake off. This specimen was dorsoventrallycompressed during the weathering process, resulting in markeddeformation of the cranial part of the skeleton. Articulated limb bonessuch as the humerus, radius/ulna, femur, and tibia/fibula were partiallydestroyed, with shallow cracking and trace fossils evident on the bone

surfaces. Detailed features of these trace fossils are described in thefollowing sections.

Fiorillo (1988) described fossil bone weathering based on mam-malian fossils, and defined four weathering stages from the abrasion offossil bone surfaces as follows, stage 0, no signs of cracking or flaking ofthe bone surface; stage 1, cracking and flaking on the outermost layer ofbone; stage 2, no outer bone remains, and cracking has started topenetrate into the bone cavities; stage 3, a fibrous texture is observedand most cracks penetrate into the bone cavities. Using these defi-nitions, the weathering stages of the Velociraptor, Protoceratops andankylosaurid skeletons were 0 or 1, and that of the Bagaceratopsskeleton was 1 or 2. These differences in weathering stage were con-sidered to have been caused by differences in the sedimentationprocesses.

4.2. Trace fossils on dinosaur bone surfaces

Trace fossils on dinosaur bone surfaces were characterized bystructure type (Hasiotis and Mitchell, 1993; Hasiotis, 2004; West andHasiotis, 2007; and Britt et al., 2008) – i.e., pits, notches, borings(tunnels) and channels. The diameters of trace fossil structures at theminor axis of each structure were measured, and the locations of thestructures on long bones from the Velociraptor, Protoceratops andBagaceratops skeletons were recorded.

Pits were a frequently observed structure, occurring on the bonesurfaces of all the skeletons in the present study (Table 1). Althoughpits were observed on all parts of the skeletons, they wereconcentrated at the cranial and dorsal vertebrae. Pits are hemispher-ical depressions that are round to elliptical in shape (Fig. 4); in theskeletons used in the present study, pits ranged in diameter from1.72.0 to 12.7014.55 mm (Table 1), with a mean depth of 1 mm. Thepits were filled with sand matrix (Fig. 4), and the walls of the pitsappeared rough and irregular, characterized by groove marks (causedby scratching or biting) with no preferred direction. Some of these pitshad relatively smooth walls with deeper depressions.

The most apparent trace fossils in the skeletons studied werenotches, which were observed on all the skeletons (Table 1). Mostnotches were observed on the proximal and epiphyseal ends and thediaphysis (Fig. 5). Notches are semi-circular or semi-elliptical inshape with cup-shaped depressions (Fig. 5A), and range in diameterfrom 2.2 to 13.55 mm (Table 1). While most notches had roughinternal walls, some appeared to have smooth internal walls. Theproximal and distal end of some bones had been completelydestroyed by notches (Fig. 5B).

Unlike pits and notches, which are relatively shallow surfacestructures, borings penetrate the bones more deeply, sometimescontinuing through to the opposite side (Fig. 6). These are same as the“tunnels” described by West and Hasiotis (2007). Borings wereobserved on the Velociraptor, Protoceratops, and ankylosaurid skeletons.Many boringswere circular or semi-elliptical in shapewith roughwalls,ranging from3.30 to32.00 mmindiameter (Table 1). The largest boring,found on one of the Protoceratops skeletons (MPC-D 100/534), waslocated between the dorsal vertebrae, ribs, and scapulae, and appearedto have smooth walls and a circular shape (Fig. 6B).

Channels, which cut into bone surfaces at a shallower level thanborings, were also evident on the bone surfaces (Table 1). These struc-tureswere observed on theVelociraptor, Protoceratops, and Bagaceratopsskeletons (Table 1), particularly on the vertebral columns (Fig. 7).Channels are much like notches in that they have a U-shaped cross-section (West and Hasiotis, 2007) with sinuous channels, varyingconsiderably in size from 2.90 to 11.45 mm in width and from 8.90 to45.10 mm in length. Most channel walls appeared rough, with somegroove marks, while other channels had smooth walls.

Pits, notches, and channels were observed on all parts of theVelociraptor, Protoceratops, and Bagaceratops skeletons, while boringswere found on all skeletons except theBagaceratops specimen (Table 1).

Fig. 3. Photographs of dinosaur specimens used in the present study (A) Articulated Velociraptor skeleton (MPC-D 100/54). (B) Articulated Protoceratops skeleton (MPC-D 100/533).(C) Articulated Protoceratops skeleton (MPC-D 100/534). (D) Skull and cervical vertebrae of an ankylosaurid (MPC-D 100/1337). (E) Articulated Bagaceratops skeleton (MPC-D 100/535).

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Notches were particularly deep at the proximal and distal ends of limbbones and long pelvic bones. Bone surface damage occurred in 80–90%of long bone epiphyses (Fig. 8).

5. Discussion

5.1. Trace makers

All structures examined in the present study were circular, semi-circular or semi- elliptical in shape, and all had a similar minor-axisdiameter (Fig. 9). Differences in the shapes of trace fossil structures onbone surfaces have been interpreted as a function of the angle anddirection of excavation of the trace maker (e.g., West and Hasiotis,2007). The different shapes observed in the present study can also beexplained by the angle and direction of trace maker activities. Whentrace makers gained access to dinosaur bones, they began to gnaw thebone surface at a shallow depth, creating pits. Notches, meanwhile,were clustered at the distal and proximal ends of long bones (Figs. 4Aand C; 5B, C and D), suggesting that the trace makers targeted theedges of each bone. Borings, created when the trace makers burroweddirectly through the bone, were similar in size and shape to notches.The difference between notches and borings was considered to be thepath location within the bone. Channels were often located near pits

or borings (Fig. 6C), and were accompanied by groove marks on thechannel edges, suggesting that the trace makers moved along thebone as they gnawed at the surface. The medianminor-axis diametersof all pits, notches, borings and channels on the dinosaur skeletons inthe present study ranged from 5.25 to 7.68 mm, respectively (Fig. 9).Tracemakers with a body diameter (width) of 5.0 to 8.0 mm thereforelikely caused the damage to all of the skeletons.

Trace fossils on dinosaur bonesmay be caused by the construction ofpupation chambers by insects in dinosaur carcasses (e.g., Martin andWest, 1995; Kirkland and Bader, 2010). In 2007, JMPJE collected naturalcasts of pupal chambers (e.g., Johnston et al., 1996) at Tugrikin Shireh(Fig. 2C). These pupal chambers (N=9) ranged from14.9 to 16.9 mm inminor-axis diameter, with an average minor-axis diameter of 15.8 mm.Generally, as the size of the chamber is larger than the body diameter ofthe larva, the natural casts of pupal chambers from Tugrikin Shirehappear to have been created by larvae that were slightly less than15.8 mm in diameter. This diameter is quite a bit larger than that of thetrace fossils observed on the dinosaur skeletons in the present study. Inaddition, these pupal chambers have not been discovered in closeproximity to dinosaur skeletons. However, burrows, which were con-nected with pits and borings on dinosaur bones, were observed on theProtoceratops skeletons (Fig. 10). This evidence suggests that the tracefossils on the dinosaur skeletons in the present study were caused by

Table 1Location and diameters of pits, notches, borings and channels on Velociraptor, Protoceratops, ankylosaurid and Bagaceratops skeletons.

Dinosaur Parts Pits Notches Boring Channel

Velociraptora

(MPC-D 100/54)Cervical X X XDorsal X XStarnal XHumerus XUlna and radius X XIllium X XSacral X XFemur X XTibia and fibra X X X.........................................................................................................................................................................................................................................................................................Diameter/lengthb 1.70–9.30 mm 2.40–11.50 mm 7.20–11.40 mm 2.90–4.80 mm/10.00–17.50 mm

Protoceratopsc

(MPC-D 100/533)Skull X X XCervical XDorsal XScapula and coracoid X X X XHumerus X X XUlna and radius X X XSacral XFemur X X X XTibia and fibra X X XMetatarsal X X XCaudal X X X...........................................................................................................................................................................................................................................................................................Diameter/lengthb 1.90–10.70 mm 2.95–10.20 mm 3.30–12.00 mm 3.20–11.10 mm/14.55–45.10 mm

Protoceratopsd

(MPC-D 100/534)Skull X X XDorsal X X X XScapula and coracoid X X X XRib X XHumerus XUlna and radius X XIlium X X XIschium XFemur X XTibia and fibra X XMetatarsal X X XCaudal X X.......................................................................................................................................................................................................................................................................................Diameter/lengthb 2.20–11.0 mm 2.20–13.55 mm 5.55–32.00 mm 3.00–4.55 mm/8.90–19.70 mm

Ankylosaurid(MPC-D 100/1337)

Skull X X XCervical X X XDiametere 3.00–9.25 mm 4.15–11.95 mm 5.25–23.65 mm –

Bagaceratopsf

(MPC-D 100/535)Skull XDorsal X XRib XHumerus XUlna and radius X XMetacarpal XIllium X X XIschium XFemur X XTibia and fibra X XMetatarsal XDigit (Pes) XCaudal X X...........................................................................................................................................................................................................................................................................................Diameter/Lengthb 2.00–12.70 mm 2.60–12.30 mm 4.50–11.45 mm/14.00–26.00 mm

a Skull is not preserved, and trace fossils are not preserved on digit (manus and pes), pubis, and chevron.b Minimum and maximum diameters of trace structures at the minor axis of each structure and length of channel structures.c Metacarpal, digit (manus and pes), pubis, and chevron are not preserved on surfaces.d Cervial, metacarpal, digit (manus and pes), pubis, and chevron are not preserved on surfaces.e Minimum and maximum diameters of trace structures at the minor axis of each structure.f Cervical, digits (manus), pubis, and chevrons are not appeared which are influenced by strong weathering.

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insects. Variations in trace diameter reflect the life cycles of severalgenerations, including scavenging activities on dinosaur carcasses (e.g.,Rogers, 1992; Hasiotis et al., 1999; Roberts et al., 2007; Mastumoto andSaneyoshi, 2010). Although no insect body fossils have been discoveredin Upper Cretaceous eolian deposits in Mongolia, previous studies havedescribed fossilized burrow structures from eolian deposits at TugrikinShireh thought to have been constructed by sand wasps, wolf spiders,tiger beetles, and larvae (Fastovsky et al., 1997). These burrows havediameters ranging from 5 to 30 mm, with an average diameter of 5 to10 mm(Fastovskyet al., 1997; Saneyoshi andWatabe, 2008b), similar in

size to the trace fossils observed on the dinosaur specimens from thesame locality. Taken together, this evidence suggests that the bonedamage in these dinosaur specimens was created by insects.

The largest boring (Fig. 6B) observed on one of the Protoceratopsskeletons (MPC-D 100/534) was 32.0 mm inwidth; themaker of thisboring was therefore most likely not an insect. Mesozoic multitu-berculate and eutherianmammal fossils have also been discovered atTugrikin Shireh (Kielan-Jaworwska et al., 2004). The skulls of thesemammals range from 20 to 50 mm in length, and are narrower inwidth (Kielan-Jaworwska et al., 2000; Kielan-Jaworwska et al.,

Fig. 4. Photographs showing pits observed on the surfaces of Velociraptor, Protoceratops and Bagaceratops skeletons. (A) Right femur of Velociraptor (MPC-D 100/54) with pit (whitearrow) in lateral view. (B) Skull of Protoceratops (MPC-D 100/533) with pit (white arrow) in left lateral view. (C) Skull of Protoceratops (MPC-D 100/534) with pits (white arrow) inright lateral view. (D) Right femur of Bagaceratops (MPC-D 100/535) with pit (white arrow) in lateral view.

Fig. 5. Photographs showing notches observed on the surfaces of Velociraptor and Protoceratops skeletons. (A) Left tibia of Velociraptor (MPC-D 100/54)with notch (white dotted circle) indorsal view. (B) Right radius and ulna of Protoceratops (MPC-D 100/533) with notch (white dotted circle) in frontal view. Proximal end is completely destroyed by notch. (C) Left frill ofProtoceratops (MPC-D 100/534)with notches (white dotted circle) in dorsal view. (D) Right ischium of Protoceratops (MPC-D 100/534)with notches (white arrows) in right lateral view.

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Fig. 6. Photographs showing borings observed on the surfaces of Velociraptor, Protoceratops and Bagaceratops skeletons. (A) Ilium of Velociraptor (MPC-D 100/54) with boring (whitearrow) in ventral view. (B) Dorsal vertebrae and distal part of right scapula of Protoceratops (MPC-D 100/534) with large boring (inside white dotted circle) in dorsal view. (C) Skullof ankylosaurid (MPC-D 100/1337) with boring (white arrow) in ventral view. (D) Dorsal vertebrate of Bagaceratops (MPC-D 100/535) with boring (white arrow) in dorsal view.

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2004), similar in size to the largest boring. This suggests that smallMesozoicmammals may have also been involved in the bone damageobserved on dinosaur remains from Upper Cretaceous eolian de-posits at Tugrikin Shireh.

5.2. Formation processes of trace fossils on dinosaur bones

Bornemissza (1957), based on analysis of guinea pig carcasses,described five stages of decay process as follows; “initial decay”,“putrefaction”, “black putrefaction”, “butyric fermentation”, and “drydecay”. During black putrefaction and butyric fermentation, unfavor-able conditions are generated beneath the carcasses, thereby repellingscavengers. Reed (1958) defined decomposition processes of dogcarcasses divided into the following four stages: fresh, bloated, decayand dry stages. In the dry stage, many plants, insects and mammalsbegin to make use of vertebrate carcasses. This suggests that, interrestrial environments, utilization of vertebrate carcasses begins afterthe dry stage (Bornemissza, 1957). In a taphonomic study, Fastovsky etal. (1997) indicated that Protoceratops discovered at Tugrikin Shireh,which was a desert environment during the Late Cretaceous, wereprobably buried during catastrophic events such as sandstorms.Following burial, arid conditions in the eolian environment preservedthe dried carcasses while they were being utilized as food andhabitation sites by insects and small mammals. This interpretationimplies a biocenotic function of dinosaur carcasses in desert environ-ments as an important source of nutrition for small animals.

Bone damage on the Bagaceratops skeleton from the Barun GoyotFormation at Khermeen Tsav has other important implications.However, the geological background of trace fossils from eoliandeposits at Khermeen Tsav remains unclear. In the present study,formation processes of trace fossils on the Bagaceratops skeleton arediscussed from the perspective of bone weathering, as established by

Fiorillo (1988), based on the amount of bone damage and patterns ofbone cracking. The weathering stage of the Bagaceratops skeleton wasdetermined to be stage 1 or 2, in contrast to that of the Velociraptor,Protoceratops and ankylosaurid skeletons, which were stage 0 or 1.This difference in weathering indicates that the specimens underwentdifferent burial processes: while the dinosaur specimens fromTugrikin Shireh were quickly buried alive in eolian deposits by acatastrophic event (Fastovsky et al., 1997), the Bagaceratops fromKhermeen Tsav died before burial and the carcass became desiccatedafter exposure to the elements, as suggested by the weathering stageof the skeleton (Fiorillo, 1988). Nevertheless, the types of trace fossilsobserved on the Bagaceratops skeleton were similar to those found onthe dinosaur specimens from Tugrikin Shireh, indicating that dinosaurcarcasses, particularly dried carcasses, were affected by similar smallanimal activities in the eolian environments of Tugrikin Shireh andKhermeen Tsav. In the arid climate of both localities, the dinosaurcarcasses quickly became desiccated, and these dried carcassesprovided a rich source of nutrition to Mesozoic insects and mammalsin the harsh desert environment.

Relationships between small animal behavior and vertebratecarcasses in desert environments have not been reported, even forextant ecosystems. However, the trace fossils in the present studyprovide insight into paleoecosystems and small animal behavior indesert environments. The Velociraptor, both Protoceratops, andBagaceratops skeletons in particular showed extensive deep bonedamages on the articular portions (Fig. 8). These structures wereproduced by intensive activity in the cartilaginous parts of thedinosaur carcasses (e.g., Kirkland et al., 1998). Watson and Abbey(1986) concluded that osteophagous behavior targets bone collagenin order to alleviate nitrogen deficiency, a characteristic problem insubtropical carbonatitic soils (Fejfar and Kaiser, 2005; Roberts et al.,2007). Desert environments are also frequently nitrogen-poor due to

Fig. 8. Trace fossils on the proximal and distal ends of long bones (scapula, humerus,ulna/radius, ilium, ischium, femur, tibia/fibula, and metatarsal) and the central part ofthe proximo-distal axis of Velociraptor, Protoceratops and Bagaceratops skeletons. Manytrace fossils are concentrated on the apophyses of long bones (gray area).

Fig. 7. Photographs showing channels observed on the surfaces of Velociraptor andBagaceratops skeletons. (A) Cervical vertebrate of Velociraptor (MPC-D 100/54) withchannel (white arrow) in dorsal view. (B) Caudal vertebrates of Bagaceratops (MPC-D100/535) with channel (white arrow) in right lateral view.

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highly permeable matrixes in the sandy landscape (Nagai et al., 1980).It therefore follows that insects and small mammals responded to theextreme conditions of the desert environment by scavenging on thenitrogen-rich cartilage in dried dinosaur carcasses. A recent studyfound that, cartilage remaining in vertebrate carcasses has beenpreserved even during dry stage of decay (e.g., Ahmad and Ahmad,2009). Therefore, the scavenging activities of insects and smallmammals on dried dinosaur carcasses are proposed as the primarycause of the damage observed on the articular portions of dinosaurbones from Upper Cretaceous eolian deposits in Mongolia.

6. Conclusion

Detailed observation of trace fossils on the surfaces of well-preserved dinosaur skeletons from Upper Cretaceous eolian depositsin Mongolia revealed the presence of various structures, includingpits, notches, borings (tunnels), and channels. These ichnofossils arecharacteristic of dried dinosaur carcasses from eolian environments,and reflect the scavenging activities of insects and small mammals.The presence of similar trace fossils observed on the bones fromseparate localities and formations suggests that scavenging activitiestargeting dried dinosaur carcasses played an important role indamages to dinosaur remains in eolian environments during theLate Cretaceous.

Bone surface damages were concentrated at the articular portionsof dinosaur skeletons, as insects and small mammals utilized dinosaurcartilage in the limb joints as a source of nutrition in nitrogen-pooreolian environments. Previous researchers have observed that smallanimals exhibit similar behavior in nitrogen-poor floodplain paleosolsand carbonated subtropical soils (e.g., Watson and Abbey, 1986; Fejfarand Kaiser, 2005). In the case of eolian environments, nitrogen-poor

conditions may affect the behavior of small animal life. However, thedetails of desert ecosystems, including the relationships betweeninsect behavior and nitrogen-poor conditions, are still unclear, evenfor extant ecosystems. The present results demonstrated that tracefossils on surfaces of vertebrate fossils fromeoliandeposits can be usedto reconstruct paleoecosystems, particularly the relationships be-tween small animals and vertebrate carcasses in desert environments.

Acknowledgements

We are grateful to Ken Hayashibara (CEO of the HayashibaraBiochemical Laboratories, Inc., Okayama, Japan in 2011) for hiscontinuous financial support to the Hayashibara Museum of NaturalSciences–Mongolian Paleontological Center Joint PaleontologicalExpedition since 1993. We are also grateful to the members of theHayashibara Museum of Natural Sciences and the Mongolian Paleon-tological Center Joint Paleontological Expedition Team for their help inthefield and at both institutions.Wewould also like to thankNobuteruIhara and Yellow Two Company for their offer to photograph thespecimens. We would also like to express our gratitude to the tworeviewers and Editor Finn Surlyk for their constructive comments onthe submitted manuscript. This study was supported by grants-in-aidfrom Hayashibara Biochemical Laboratories, Inc. and the HayashibaraMuseum of Natural Sciences. This paper constitutes ContributionNumber 71 of the HMNS–MPC Joint Paleontological Expedition.

Fig. 9. Size of observed trace fossils, including width and diameter of pits, notches, borings, and channels, on five dinosaur specimens. (A) Velociraptor, (B) Protoceratops (MPC-D100/533), (C) Protoceratops (MPC-D 100/534), (D) ankylosaurid and (E) Bagaceratops. Arrows and numbers under graphs indicate median diameter of trace fossils for eachspecimen. Structures with a diameter of over 30 mm are excluded from this figure and from the calculation of median diameter.

Fig. 10. Photograph showing trace fossils on dinosaur bones and burrows on Protoceratops skeleton (MPC-D 100/533). (A) Burrow (dotted white arrow) connected to a boring (whitearrow) on the skull surface in left lateral view. (B) Burrow (dotted white arrow) connected to a pit (white arrow) on the surface of the dorsal vertebra in left lateral view.

46 M. Saneyoshi et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 311 (2011) 38–47

47M. Saneyoshi et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 311 (2011) 38–47

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