Ichnological evidence of Megalosaurid Dinosaurs Crossing Middle Jurassic Tidal Flats

A new dinosaur tracksite in the Vale de Meios quarry (Serra de Aire Formation, Bathonian, Portugal)preserves more than 700 theropod tracks. They are organized in at least 80 unidirectional trackways arranged in a bimodal orientation pattern (W/NW and E/SE). Quantitative and qualitative comparisons reveal that the large tridactyl, elongated and asymmetric tracks resemble the typical Late Jurassic-Early Cretaceous Megalosauripus ichnogenus in all morphometric parameters. Few of the numerous tracks are preserved as elite tracks while the rest are preserved as different gradients of modified true tracks according to water content, erosive factors, radial fractures and internal overtrack formations. Taphonomical determinations are consistent with paleoenvironmental observations that indicate an inter-tidal flat located at the margin of a coastal barrier. The Megalosauripus tracks represent the oldest occurrence of this ichnotaxon and are attributed to large megalosaurid dinosaurs. Their occurrence in Vale de Meios tidal flat represents the unique paleoethological evidence of megalosaurids moving towards the lagoon, most likley during the low tide periods with feeding purposes.

. Sedimentologically, the Middle Jurassic series from Portugal mainly include high-energy deposits originated in barrier-islands paleoenvironments and lagoonal and peritidal deposits formed within the protected areas of the internal back-barrier. Azerêdo et al. 18 suggested a depositional model for the Middle Jurassic of the Lusitanian Basin with an E/SE to W/NW carbonated-ramp system. During the Bajocian-Bathonian interval (Fig. 2), the eastern part of the basin was characterized by margino-marine and confined lagoon environments suggesting a system progradation from east to west 16 . The barrier island environment is represented by the Santo António-Candeeiros Formation, while the associated lagoonal and peritidal ones are represented by the Serra de Aire Formation. This last formation contains the Vale de Meios tracksite here reported, which is Bathonian in age after the occurrence of agglutinated foraminifera (i.e. Alzonella cuvillieri 19 ). Our sedimentological observations are in agreement with this scheme 16  No lamination is observed. Sparitic and micritic matrix are found, therefore this microfacies can be classified both as pelbiosparite and pelbiomicrite, respectively 23 . In fact, both kinds of matrix are observed in a single thin section (Fig. 4A,B). Fig. 4C,D). They correspond to mudstones 21 where ostracodes tests are abundant and foraminifera are absent. Micrite aggregates (peloids) are found and no strict pellets are observed. According to the components, this microfacies can be classified as pelbiomicrites 23 . Lamination is also visible in thin section (Fig. 4C) as clotted micrite layers with irregularly elongated, laminated fenestral pores (probably resulting from the deterioration of organic matter). This microfacies contains small isolated unimodal and euhedral relics of rhombohedrons, which are likley to have belonged to dolomite crystals 24 (see Fig. 4D).
As a general observation, both microfacies display no mud-cracking evidence, meaning that the tracking surface did not undergo a strong dessication and therefore the tracking surface was a moisture-laden sediment. This does not exclude that some initial dessication cracks may be present at the Vale de Meios tracksite. In any case, cracking due to dinosaur activity seems to be the number one cause of non-tectonic cracking.  theropod tracks (but more than 3,000 estimated) organized in more than 80 trackways (Fig. 3A). The trackways are long (trackway lengths range from 30 to 40 meters) and show straight (unidirectional) paths with a bimodal orientation pattern. From the directional analyses we distinguished more than 10% of the trackways with an E/SE orientation while the majority of the trackways following the opposite W/NW orientation. There are some crossing areas between different trackways; most of them correspond to crossing trackways orientated in opposite directions. No evidence of trackways turning back or re-crossing themselves have been observed. Description. Tracks are tridactyl, sometimes tetradactyl (hallux impression, Figs 6I,K and 7H), large (TL range from 22 cm to more than 80 cm), elongated (TL/TW ranges from 1.24 to 1.39) and asymmetric. The mesaxonic index ranges from weak mesaxony, implying a short developement of digit III or a longer distance between digit impressions II-IV to a stronger mesaxony, with a long development of digit III or shorter distance between digit impressions II-IV (anterior triangle l/w ranges from 0.26 to 0.48, Fig. 5A-F). They are featured by the general absence of clear pad impressions, although they do display them in tracks VMX.1 and VMX.2 (Fig. 5A′,B‴ and Supplementary Information for three-dimensional models), the presence of pointed claw marks, a slightly sigmoidal impression of digit III and a squared U-shaped metatarso-phalangeal impression. Interdigital angles are variable along a trackway, with general low values for both II^III and III^IV (minimum 22° maximum 40°) reflecting a minor parallelism of digits on the distal anterior half of the track. The difference between interdigital angles II^III and III^IV is usually less than 10°. Pace length and pace angulation are very irregular (e.g. in trackway VM1, pace length SD ± 19.6, pace angulation SD ± 9.01, Table 1), with an inward rotation of the distal end of digit III impression with respect to the trackway middle line. Trackways VM1 (24 tracks) and VM2 (28 tracks) are directed toward W/NW and measure 35 and 40 meters respectively, while trackway VM3 (29 tracks) is directed toward E/SE and it measures 30 meters in total lengths. See Table 1 for full measurements, Table 2 for average measurements and Supplementary Information for three-dimensional models.

The
Remarks. Tracks from the Vale de Meios tracksite are here compared with the main valid large theropod ichnotaxa regardless of the geography and time-period (Fig. 8). Kayentapus 26 (Fig. 8A) do not fit into the studied   slender digits and the larger interdigital angle. Besides some similarities in size and proportions of the 86-cm-long Tyrannosauripus pilmorei track 30 (Fig. 8D) and the recently erected new ichnogenus and ichnospecies Bellatoripes fredlundi 31 (Fig. 8E) from the Upper Cretaceous of North America, they differ from the Vale de Meios tracks especially on the robustness of the digit impressions, which are proximally wide and strongly taper distally, on the lack of a clear phalangeal pad formula and in wider metatarsal pad trace. The emended Bueckeburgichnus maximus track 32 (Fig. 8F) from the Lower Cretaceous of Germany is similar to the Vale de Meios tracks in size (TL: 56 cm) and in the medially-directed hallux impression, but they clearly differ in the presence of a more massive metatarsal area, in the lateral digits broadness and divergence of digit IV and in the longer digit III impression resulting in a stronger mesaxony (> 0.55) 33 . Eutynichnium lusitanicum 34 (Fig. 8G) is another large theropod described from the Late Jurassic of Portugal and diagnosed on the presence of an anteriorly oriented hallux, short metarsal and stocky and non taper digits impressions. Nontheless, in the few tetradactyl tracks preserved in the Vale de Meios tracksite, the hallux is medially oriented (Fig. 6I,K), the metatarsal is elongated (Fig. 7H) 34 ) and Morocco 36 (Fig. 8N) also recall the studied track morphologies.
For similarities with both qualitative and morphometric parameters of Megalosauripus uzbekistanicus together with the strong resemblance with the aforementioned Megalosauripus-like tracks, the Vale de Meios tracks are here assigned to Megalosauripus ichnogenus, representing the oldest occurrence of this ichnotaxon.
The assignment to Megalosauripus isp. is based on general morphology and morphometric ratios, irrespective of differences in the track lengths. Therefore, the intra-trackway track length variation discards the possibility that the site was crossed by a stock of taxonomically diverse theropods. This is the reason explaining that the track morphology remains the same among tracks with different sizes. As a result, isolated small-sized tracks could be the reflection of a high variety of preservational modes (due to different stages of substrate consistencies) or to different ontogenetic stages of the trackmakers. Finally, preservation of tracks could be strongly influenced by the tidal cycle, which produced preservations types such as modified true tracks and modified true tracks with mud collapsing through erosion and water saturation respectively. Tracks preservation. Only few tracks are considered well-preserved while the rest are morphologycally affected by substrate consistency changes or taphonomical processes transforming true tracks with anatomical details and preservation grade between 2 and 3 (following Belvedere and Farlow 37 ), into different gradients of modified true tracks according to water content, erosive factors (Fig. 6), primary features (i.e. radial fractures) and secondary features (i.e. internal overtrack formation, Fig. 7). Throughout the outcrop, no clear spatial distribution of these preservational types is observed. Tracks display three different types of taphonomic preservations: (1) True tracks with preservation grade between 2 and 3 ( Fig. 6A-D). Following Belvedere and Farlow 37 , this type of tracks is comprehended between grade 2, in which tracks preserve fairly clear and sharp toe marks, ungual marks and some digital pads recognizable and grade 3, in which all digit impressions are completely sharp and clear, digit walls well defined, ungual marks and distinct digital pads clearly preserved. As a result of the environmental setting, characterized by moist sediment, these types of tracks are not so common at the Vale de Meios tracksite (5%). (2) Modified true tracks (Fig. 6E-H). This type of preservation, as described in Marty 21 , is modified by physico-chemical (e.g.,weathering) and/or biological influences after they were made. It is the most abundant type of the site (75%), as it could be expected by the non-laminated nature of the tracking surface. Note that this preservation represents modified true tracks in the sense of Marty 20 and Marty et al. 38 , that is to say, the track is not morphologically overestimated due to depth propagation. (3) Modified true tracks with mud collapsing (Fig. 6I,L). These tracks result from water-saturated sediments and are evidenced by the collapse of the sediment inside the digits and ocasional metarsal and hallux impressions. It is remarkable that throughout VM1, VM2 and VM3 trackways, the degree of mud collapsing is variable, causing intra-trackway track length variability (sensu Razzolini et al. 39 ).
Preservation of tracks could be strongly influenced by the tidal cycle, which produced preservation grades such as modified true tracks and modified true tracks with mud collapsing through erosion and water saturation respectively.
All three preservation types can display two associated features: radial fractures and internal overtracks (Fig. 7). Radial fractures have been described in literature of general and experimental ichnology 20,38,40,41 . In the Vale de Meios tracksite, radial fractures are found in most of the tracks (Fig. 6 and 7A-D), are always normal to the profile of the print and develop preferentially from the claws outwards. Typically, more than 10 fractures per track are observed and they may branch out. They reach a longitude of up to 50 cm and the width of the open space is variable, but generally less than 0.5 cm. These structures are not strictly linked to the ocurrence of the displacement rims as it happens in other cases (Fig. 5E in Marty et al. 38 ). Other longer (centimeters to tens of meters) non-radial fractures are also observed (Fig. 7E).
Regarding internal overtracks (Fig. 7E-H, sensu Marty 20 ) they are very common and can also be found in all the three preservation types. Probably, the lack of this feature in some tracks is the result of recent removal during quarry works. A remarkable feature is that overtrack sediment wedges towards the edges of the track. The samples collected (Fig. 4C,D) revealed that the thin lamination of the sediment inside the track is due to microbial mats. The track bottom (true track sensu stricto) was covered with water during tidal events and the resulting internal overtrack was induced by repeated growth of microbial mats in the wetter track interior, by the trapping of sediment, or by an alternation of both processes. After the track formation, microbial mats developed preferentially within the tracks, as observed by the internal overtracks (Fig. 7E-H). This kind of overtracks has been commonly reported in other tidal environments 21,38,42 .
The relationship between tracks and associated features do not only provide a cross cutting sequence, but also clues to the origin of fractures. Non-radial fractures are tectonic joints, as supported by their length (up to tens of meters) and by the parallel disposition in joint families. Sometimes, non-radial fractures have calcite crystals infill. Additionally, non-radial fractures crosscut both the tracking surface and internal overtracks. In contrast, radial fractures never cut the internal overtrack, i.e. radial cracking is previous to the internal overtrack formation.
Trackmaker identification. The Vale de Meios trackmakers are large theropods or megatheropods as their estimated hip heights overpass the threshold (250 cm) proposed by some authors 33,43 and the footprint length exceed 45 cm 20,43,44 . These theropod tracks are among the largest theropod tracks described worldwide 30,31,45,46 . Nevertheless, other very large tracks are known. In general, trackmaker identity should reflect the least inclusive group that bounds all taxa sharing similar morphological characteristcs and spatiotemporal distributions. Therefore, in order to ascertain which group of theropods might be the best trackmaker candidate for the studied tracks, we reviewed the bone record of large-sized theropods in the Middle Jurassic of Europe. In the Iberian Peninsula, the osteological remains for this clade at that age are absent; out of this region, theropod osteological remains are recovered mainly from England (Duriavenator hesperis 47 ; Megalosaurus bucklandii 6 , Magnosaurus nethercombensis 7 ; Cruixicheiros newmanorum 8 ), France (Poekilopleuron bucklandii 4,5 ; Dubreillosaurus valesdunensis 3 ). They are all Bajocian-Bathonian in age and have been attributed to the Megalosauridae family, which is the dominant clade for the Middle Jurassic in Europe.
The synapomorphy-based correlation of the trackmakers depends on appendicular and pedal elements, which are usually lost during fossilization 48 . Plus, the osteological convergence and substantial overlap in phalangeal proportions of the theropod foot would not allow a lower level distinction among different theropod taxa 48 . Buckley et al. 49 indicate that tracks are not consistently preserved so as to reproduce the proportions of the trackmaker's foot with perfect fidelity, especially during animal locomotion. However, considering additional data such as the size and the provenance (taking into account both temporal and spatial distributions) 48 , there are no other possible candidates other than megalosaurids, as this is the unique group of large theropods capable to produce large tracks during the Bajocian-Bathonian times. Megalosaurid behaviour inferred from tracks. The orientation patterns of the trackways can provide useful information about the behaviour and habitat propensity of the trackmakers, especially if there is some preferred orientation of the trackways 50,51 . For example, Day et al. 11 reported various trackways at the Ardley Quarry, a Middle Jurassic tracksite with similar theropod tracks and trackways. The Ardley Quarry trackways display a degree of parallelism, suggesting that the trackmakers movements were either constrained by a linear geographical feature, or that they were moving in a herd. Generally, unidirectional orientation patterns, together with other parameters (similar locomotion velocity, regular intertrackway spacing, identical pace rhythm) are the best evidence to suggest gregarious behaviour among the trackmakers 31,52 . It is noteworthy that this kind of behaviour is not usually reported in large theropods on the basis of the footprint record [53][54][55][56] . Moreover, the presence of a huge number of large theropod footprints (more than 700 hundred) is highly uncommon in the fossil record and the Vale de Meios tracksite is therefore a rare site of great paleobiological and paleoethological relevance.
The detailed picture of the Vale de Meios tracksite shows an inter-tidal flat crossed normally by large theropods showing a general bimodal orientation pattern. The tidal flat is located in an inner platform (i.e. landwards edge of a lagoon, Fig. 9A) with a coastal barrier arranged in a E/NE-W/SW orientation. The majority of trackways (black colour, Fig. 3A) follows a W/NW orientation, toward the barrier (Fig. 9B). In contrast, the E/SE direction of trackways (red colour, Fig. 3A) is directed opposite, towards the land edge of the inner platform.
Bimodal orientation patterns have often been associated with physical features of the paleoenvironment such as the shoreline 57,58 and also to the paleogeographic conditions 59 . For instance, the most common condition found in fossil and modern trackways is that of trackways running parallel to the shoreline, typically linked to migratory animals moving from one area to another within the lake 51 . Besides, these authors suggested "shoreline position exerts a stronger influence on the distribution of animal activity than any other environmental factor".
Nevertheless, the opposite trend is observed for the Vale de Meios trackways where the bimodal orientation pattern is represented by trackways (the majority of them) directed perpendicular to the shoreline. In fact, 90% of the trackways is subparallel and are heading to the barrier while 10% of the trackways is heading opposite to the barrier (E/SE direction). Cohen et al. 51 also reported perpendicular trackways to the shoreline suggesting that animals can approach the margin of the lake to "drink, forage, or pass by (or, in the case of carnivores, to hunt herbivores doing any of the above)". Following Getty et al. 56 , if the subparallel orientation of the trackways is not caused by the gregarious behaviour, something else must have caused it. It should be noted that the parameters suggesting gregarious behaviour are not fully appreciable for the Vale de Meios trackways. Anyway, what seems clear is that the bimodal orientation pattern in the case of Vale de Meios is not related to the shoreline configuration as in the aforementioned papers. The sedimentological and taphonomic analyses together with data on the distribution and orientation of trackways permit us to infer theropod behavior throughout the tidal flat environment. Thus, the majority of trackways at Vale de Meios is likely to have been impressed during low tide periods, when the conditions to produce footprints are more suitable. The new surfaces exposed during the low tide periods favoured the preservation of footprints and the moisture-laden sediment counts for the variety of preservation modes (Fig. 6). A possible explanation for the direction of movement of the majority of trackways (black colour, Fig. 3A) is that of megalosaurids crossing the exposed area of the tidal flat when the water recides, that is to say during low tide periods. This hypothesis is based on the strong directionality (and bimodality) in theropod paths, normal to the barrier. The long linear trackways across the site represent a directional pattern (sensu Cohen et al. 51 ) suggesting that the megalosaurids cross the tidal flat with a precise purpose (not milling).
The unusual behaviour of large theropods moving toward the coast had not been previously documented and entails the possibility that megalosaurids invaded the area to feed on fish, invertebrates and other vertebrates exposed on the tidal surface. Although there are examples in literature of gregarious behaviour in large theropods supported through both bonebeds 60 and trackways 31 , it has been usually suggested that large theropods were solitary hunters 61,62 The numerous trackways might represent few individuals crossing the tidal flat recurrentely. In fact, some reports of theropods moving towards and away from the shoreline have been considered possible evidence of piscivory 58 or feeding on other vertebrate carcasses (sensu Roach and Brinnkman 63 and contra Ostrom 53 ).
The inferred piscivory diet of megalosaurids is not unexpected and has been documented by stomach contents in Poekilopleuron 64 . Allain 3 stated that the inclusion of fishes as part of the megalosaurid diet is consistent with both taphonomic and phylogenetic data. Moreover, the deposits yielding the described megalosaurid taxa indicate paralic and shallow marine environments, including marine-influenced lagoon 9 and coastal mangrooves grounds 3 . These data combined with the trackway evidence from Vale de Meios may suggest that megalosaurids frequented this palaeonvironment, and similar to spinosaurids, would have been opportunistic carnivores, feeding on terrestrial vertebrates but also on fishes. In this regard, the long trackways documented at Vale de Meios tracksite reveal a stock of large megalosaurids moving to the shoreline and back from the land to the coastal barrier and invading new exposed areas of the tidal flat. The reason of such striking behaviour could be the occasional piscivory diet of megalosaurids, as these large theropods would take advantage of new exposed areas to feed on fishes and other vertebrates.

Conclusion
The Vale de Meios limestone quarry from the Serra de Aire Formation, Bathonian in age (Santarém, West-Central Portugal) is a key and unique reference for understanding the composition and distribution of the Middle Jurassic theropod fauna, especially due to both the ichnological and osteological record for this age being extremely scattered. In this study, tracks and trackways from the whole tracksite are assigned to Megalosauripus isp. according to quantitative and qualitative analyses and comparisons undertaken. This ichnogenus occurrence, traditionally reported for the Late Jurassic-Early Cretaceous, should therefore be expanded also to the Middle Jurassic. The Vale de Meios tracks are among the largest theropod tracks ever reported, and they were produced by large individuals of the Megalosauridae family, the dominant tetanuran clade during this age in Europe. Furthermore, this is the first tracksite in which Megalosauripus is in a probable coincident correlation with megalosaurids. The directional analyses of trackways, which are preserved in an inter-tidal flat located at the edge of a lagoon, reveals that various individuals crossed a tidal flat in accordance to tide cycles, directing toward the barrier during low tide periods, probably for feeding purposes on exposed vertebrate. Such clear bimodal orientation arrangement (forth and back) interpreted as single or small aggregates of large theropods individually moving toward a carcass on the shoreline is highly uncommon as it is the presence of such a large number of large theropod footprints.