Bioerosion and palaeoecological association of osteophagous insects in the Maastrichtian dinosaur
 Arenysaurus ardevoli

Bioerosions produced by the osteophagous diet of animals that fed on dinosaur bones are very scarce in the European fossil record. Herein we present bioerosion on hadrosaurid remains from the Maastrichtian Tremp Formation of the Pyrenean Basin, which is only the second such case recorded from the Iberian‐Occitan Plate besides a sauropod from the Jurassic‐Cretaceous of Valencia. The hadrosaurid fossil record is particularly rich in the Blasi sites of the Tremp Formation located in the municipality of Arén (Huesca, Spain). In this article, bones referred to the hadrosaurid Arenysaurus ardevoli from the Blasi‐3 site are analysed to shed light on the palaeoenvironment and on the presence of a palaeoecological interaction between the hadrosaurid carcase and osteophagous tracemakers. Bioerosions recorded on the bones comprise tunnels, roundish holes, and straight notches, similar to the traces attributed to necrophagous insects (cf. Cuniculichnus seilacheri). Here, we record the first instance of the activity of these animals on dinosaur bones in the Upper Cretaceous of the Ibero‐Occitan Plate. The results presented lead us to infer that the Arenysaurus bones were possibly transported by a storm or similar event to the Blasi‐3 site, where they were exposed to post‐mortem biotic interactions (eaten and partially decomposed by dermestid beetles) for a prolonged time period before they were completely buried. □ dermestid, hadrosaurid, Ibero‐Occitan Plate, necrophagous, taphonomy.

Bioerosions produced by the osteophagous diet of animals that fed on dinosaur bones are very scarce in the European fossil record. Herein we present bioerosion on hadrosaurid remains from the Maastrichtian Tremp Formation of the Pyrenean Basin, which is only the second such case recorded from the Iberian-Occitan Plate besides a sauropod from the Jurassic-Cretaceous of Valencia. The hadrosaurid fossil record is particularly rich in the Blasi sites of the Tremp Formation located in the municipality of Arén (Huesca, Spain). In this article, bones referred to the hadrosaurid Arenysaurus ardevoli from the Blasi-3 site are analysed to shed light on the palaeoenvironment and on the presence of a palaeoecological interaction between the hadrosaurid carcase and osteophagous tracemakers. Bioerosions recorded on the bones comprise tunnels, roundish holes, and straight notches, similar to the traces attributed to necrophagous insects (cf. Cuniculichnus seilacheri). Here, we record the first instance of the activity of these animals on dinosaur bones in the Upper Cretaceous of the Ibero-Occitan Plate. The results presented lead us to infer that the Arenysaurus bones were possibly transported by a storm or similar event to the Blasi-3 site, where they were exposed to post-mortem biotic interactions (eaten and partially decomposed by dermestid beetles) for a prolonged time period before they were completely buried. □ dermestid, hadrosaurid, Ibero-Occitan Plate, necrophagous, taphonomy. The term bioerosion includes any form of biological penetration of hard substrates (Bromley 1992 Hadrosaurid dinosaurs are particularly abundant -as part of a generally diverse vertebrate fauna-in the Maastrichtian of the Central Pyrenees (Iberian deposits between the Maastrichtian and the Palaeogene (Puértolas-Pascual et al. 2018), but no bioerosional trace fossils in bones have been reported from there. Of particular interest here is the Blasi-3 site, a vertebrate-bearing locality in the Central Pyrenees where remains of one juvenile and two adult hadrosaurid specimens have been recovered in the Tremp Formation. It is also the type locality of the hadrosaurid dinosaur Arenysaurus Pereda-Suberbiola et al. 2009b, described from numerous articulated and disarticulated remains, including cranial and postcranial elements corresponding to an adult specimen (Pereda-Suberbiola et al. 2009b;Cruzado-Caballero et al. 2013. Some post-cranial elements of this latter specimen, corresponding to the paratypes of the taxon, present trace fossils that have never been previously reported for this taxon or indeed for any terrestrial vertebrate.
In the light of the previous considerations, the main goals of this study are to describe the bioerosion preserved in some bones of the hadrosaurid Arenysaurus, as well as to analyse and discuss the identity and palaeobiology of the potential tracemaker. In addition to this, taphonomic and palaeoenvironmental aspects of the specimens are also discussed.

Geological setting
The vertebrate-bearing site of Blasi-3 is located 2 km to the west of the municipality of Arén (or Areny de Noguera, Huesca Province) in northeastern Spain (Fig. 1).
Blasi-3 is located stratigraphically within the Tremp Formation, being laterally equivalent to the upper Campanian-Maastrichtian of the Arén Sandstone Formation (Pereda-Suberbiola et al. 2009b). The Tremp Formation can be sub-divided into four informal lithological units named as follows from the base to the top: the 'Grey Garumnian', the 'Lower Red Garumnian', the Vallcebre Limestone (and lateral equivalents), and the 'Upper Red Garumnian' (Rosell et al. 2001). The 'Grey Garumnian' of Rosell et al. (2001) is equivalent to the Posa Fm, whereas the 'Lower Red Garumnian' is equivalent to the Conques and Talarn formations of Cuevas (1992). The 'Grey Garumnian' is mainly built up of greyish marls with intercalations of coal and sandstone, with abundant fossil remains of marine or brackish organisms such as benthic foraminifera, gastropods, rudists, coelenterates, chondrichthyans and osteichthyans, as well as freshwater microorganisms such as charophytes and ostracods, vascular plants and continental vertebrates such as lissamphibians, chelonians, lizards, crocodylomorphs, and dinosaurs (López-Martínez et al. 2001;Pereda-Suberbiola et al. 2009a, b;Blain et al. 2010;Villalba Breva et al. 2012;Blanco et al. 2015;Company et al. 2015). The sediments that formed the 'Grey Garumnian' of the Tremp Formation (of which Blasi-3 forms part) were deposited in wide, shallow protected areas of variable salinity that are interpreted as tidal-plain, lagoonal, and estuarine environments, located laterally and proximally to the barrier-island or deltaic deposits of the Arén Formation (Puértolas-Pascual et al. 2018;Pérez-Pueyo et al. 2021).
Blasi-3 is located in a 1-m-thick, grey, massive, calcareous sandstone. The vertebrate remains of Blasi-3 were found in an area of about 70 m 2 (Fig. 2), most of them belonging to the partially articulated holotype of Arenysaurus and other disarticulated hadrosaurid ornithopods (see Pereda-Suberbiola et al. 2009). The sandstone of Blasi-3 is a greywacke, very different from the typical mature, calcareous sandstone of the Tremp Formation. Blasi-3 consists of a texturally immature sandstone, poorly sorted angular grains of quartz, feldspar, and small rock fragments in a compact and finegrained clay matrix. The combination in Blasi-3 of a massive deposit, with immature sandstone and the presence of a semi-articulated dinosaur carcase, can be interpreted as being the result of a rapid sedimentation event, which in a coastal environment could be a storm. In Blasi-3, no typical tsunami sequences have been found (Navarrete et al. 2014), but the outcrop is small and the lateral relationships of Blasi-3 cannot be observed.
Blasi-3 has been included in several detailed stratigraphical, magnetostratigraphical and biostratigraphical overviews of the regional Upper Cretaceous (see Canudo et al. 2016, for further details). As a result, it has been ascertained that the Blasi-3 site is located in a normal-polarity chron correlated with sequence C30n, dated from 67.6 to 65.5 Ma (Canudo et al. 2016).

Material and methods
The trace-fossil-bearing bones are stored at the Museo de Ciencias Naturales of the Universidad de Zaragoza, under the label MPZ (Canudo 2018). The bones are paratypes of the lambeosaurine hadrosaurid Arenysaurus from the Blasi-3 site and include the following: in the scapula MPZ2008/333b (

Laboratory preparation
All the bioerosional trace fossils were originally filled with sedimentary matrix when the specimens were recovered from the field, although they were subsequently prepared in the laboratory. Currently some of the borings are partially filled with sediment or are devoid of any sediment matrix, whereas others are still completely filled. The right femur MPZ 2007/ 711 was cleaned using only physical methods (i.e. a pneumatic micro-hammer), whereas the right scapula MPZ 2008/333a-333b, the right humerus MPZ2008/336 and the left femur MPZ2008/337 were cleaned using both physical and chemical methods (8% formic acid solution) to remove the surrounding rocky matrix. During bone preparation, a few bone parts were affected by the preparation process (both mechanical and chemical), and these traces are excluded from the description and discussion below. Therefore, all of the traces described below are real bioerosional trace fossils and we can exclude an artificial origin for them (i.e. that they were produced by the preparation process).

Compute tomography
A micro-focus X-ray computed tomography (micro-CT) system, the Multi-TOM Core (XRE nv, Ghent, Belgium), located in the CORELAB Laboratory (Universitat de Barcelona, Catalonia, Spain), was used. The bones were scanned at 150 kV and at a power of 58 W, using a 1.5 mm A1 filter in order to reduce the beam-hardening effect (Cnudde & Boone 2013). In all cases, a complete rotation along the  (MPZ 2008/336). Raw data from each scan were imported (as a stack of TIFF 8-bit files) to Avizo 7.0 to generate a 3D surface from the micro-CT images, digitally extracting the bioerosions from the bone matrix. Due to the density of the bone and internal matrix, the CT images present several artefacts such as beam hardening, cupping artifacts and ring artifacts. As a consequence of these artifacts, automatic segmentation was difficult and not optimal, and thus semiautomatic (or manual in some regions) segmentation was required, as also reported for the study of cranial elements of the same specimen (see Cruzado-Caballero et al. 2015).

Measurements and nomenclature
The measurements for all the traces described in this study (length, width, and depth) were taken with a calliper, and digital measurements (from CT scan data) with the help of ImageJ 1.52v. Other measurements such as volume were obtained using Avizo 7.0 and Rhinoceros 4.0. The descriptive terminology and identification of the borings follows Roberts et al.

Results
Description of the trace fossils and may co-occur in the same bone, preserved mainly in the cortical tissue, although some of the holes also affect the spongy tissue. Both femurs are densely bioeroded, especially at the ends, whereas the humerus shows relatively fewer traces and the scapula only displays three long traces (Figs. 3-6; see Supplementary data for further details). The traces are described individually for convenience, but usually they form a continuum, so often the notches are not distinguishable from the furrows and the holes are the starting points for the furrows. Many of the trace fossils have been altered due to the preparation process (see Materials and Methods section), so it is not possible to confirm the boundaries of the walls or potential surface features, although it appears that the surface of the bioerosions is quite smooth, with no bioglyphs such as rasping or scratching microstructures on the walls. Nevertheless, the general features of the bioerosions are still visible and distinguishable, except where they are too densely occurring and thus overlap. The furrows are unbranched structures and are almost straight, usually running parallel to the bone fibre. There are relatively few notches, all of them with irregular borders and ends, sometimes with a slight curvature and varying depth. The holes occur near the ends of the bones, normally spaced apart from each other, and are mostly rounded to irregular vertical pits, also varying in depth.
Three furrows are located in the anterior half of the scapular blade MPZ2008/333b, parallel to each other, one of them beginning with a hole (Fig. 3 B-D). They display an average depth of 2.4 mm, and a minimum and maximum depth of 0.8 mm and 5 mm, respectively. Their width varies between a minimum of 2.1 mm and a maximum of 8.5 mm, with an average of 3.6 mm, while the maximum preserved length is 142 mm.
The longer furrow in the humerus MPZ2008/336 is preserved in the distal epiphysis (MPZ2019/1473; Fig. 4C), with a length of 102.4 mm and an average width and depth of 1.14 mm and 4.4 mm, respectively. The other furrow runs parallel to the first one and begins with a hole with rounded edges (MPZ2019/1474; Fig. 4D). This furrow has a width and depth of 4.2 mm and 2.1 mm, respectively, and is at least 35.8 mm long; the hole at the beginning of the furrow is rounded but slightly irregular, and measures 9.1 mm in diameter.
There are three other holes in the humerus. One of them has irregular borders, is located on the intercondylar groove (MPZ2019/1475; Fig. 4E) and is about 10 mm in diameter and 7.4 mm in maximum depth. The second one is isolated in the diaphysis (MPZ2019/1476; Fig. 4F), with a maximum depth of 7.6 mm and a diameter of about 9 mm. The third hole of the three is almost perfectly circular, with a diameter and a depth of 9.4 mm and 10.8 mm, respectively (MPZ2019/1478; Fig. 3G).
The left femur MPZ 2008/337 has many holes and other traces densely preserved in the epiphysis (Fig. 5). One of the holes is distinctive because of its circular, rounded edge ( Fig. 5E-G marked by an arrow; MPZ2019/1484), lacking any irregularity, with a diameter of 8.9 mm and a maximum depth of 6.7 mm.
The right femur MPZ 2007/711 is the most heavily bioeroded bone in the sample (Fig. 6), bearing so many trace fossils that it is difficult to distinguish them with confidence. However, some of them can be kept apart. Two furrows run parallel to each other from the distal epiphysis to the diaphysis; they extend parallel to the bone fibre and are more than 350 mm long (Fig. 6B, C; MPZ2019/1486 to MPZ2019/1487, both marked by an arrow).
To conclude, the trace fossil record in these Arenysaurus paratypes is characterised mainly by the presence of furrows and holes, and a few clear and welldefined notches, all of them rounded in crosssection, and more or less parallel to the surface in direction. Because these traces are mostly eroded and, in many parts, densely overlapping, it is difficult to assign them with confidence to an ichnotaxon. However, the general morphology and spatial distribution of the trace fossils allow them to be referred, tentatively, to the ichnospecies cf. Cuniculichnus seilacheri (see Supplementary data for more information on the ichnotaxonomy, Höpner & Bertling 2017).

Palaeoenvironment
The vertebrate-bearing site of Blasi-3 is located in a 1-m-thick, channelized, massive calcareous sandstone with abundant Ophiomorpha specimens. The sandstone containing bones has a complex depositional history influenced by a variety of factors. The site has yielded hadrosaurid bones that, as mentioned above, are present partially in anatomical connection (Arenysaurus) and partially disarticulated (indeterminate hadrosaurids), covering an area of about 70 m 2 (Fig. 2). Moreover, isolated fossils, such as turtle plates and crocodyliform bones, have also been recovered ( Fig. 7; López-Martínez et al. 2001;Murelaga & Canudo 2005).
The presence of bothremydid and solemydid turtles and crocodyliform remains suggests an aquatic palaeoenvironment. On the other hand, Ophiomorpha burrows are interpreted as being the products of crustaceans that lived near the coast (Boggs 1995).
Furthermore, the absence of bivalves suggests that water was not permanently present at the site. The occurrence of dry periods during the sedimentation of the Blasi-3 site is now also confirmed by the presence of bioerosion (Fig. 7).

Weathering stages
Hadrosaurid remains are concentrated in three main areas. The outcrop where the remains were recovered is sloping (at around 55°). The first area corresponds to the top of the slope (Fig. 2 grids 5D; 6C-D; 7), whereas the second area represents the central part of the site (Fig. 2  The right femur (MPZ 2007/711) is the most bioeroded bone, with almost its entire surface bearing traces, whereas the left femur (MPZ 2008/337) is partially preserved and only shows traces in the condyles. In the case of the right humerus (MPZ 2008/ 336), the traces are distributed over part of the diaphysis and the condyles. Finally, the scapula has only one surface that is bioturbated. These spatial distributions and the fact that the bones do not show signs of abrasion due to transport and only show flaking and cracking in restricted parts of the bones suggest that the bones were only partially exposed while the bioerosion took place, and that they hardly moved once they were deposited in the Blasi-3 site.
The external surfaces of the bones recovered in area 1 present weathering stages that are intermediate between the final stages of 'Stage 1' and early stages of 'Stage 2' weathering, as defined by Behrensmeyer (1978). The humerus MPZ 2008/336 presents a cracked and flaked surface along its length, which, according to Behrensmeyer (1978), suggests 'Stage 2'. The femur MPZ 2008/337 also presents a cracked and flaked surface, but less developed, which may indicate 'Stage 1' or early 'Stage 2' weathering. Regarding the scapula MPZ 2008/333a-333b, this bone element is less damaged but nevertheless has equally cracked and flaked surfaces. The damage is concentrated around the scapular neck, whereas the scapular lamina does not present any signs of weathering. This could mean that the scapula was partially buried while its weathering took place. In accordance with Behrensmeyer (1978), the features seen in the femur and the scapula thus indicate 'Stage 1' or early 'Stage 2' weathering.
The external surface of the femur MPZ 2007/711 recovered in the third area presents cracked and flaked surfaces in the middle and the distalmost parts of the bone, whereas the proximal parts have an undamaged surface. This suggests that the femur may have been partially buried, too, during subaerial weathering. These features of surface damage indicate 'Stage 1' or early 'Stage 2' weathering.

Discussion
Identity of the potential producer of the trace fossils at Blasi-3 There is an extensive record of trace-fossil-bearing bones preserved either in terrestrial and freshwater or in marine environments (e.g. Hasiotis 2004;Rouse et al. 2004;Britt et al. 2008;Höpner & Bertling 2017). Regarding trace-fossil-bearing bones preserved in marine environments as shown by Antonelli et al. 2019, with remains deposited in a possible tidal-plain, lagoonal or estuarine, with variable salinity, clearly contrasts with the presence of cracking and desquamation on the surface of the bioeroded bones of Arenysaurus. Even more, the absence of bivalve remains and the presence of burrows of Ophiomorpha indicates that the remains of Arenysaurus should not have been submerged under the water, but rather in an area near the coast with parts of the bones exposed to dry periods while bioerosion occurred.
Beetles, and more specifically the dermestids, are the most common tracemakers that produce pupation chambers (see references in Xing et al. 2015;Serrano-Brañas et al. 2018;Augustin et al. 2019). The first fossil record of dermestid beetles comes from the Late Cretaceous (Parkinson 2013). According to actualistic experiments performed by Zanetti et al. (2019), the dermestid beetles could produce pupation chambers on bones. Besides, it is known that dermestid larvae feed on carrion and perforate various durable substrates (wood and stone) during pupation (Hefti et al. 1980;Kirkland & Bader 2010;Holden et al. 2013;Zanetti et al. 2014Zanetti et al. , 2019. To infest a corpse, these insects need a carcase of a dead animal with dry skin and dried soft tissues (muscles, tendons, and cartilage), in other words to be in a dry stage of decomposition. At this stage, the carcase is above water and dry, and the bones are not buried quickly (Bornemissza 1957;Reed 1958;Coe 1978;Timm 1982;Hasiotis 2004;Serrano-Brañas et al. 2018;Augustin et al. 2019). Moreover, these insects are able to bore into cortical and spongy bone, producing pupation chambers, tunnels and furrows (Timm 1982;Jodry & Stanford 1992;Schroeder et al. 2002;Roberts et al. 2007;Britt et al. 2008;Huchet et al. 2013;Höpner & Bertling 2017). Our results suggest that most of the traces found in Arenysaurus were possibly produced by dermestid beetles.
However, experimental and/or additional observational data will be necessary to confirm it with confidence.

Taphonomic stage
Bioerosions give us information about the behaviour and biotic interactions of the organism that produced them and the palaeoenvironment in which it lived (Saneyoshi et al. 2011;Xing et al. 2013;Serrano-Brañas et al. 2018), as well as about the taphonomic history of vertebrate remains (e.g. Rogers 1992;Bader et al. 2009;Saneyoshi et al. 2011;Serrano-Brañas et al. 2018;Augustin et al. 2019Augustin et al. , 2021. In the Blasi-3 site, the sedimentological data show the presence of a massive deposit of immature sandstone, together with the spatial arrangement of the specimens and the different degrees of articulation and weathering stages of these remains ( Fig. 1-6; see Weathering Stages section). These data suggest that the carcase of Arenysaurus, partially decomposed, was possibly transported by a storm or similar event ( Fig. 7; Navarrete et al. 2014). During transport the carcase was fragmented, leaving an articulated part in the middle eastern and western section of the site (Fig. 2 grids 2 H-I; 3H-J, L; 5L, M; 6M-N); this was quickly buried and was not subject to attack from osteophagous insects. Meanwhile, the bones located in the top and middle parts of the sloping western section of the site were not buried or only partially so, as indicated by the distribution of the traces (i.e. On the other hand, the presence of bioerosions produced by insect activity only in some bones suggests that these were sub-aerially exposed above the water level for a certain period of time, allowing them to dry out (Behrensmeyer 1978). This is indicated by the presence of bioerosions produced by necrophagous insects such as the dermestid beetle, which colonises carcases only if they are sub-aerially exposed and at the dry stage of decomposition, which occurs several days or weeks after death (Fig. 7;Bornemissza 1957;Reed 1958;Martin & West 1995;Mariani et al. 2014;Augustin et al. 2021).

Conclusions
The bones of the hadrosaurid dinosaur Arenysaurus are the first that record the activity of necrophagous insects (cf. C. seilacheri) in the Maastrichtian of the Ibero-Occitan Plate. The fossil fauna recorded in the Blasi-3 site indicates that the Arenysaurus carcase was deposited in wide, shallow protected areas of variable salinity that are interpreted as a coastal environment. Our taphonomic reconstruction suggests that the Arenysaurus bones along with other indeterminate hadrosaurids were possibly transported by a storm or similar event, being partially fragmented and disarticulated during transport. The dinosaur remains were not buried or only partially so, with the sub-aerial exposure of the carcase lasting for at least several days or weeks resulting in the dry stage of decay that allowed the osteophagous insects to infest it. Dermestid beetles are proposed as the most probable tracemakers.