Abstract
Macronaria, a group of mostly colossal sauropod dinosaurs, comprised the largest terrestrial vertebrates of Earth’s history. However, some of the smallest sauropods belong to this group as well. The Late Jurassic macronarian Europasaurus holgeri is one of the best-known sauropods worldwide. So far, the braincase material of this taxon from Germany pended greater attention. With the aid of microCT, we report on the neuroanatomy of the almost complete braincase of an adult individual, as well as the inner ears of one other adult and several juveniles (also containing so far unknown vascular cavities). The presence of large and morphologically adult inner ears in juvenile material suggests precociality. Our findings add to the diversity of neurovascular anatomy in sauropod braincases and buttress the perception of sauropods as fast-growing and autonomous giants with manifold facets of reproductive and social behavior. This suggests that – apart from sheer size – little separated the island dwarf Europasaurus from its large-bodied relatives.
Introduction
Sauropoda is a taxon of saurischian dinosaurs and comprise popular taxa like Diplodocus, Giraffatitan and Argentinosaurus1. Sauropods were diverse and successfully distributed worldwide (e.g.1, 2).The oldest indubitable sauropod taxa are known from Early Jurassic strata; the youngest representatives went extinct during the end-Cretaceous disaster2. Whereas bipedal early sauropodomorphs (in which sauropods are phylogenetically nested) were probably capable of swiftly tracking down prey3, the later evolutionary history of the group is characterized by an unrivaled increase in body size (among land-dwelling vertebrates), accompanied with herbivory, an extreme elongation in neck length and graviportal quadrupedality (e.g.1, 4, 5).
While fossil braincases are generally rare, studies of sauropod endocrania are surprisingly numerous (e.g. 6,7,8), serving as a good base for comparisons. Potentially, aspects of lifestyle can be inferred from certain morphological details of cavities that once contained the brain, inner ear and other associated neurovascular structures within the bony braincase of vertebrates (e.g.9,10,11,12). Furthermore, ontogenetically induced morphological shifts of neuroanatomy can hint towards different ecological tendencies within a species, for example, in respect to bipedal or quadrupedal locomotion13.
The middle Kimmeridgian (Late Jurassic) sauropod Europasaurus (represented by a single species, E. holgeri) is regarded as an unequivocal example for insular dwarfism with paedomorphic features, having reached adult body lengths of nearly 6 metres and weighing about 800 kg14,15,16,17. From this taxon, a great number of cranial and postcranial fossil bones are known (housed in the Dinosaurier-Freilichtmuseum Münchehagen/Verein zur Förderung der Niedersächsischen Paläontologie e.V., Rehburg - Loccum, Münchehagen, Germany), of which the former hint to at least 14 individuals of different ontogenetic stages17.
The paratype specimen of Europasaurus, DFMMh/FV 581.1, comprises a largely complete, articulated and probably mature braincase, with DFMMh/FV 581.2 & 3 representing the respective detached parietals (Figs. 1–3; Supplementary Figs. 1–4). The outer morphology of this material has previously been described17. For this study, the parietals were put in their place on the remaining endocranium and subsequently documented with microCT. The endocranial cavities which once housed the brain, inner ears and other soft neuroanatomical structures, such as nerves and blood supply, were manually segmented. The articulated specimens DFMMh/FV 581.1, 2 & 3 measure about 120 mm in mediolateral width, 80 mm anteroposteriorly and 100 mm dorsoventrally.
Additionally, the specimens DFMMh/FV 1077 (Fig. 4; Supplementary Figs. 5, 6; adult fragmentary braincase, complete inner ear), DFMMh/FV 466+205 (Figs. 5, 6; Supplementary Figs. 7–11; juvenile prootic and otoccipital, nearly complete inner ear; the common bond of these two specimens has not been recognized in former studies17), DFMMh/FV 964 and DFMMh/FV 561 (Fig. 7; Supplementary Figs. 8, 9; prootics of uncertain maturity, anterior labyrinth), DFMMh/FV 981.2, DFMMh/FV 898 and DFMMh/FV 249 (Fig. 8; Supplementary Figs. 10, 11; juvenile otoccipitals, posterior labyrinth) were documented with microCT. Since the isolated specimens contain different parts of the endosseous labyrinths, cranial nerves and vascular cavities, the respective digital models were reconstructed in order to describe, compare and contextualize their characteristics. Whereas the smallest of these specimens (DFMMh/FV 898) hints to an approximate posterior skull width of under 5 cm, the largest specimens DFMMh/FV 581.1 and DFMMh/FV 1077 suggest a maximum mediolateral width of about 14 cm.
The microCT data and our digital reconstructions (Europasaurus holgeri - neuroanatomy - DFMMh/FV - Schade et al. 2023 // MorphoSource) of different Europasaurus individuals add to the knowledge of diversity of dinosaur neuroanatomy and allow a better understanding of ontogenetic development. We discuss our findings in context of insights into the lifestyle of this long-necked insular dwarf from the Late Jurassic of Germany.
Results
Cranial endocast, innervation and blood supply
As is generally the case in non-maniraptoriform dinosaurs (e.g.8, 18, 19), many characteristics of the mid- and hindbrain are not perceivable with certainty on the braincase endocast of DFMMh/FV 581.1 (Fig. 1A), which implies scarce correlation of the actual brain and the inner surface of the endocranial cavity (see20 for ontogenetic variations in recent archosaurs).
The endocast suggests low angles in the cerebral and pontine flexures. There is a prominent dorsal expansion, spanning from around the posterodorsal skull roof to approximately the anteroposterior mid-length of the endocast (Figs. 1, 2). In posterior view, the dorsal expansion is T-shaped with a more or less straight top and dorsolateral beams that become dorsoventrally higher and gradually lead over anteriorly to the area where the posterior part of the cerebral hemispheres are expected. In lateral view, the posterior-most extent of the dorsal expansion is separated from the dorsal margin of the medulla oblongata by a concavity.
Anterolaterally to this concavity, the eminence for the vena capitis media is present. Although the respective openings are identifiable on DFMMh/FV 581.1 (close to a kink on the posterodorsal contact between the parietals and the supraoccipital, called ‘external occipital fenestra for the caudal middle cerebral vein‘ in17), it was only roughly possible to reconstruct the course of the veins (Figs. 1, 3). There is a large semicircular depression on the posterodorsolateral aspect of the endocast, being anterodorsally bordered by the dorsal expansion and anteroventrally by the eminence of the vena capitis media. On the anterodorsal skull roof, a mediolateral expansion of the endocast possibly marks the position of the cerebral hemisphere (Figs. 2, 3). In lateral view, there is a distinct ventral step on top of the endocast (also present in many other sauropod taxa; see e.g.7, 21, 22), between the anterior-most part of the dorsal expansion and the posterior part of the cerebral hemispheres, followed by a slight ascent in anterior direction. The left side of the endocast suggests that the cerebral hemisphere impressions are delimited approximately by the contact between the orbitosphenoid and the laterosphenoid anteriorly, and by the trochlear nerve (CN IV) ventrally. Anteriorly, the orbitosphenoid bears a prominent medial incision for the optic nerve (CN II). Posteroventrally to the optic nerve canal and anteroventrally to the trochlear nerve canal, the canal of the oculomotor nerve (CN III) is situated. On the anteroventral aspect of the endocast, the pituitary reaches about as far ventrally as the ventral-most margin of the medulla oblongata, producing an angle of about 50° to the lateral semicircular canal of the endosseous labyrinth (see23). On the anterodorsal aspect of the pituitary, two small and dorsolaterally diverging canals of uncertain identity branch off (Figs. 1–3; Marpmann et al.17 labeled the openings as carotid artery: Fig. 13D). In the titanosaur specimen CCMGE 628/12457 and Sarmientosaurus, structures of a similar position were identified as sphenoidal arteries24, 25. However, in Bonatitan and the titanosaur braincase MPCA-PV-80, anterolateral openings on the pituitary, close to the abducens nerve (CN VI) canal, have been assigned to canals leading to the adenohypophysis7. Posterolaterally to these canals, the abducens nerve (CN VI) canals trend in an anteroposterior direction (Figs. 1–3; Supplementary Figs. 1–3). The specimen DFMMh/FV 581.1 suggests a natural connection between the pituitary fossa and the left CN VI canal, close to its anterior opening. This condition may be due to breakage, since the microCT data suggests a continuous wall on the right side. In ventrolateral view, the left side of DFMMh/FV 581.1 shows an additional small medial opening dorsally within the depression for CN VI (Figs. 2A,B, 3C,D; Supplementary Figs. 1–3). This opening seems natural, but for preservational reasons, this cannot be confirmed on the right side of the specimen. On the ventrolateral part of the pituitary, two short canals of uncertain identity are branching off ventrolaterally (Figs. 1–3; Supplementary Fig. 1; in Bonatitan, anterolateral canals on the ventral portion of the pituitary have been identified as leading to the neurohypophysis7). Directly behind, the pituitary bears the long internal carotid canals, branching off ventrolaterally as well.
The endosseous labyrinth is situated within an anteroventrally inclined lateral depression of the endocast, directly ventral to the vena capitis media eminence. Here, an opening is present, leading to the medial aspect of the common crus in DFMMh/FV 581.1 and 1077 (the opening is considerably larger in the latter specimen; Figs. 4, 6; Supplementary Figs. 4, 6).
Whereas the trigeminal (CN V), facial (CN VII) and vestibulocochlear (CN VIII; two openings) nerve canals are mainly anterior to the endosseous labyrinth, the vagal foramen (=jugular foramen for CN IX-XI and jugular vein) and two canals for the hypoglossal nerves are situated posterior to the cochlear duct (Figs. 1–3). Within the depression for CN V, dorsally, a very small opening for the mid cerebral vein is situated on both sides of DFMMh/FV 581.1. However, only the right canal could approximately be reconstructed (Figs. 1A, 2A). Dorsal to the right slit-like opening for CN VII, a small depression is present in DFMMh/FV 581.1.The microCT data do not suggest penetration. Whereas the posterior canals for the hypoglossal nerve (CN XII) are clearly discernable in the microCT data, the anterior ones are not as obvious to detect.
However, because of the expression of their respective openings on the actual fossil, their course could be established (anterior to the proximal openings of the anterior CN XII canals, one depression each is visible on the fossil, however, the microCT data do not suggest a penetration). Marpmann et al.17 only identified one hypoglossal canal (CN XII). However, the specimens considered herein, support the presence of two openings on each side.
Anterodorsally to the endosseous labyrinth, the cerebellum seems perceivable as a mediolaterally expanded part of the endocast, almost reaching the trigeminal nerve (CN V) anteriorly and being delimited by the eminence of the vena capitis media posterodorsally (Fig. 1A). Furthermore, a small floccular recess is present close to the mid-length of the anterior semicircular canal in DFMMh/FV 581.1. The ventral aspect of the endocast is anterodorsally inclined and bears a medial ridge (Figs. 1A, 2C, 3A) becoming mediolaterally narrower in anterior direction), reaching between the foramen magnum and the anteroventral portion of the endocast (excluding the pituitary). Posteroventral to the abducens nerve (CN VI), a single median protuberance is present on the endocast, produced by a fossa on the floor of the endocranial cavity (Figs. 2C, 3; Supplementary Figs. 2, 3). In addition, anterodorsally to the proximal openings for the abducens nerve (CN VI), a single median opening is present on the braincase floor, producing a connection to the pituitary fossa (probably for vascularization; see7, 24 for arguments on arterial or venous identity). The general osteological configuration of the endocranial floor (Supplementary Figs. 2, 3) seems very similar in the macronarian Giraffatitan (6: Fig. 117). The anterodorsally incomplete endocranial cavity of DFMMh/FV 581.1, 2 & 3 comprises a volume of about 35 cm3 (including the pituitary fossa). A small funnel-like depression anterior to the occipital condyle on the ventral aspect of DFMMh/FV 581.1 ends blindly (Fig. 2D).
Endosseous labyrinth
Both vestibular systems are preserved and are ventrally connected to the respective cochlea in DFMMh/FV 581.1 (the semicircular canals of the left inner ear were only vaguely perceptible in some places). Whereas only the left endosseous labyrinth is preserved in DFMMh/FV 1077, only the right one is contained within DFMMh/FV 466+205. The following description is based on the mentioned endosseous labyrinths (Fig. 6). The vertical semicircular canals are relatively long and slender. Dorsoventrally, the anterior semicircular canal reaches considerably higher than the posterior one, and the ASC occupies more of the anteroposterior length of the vestibular system. The common crus is dorsally slightly posteriorly inclined (where preserved). While the PSC forms a low arc, the ASC turns about 180° to contact the common crus dorsomedially. The medial aspect of the common crus is exposed to the endocranial cavity in DFMMh/FV 581.1 and DFMMh/FV 1077 (Figs. 4, 6G; Supplementary Figs. 4, 6). The angle between the ASC and the PSC amounts 80° (measured in dorsal view with the common crus as fixpoint). The lateral semicircular canal is anteroposteriorly short. In dorsal view, its anterior ampulla appears posteriorly shifted, producing a medially concave gap between the ASC and LSC (Fig. 6B,F,J). Such a medial concavity is also present between the LSC and the PSC (best seen in dorsal view). The cochlear duct is approximately as high as the vestibular system dorsoventrally, points anteroventrally and very slightly medially (in DFMMh/FV 581.1 and 1077). In lateral view, the cochlear duct is anteroposteriorly slender with sub-parallel anterior and posterior margins. However, mediolaterally, the cochlear duct is very wide, resulting in an elongated oval-shaped cross section. The fenestra ovalis (Figs. 1A,B, 2A,B, 6; Supplementary Fig. 5) is situated close to the dorsoventral mid-length of the lateral aspect of the cochlear duct (in DFMMh/FV 581.1 and DFMMh/FV 1077).This is also true for the anteroposteriorly oriented fenestra pseudorotunda (Figs. 4, 6D; Supplementary Fig. 4), lying on the posteromedial aspect of the cochlear duct. The hiatus acusticus expresses as an anteromedially open notch (similar to the theropod Irritator challengeri26) on the actual fenestra pseudorotunda in DFMMh/FV 581.1 (Supplementary Fig. 4).
Auditory capabilities
To get a rough idea of the audition of Europasaurus, we measured the dorsoventral cochlear duct length of DFMMh/FV 581.1 (c. 16 mm; as outlined by27) and the anteroposterior basicranial length (c. 55 mm; from the anterodorsal part of the pituitary fossa to the posterior-most part of the occipital condyle). Based on the equations of27, we assume the mean hearing frequency of Europasaurus as 2225 Hz and the frequency bandwidth as 3702 Hz (374–4076 Hz).
Inner ears and cavities of incomplete specimens
In addition to DFMMh/FV 581.1, 2 & 3 (Figs. 1–3, 6A–D; Supplementary Figs. 1–4), eight other braincase specimens (that hold parts of the endosseous labyrinth), assigned to Europasaurus, were scanned. DFMMh/FV 1077 (Figs. 4, 6E–H; Supplementary Figs. 5, 6) contains a complete left endosseous labyrinth and was categorized as belonging to an osteological mature individual in Marpmann et al.17 (as DFMMh/FV 581.1, 2 & 3). Furthermore, there are two right elements (Figs. 5, 6I–L, 7A,B, 8G,H; Supplementary Figs. 7, 8A,B, 9A, 10G,H, 11E; DFMMh/FV 205, a fragmentary otoccipital, and DFMMh/FV 466, a fragmentary prootic) that were originally found some 10 cm apart from each other in the sedimentary matrix. Whereas DFMMh/FV 205 was thought to belong to a juvenile, DFMMh/FV 466 was supposed to belong to a considerably older individual (both estimations mainly based on size and surface texture17). However, DFMMh/FV 205 and DFMMh/FV 466 articulate well with each other and jointly contain most of the endosseous labyrinth and the dorsal portion of the lagena, all in a meaningful manner in respect to size, position and orientation of its compartments. DFMMh/FV 466 is of similar size and texture as the other prootics considered here. DFMMh/FV 205 is considerably smaller than the otoccipitals in the adult specimens. Hence, DFMMh/FV 466+205 are herein interpreted to belong to the same juvenile individual. Furthermore, there are two left fragmentary prootics (Fig. 7C–F; Supplementary Figs. 8C–F, 9B,C; DFMMh/FV 561 and DFMMh/FV 964) containing most of the ASC, the ventral base of the common crus, the anterior ampulla of the LSC and the anterior base of the lagena; both specimens were assigned to relatively mature individuals17.
The three right fragmentary otoccipitals DFMMh/FV 249, DFMMh/FV 898 and DFMMh/FV 981.2 (Figs. 8A–F; Supplementary Figs. 10A–F, 11A–D) contain at least the posterior parts of the LSC and the lagena, as well as most of their PSCs; these specimens were assigned to immature individuals17.
In general, the morphology of the inner ears contained within these isolated specimens corresponds to what can be observed in DFMMh/FV 581.1 and DFMMh/FV 1077. Since Marpmann et al.17 used the vascularization (indicated by surface texture) of Europasaurus specimens as a critical character in judging the relative maturity, the inner cavities surrounding the endosseous labyrinths were examined herein.
No discrete cavities could be found in DFMMh/FV 581.1, DFMMh/FV 1077, DFMMh/FV 964 and DFMMh/FV 561 (all considered to represent more or less mature individuals).The otocipitals DFMMh/FV 249, DFMMh/FV 898 and DFMMh/FV 981.2 and the articulated specimens DFMMh/FV 205 (otoccipital) and DFMMh/FV 466 (prootic) show very similar, or corresponding, patterns of inner cavities (Figs. 7, 8; Supplementary Figs. 9, 11). All four otoccipitals show dorsoventrally deep cavities posterodorsal to anteromedial to the PSC, close to the articulation surface with the supraoccipital (except for DFMMh/FV 205, in which this cavity network is not as much extended anteriorly). There are T- (DFMMh/FV 898 and DFMMh/FV 981.2), V- (DFMMh/FV 205), or X- (DFMMh/FV 249) shaped (in cross-section in anterior view), dorsoventrally high and mediolaterally thin structures anterior to the PSC and dorsal to the LSC (close to the articulation surface with the prootic). Additionally, all four otoccipital specimens bear relatively small cavities ventral to the LSC (again, close to the articulation surface with the prootic). DFMMh/FV 981.2 shows dorsoventrally high cavities posteroventrally to the endosseous labyrinth (close to the articulation surface with the basioccipital). Generally, the cavities, likely of vascular purpose, of DFMMh/FV 205 seem not as large and extensive as in the other three otoccipitals. This coincides with their size and assumed relative maturity (DFMMh/FV 205 being the largest, smoothest and, hence, most mature of them17). Whereas DFMMh/FV 466 bears a small cavity ventral to the LSC (corresponding to the respective cavity in the otocipital DFMMh/FV 205), no other unequivocal cavities could be found, which is surprising when the V-shaped cavity close to the prootic contact of DFMMh/FV 205 is considered.
Discussion
Comparison of neurovascularanatomy and potential ecological implications
Although not as prominent as in Dicraeosaurus6, 28 and some specimens of Diplodocus29, the position and morphology of the dorsal expansion of Europasaurus, gives a rather ‘upright’ or sigmoidal appearance to the endocast (Fig. 1A; see also23). This is partly explained by the (preservational) lack of its olfactory bulb and tract. The first cranial nerve is not expected to be very prominent in many sauropods, especially in the closely-related macronarian taxa Camarasaurus and Giraffatitan21, 29. In contrast, the braincase endocast is rather tubular in some taxa, e.g. the early-diverging sauropodomorph Buriolestes3, the rebbachisaurid Nigersaurus taqueti30, and the titanosaur specimen MCCM-HUE-16678. Instead, the endocast of Europasaurus seems to be most similar to Giraffatitan6, 21 (formerly Brachiosaurus brancai).
Different from some other sauropod taxa (e.g., Spinophorosaurus, Diplodocus, Camarasaurus and Sarmientosaurus; see25, 29, 31), there are no discrete canals for vascular features such as e.g., the rostral middle cerebral vein or the orbitocerebral vein on the endocast of Europasaurus.
A ventral ridge on the medulla, as seen in Europasaurus (Figs. 1A, 2C, 3A), seems to be present, although not as pronounced, in Thecodontosaurus32, the early-diverging sauropod specimen OUMNH J135965, Spinophorosaurus31, Camarasaurus29 and, potentially, Giraffatitan6, 21 as well.
Although not obvious on the endocast21, Giraffatitan seems to bear a median fossa posteromedially to the proximal CN VI openings (6: Fig. 117); the respective protuberance in Europasaurus marks a distinct kink on the endocast (Figs. 2C, 3; Supplementary Figs. 2, 3).
The endocast of Europasaurus bears two pairs of canals on the ventrolateral aspect of the pituitary, the posterior of which is interpreted to represent the internal carotid here (Figs. 1A, 2, 3; Supplementary Fig. 1; in accordance to Marpmann et al.17: Fig. 13A). Whereas structures identified as the craniopharyngeal canal are present anterior to the carotid artery in the titanosaur specimen CCMGE 628/1245724 and the diplodocid specimen MMCh-Pv-232 (assigned to Leinkupal33), it is situated posteriorly in Apatosaurus34 (see also7, 35 for the – in respect to the internal carotid – anteriorly situated canal of the subcondylar foramen in Amargasaurus). However, in these taxa, the craniopharyngeal canal is a singular median canal. This may render the anterior of the two pairs of canals on the ventral aspect of the pituitary in Europasaurus the canals for the neurohypophysis7. The pituitary of the Europasaurus endocast of DFMMh/FV 581.1 does not project much more ventrally than the posteroventral margin of the medulla oblongata. The pituitary is slightly higher dorsoventrally than the anterior semicircular canal (Fig 1A). Usually in sauropods, the pituitary is large and inclined posteroventrally, reaching much more ventrally than the ventral margin of the hindbrain (see e.g. 21, 25; see24 for an extreme reached in the titanosaur specimen CCMGE 628/12457 with a short anterior semicircular canal and an enormous pituitary). The finding of a relatively small pituitary fossa in Europasaurus and early-diverging sauropodomorphs seem to support a close connection of body and pituitary size3, 36. The microCT data of DFMMh/FV 581.1 suggest that the right CN VI canal closely passes by the pituitary fossa without a penetration, whereas the left CN VI canal tangents on the pituitary fossa and opens into the latter (Supplementary Fig. 3). The feature of the CN VI canals not penetrating the pituitary seems typical for titanosaurs (e.g.7, 8, 23). Whereas Knoll & Schwarz21 note such a penetration or connection on the endocast of MB.R.1919, Janensch6 originally described penetrating canals in the Giraffatitan specimens t 1 and Y 1.
However, the specimen S 66 seems to show CN VI canals rather passing by the pituitary fossa. This may suggest a certain role of individual expressions (Giraffatitan), asymmetries (Europasaurus) and/or represents a phylogenetically potentially reasonable intermediate state (however, this feature may also be prone to preservational bias).
The endosseous labyrinth of Europasaurus (Fig. 6) is most similar to Giraffatitan6 and Spinophorosaurus31 in bearing a relatively long ASC and a long lagena. In dorsal view, the anterior ampulla of the short LSC in Europasaurus displays a medially concave gap between the ASC and LSC (Fig. 6B,F,J). Similarly, a pronounced concavity is present between the LSC and the PSC (best seen in dorsal view). Both concave gaps (the ASC and the PSC project further laterally than the lateral outline of the LSC reaches medially) are similarly present in many Titanosauriformes (with the exception of FAM 03.06437): Giraffatitan6, Malawisaurus38, Sarmientosaurus25, CCMGE 628/1245724, Jainosaurus38, Ampelosaurus22, Narambuenatitan23, Bonatitan, Antarctosaurus, MCF-PVPH 765 and MGPIFD-GR 1187, but also in the rebbachisaurids Limaysaurus and Nigersaurus39. In contrast to other sauropods, the anterior portion of the LSC, as well as its lateral-most extent (best seen in dorsal view) seems somewhat posteriorly shifted in the macronarians Camarasaurus29 and Europasaurus (Fig. 6B,F,J; for further discussion see Supplementary Information).
Although the mediolateral width of the lagena seems not associated with auditory capabilities27, the lagena of Europasaurus is conspicuously thick mediolaterally, especially when compared to its anteroposterior slenderness (Fig. 6). The calculated auditory capacities (based on27) impute Europasaurus a relatively wide hearing range with a high upper frequency limit (among non-avian dinosaurs40,41,42). Walsh et al.27 could show a certain correlation between hearing range, complexity of vocalizing and aggregational behaviour in extant reptiles and birds (see also12, 43). Following this, it appears plausible that Europasaurus lived in groups with conspecifics, which made airborne communication crucial. However, while a given species is likely to perceive sounds within the frequency spectrum it is able to produce, it may be rather unlikely that the full range of frequencies that can be heard is covered by the sound production ability (see27, 44). Habitat preferences potentially play a role as well: ‘acoustically cluttered’ habitats like forests seem associated with a tendency towards high frequency intraspecific communication in recent mammals45. Together with tropic Late Jurassic conditions in Europe46, this may be part of the explanation of the recovered auditory capacities of Europasaurus.
Fragmentary bones and their eco-ontogenetic meaning
An interesting issue are the different morphological ontogenetic stages of DFMMh/FV 466 and DFMMh/FV 205 stated in Marpmann et al.17. The authors considered the prootic DFMMh/FV 466 more mature than the otoccipital DFMMh/FV 205. Indeed, DFMMh/FV 466 is about as large as the prootics of DFMMh/FV 581.1, DFMMh/FV 1077, DFMMh/FV 964 and DFMMh/FV 561 (Fig. 7; Supplementary Fig. 8), but the otoccipital DFMMh/FV 205 is much smaller than the ones in DFMMh/FV 581.1 and DFMMh/FV 1077 (and only slightly larger than DFMMh/FV 981.2, DFMMh/FV 898 and DFMMh/FV 249; Fig. 8; Supplementary Fig. 10).
In addition to general size of the specimens, and build and rugosity of articular facets, Marpmann et al.17 (see also47) defined the morphological ontogenetic stages also by bone surface smoothness, advocating for vascularization: the smoother the surface, the lesser the degree of vascularization and – in tendency – the more mature the individual bone. Our findings support this (Figs. 7, 8; Supplementary Figs. 9, 11). While the bases of individual cavities described herein may represent depressions of articulation areas, their deep penetration into the bone is unambiguous. Apart from this, the described structures might represent sutures.
However, the position and orientation of individual cavities do not conform to what would be expected. Since these cavities make sense in the frame of morphological ontogenetic stages used in Marpmann et al.17, they are considered as so far unknown vascular expressions of juvenile Europasaurus individuals here.
DFMMh/FV 466 and DFMMh/FV 205 articulate very well with each other, especially on their lateral aspects. Additionally, there are cavities ventral to the LSC that seem to have been continuous originally (Figs. 5, 7A,B, 8G,H; Supplementary Fig. 7). However, whereas the fenestra ovalis is considerably smaller than the vagal foramen in DFMMh/FV 581.1 and DFMMh/FV 1077 (Fig.3B; Supplementary Fig. 5A), it seems that in DFMMh/FV 466+205 this is vice versa (although this impression may be due to the fragmentary nature of the latter two specimens; Fig. 5L; Supplementary Fig. 7F). If DFMMh/FV 466 and DFMMh/FV 205 are in articulation, there is a large gap on their common dorsal aspect (Fig. 5J; Supplementary Fig. 7H). Considering DFMMh/FV 581.1 and DFMMh/FV 1077 and e.g., the braincase of Massospondylus48, the supraoccipital usually occupies this gap. In case our interpretation of a common bond between DFMMh/FV 466 and DFMMh/FV 205 is misleading and they actually represent two differently-matured individuals, it is still noticeable that the preserved parts of the conjoined endosseous labyrinth of DFMMh/FV 466 and DFMMh/FV 205 display the same features as DFMMh/FV 581.1 and DFMMh/FV 1077 and is anteroposteriorly almost as long as the latter two specimens (Figs. 5, 6; Supplementary Table 1). This suggests an allometric growth between the prootic and otoccipital: during growth, the prootic reaches the ‘adult’ size faster than the otoccipital, producing a surprisingly small paroccipital process (or a surprisingly large prootic) in juvenile individuals of Europasaurus (seemingly, also seen in Massospondylus49), containing a relatively large endosseous labyrinth (see also50 for ontogenetic transformations in sauropodomorphs). A relatively large immature endosseous labyrinth is also present in the ornithischians Dysalotosaurus lettowvobecki51, Psitaccosaurus lujiatunensis13 and Triceratops52. Furthermore, the inner ear is relatively large in juveniles of Massospondylus53 and the extant, precocial ostrich54, and stays morphologically relatively stable throughout ontogeny.
The vestibular apparatus detects movements with the aid of endolymphatic fluid and cilia contained within the semicircular canals, which is crucial for locomotion55. Thus, a relatively large and morphologically adult-like endosseous labyrinth in expectedly very young individuals of Europasaurus suggests that hatchlings had to be light on their feet very fast in this dwarfed sauropod taxon.
Conclusion
Europasaurus has a rather sigmoid general braincase endocast shape, with a comparably large dorsal expansion, two openings for CN XII, an angle of 50° between the pituitary fossa and the LSC, and the ASC is clearly dorsoventrally higher than the PSC (Figs. 1–4, 6). This and additional novel details, such as the highly uniform vascular cavities within the juvenile braincase material (Figs. 7, 8; Supplementary Figs. 9, 11) add to our knowledge about dinosaur neuroanatomy. The relatively small pituitary fossa (Fig. 1A) in an insular dwarf lends support to the idea of being a proxy for body size36.
Many sauropods were extremely large land-dwellers as adults, and still, started as tiny hatchlings, indicating enormous growth rates (e.g.56,57,58). The threat arising from the discrepancy of several tens of tons between adults and juveniles makes it, among other reasons, unlikely that these animals were able to take good care of their offspring (e.g.4, 58).This implies a great mobility early in life (precociality in a broader sense59) of sauropods. Although Europasaurus represents an island dwarf (adults were probably not as dangerous for their juveniles), having roamed islands about as large as three times nowadays Bavaria, this taxon seemingly retained precociality (and potentially r-strategy57, 60) from its large-bodied ancestors. As also suggested by the taphonomic circumstances14, 16, 17, (see also Supplementary Information) Europasaurus individuals likely stayed in a certain social cohesion, and potentially practiced colonial nesting as is known from other sauropods2, 60, 61. In concert with the approximate auditory capabilities offered here, our findings add hints towards the nature of aggregation with a certain complexity of reproductive and social behaviors for these little real- life titans, thriving in Europe some 154 Ma ago.
Materials and Methods
The articulated braincase specimen of Europasaurus holgeri, DFMMh/FV 581.1, together with both loose parietals (FV 581.2 & 3), represents a braincase that is traversed by breakages but not strongly deformed, lacking parts of the anterior and dorsomedial skull roof, as well as the anteromedial walls of the endocranial cavity. The articulated and assembled braincase lacks the frontals, the right orbitosphenoid and laterosphenoid. The parietals are anteriorly, posterodorsomedially and posteriorly incomplete and somewhat deformed (if they fit posteromedially with the supraoccipital they do not fit with the supraoccipital, prootic and laterosphenoid further anteriorly, and vice versa). The braincase of e.g., the macronarian Giraffatitan brancai suggests a plain posterior skull roof not exceeding the dorsal extent of the sagittal nuchal crest; this served as an orientation here.
Macro-photography
All specimens, except DFMMh/FV 581.1, 2 & 3, were documented using a Canon EOS 70D reflex camera equipped with a Canon EFS 10-135 mm objective, extension tubes (13 mm or 21 mm), and a Canon Macro Twin Lite MT-26EX-RT. Light was cross-polarized in order to reduce reflections of the specimen surface. Images were recorded in different focal planes (z-stacks) and subsequently fused with CombineZP (Alan Hadley). All obtained images were optimized for color balance, saturation and sharpness using Adobe Photoshop CS2.
Micro-computed tomography (microCT)
MicroCT of DFMMh/FV 581.1, 2 & 3 (Figs. 1–3; Supplementary Figs. 1–4) was performed using a Metrotom 1500 (Carl Zeiss Microscopy GmbH, Jena, Germany) in a subsidiary of Zeiss in Essingen. 1804 images were recorded with binning 1 resulting in a DICOM data set (for further details of settings and voxel size see Supplementary Table 1).
All other specimens (Figs. 4, 5, 7, 8; Supplementary Figs. 5–11) were documented with a Xradia MicroXCT-200 (Carl Zeiss Microscopy GmbH, Jena, Germany) of the Imaging center of the Department of Biology, University of Greifswald. 1600 projection images were recorded each, using 0.39x objective lens, with binning 2 (for further details of settings and voxel size for each specimen see Supplementary Table 1). The tomographic images were reconstructed with XMReconstructor software (Carl Zeiss Microscopy GmbH, Jena, Germany), binning 1 (full resolution) resulting in image stacks (TIFF format).
Digital segmentation and measurements were produced utilizing the software Amira (5.6), based on DICOM files (DFMMh/FV 581.1, 2 & 3) and tiff files (remaining material). The microCT data were manually segmented to create 3D surface models. In DFMMh/FV 581.1, 2 & 3, the x- ray absorption of the fossil and the sediment within is quite similar, resulting in low contrast in many places. Furthermore, for preservational reasons (lack of both frontals, right orbitosphenoid, laterosphenoid and loose parietals), the extent of the digital model of the endocast was conservatively estimated on the skull roof and on the anterodorsal region; some asymmetries on the endocast are explained by this circumstance.
Data availability
The microCT data and neuroanatomical models of all fossil specimens depicted herein are published online, in the repository MorphoSource (Europasaurus holgeri - neuroanatomy - DFMMh/FV - Schade et al. 2023 // MorphoSource)
Author contributions
M.S. designed the project, interpreted the data, wrote the manuscript and segmented the CT data of all specimens depicted, whereas C.P. segmented all specimens except for DFMMh/FV 581.1, 2 & 3. N.K. originally unearthed and prepared the fossils. M.S., S.S., C.P. and M.H. prepared the figures. N.K., C.P., M.H. and S.S. contributed to the manuscript.
Competing interests
The authors declare no competing interests.
Supplementary Information and Figures
Neurovascularanatomy and potential implications
The fenestra pseudorotunda probably functioned as a pressure relief for the inner ear, and it is considered as the lateral opening of the recessus scalae tympani1,2,3. Because a fenestra pseudorotunda seems to be distributed haphazardly among dinosaurs, it was assumed that the three main dinosaur groups (ornithischians, sauropods and theropods) acquired this feature independently4. According to the authors, many ornithischians possess a fenestra pseudorotunda (although lost in pachycephalosaurs, ankylosaurs and stegosaurs). Basal sauropodomorphs may originally possessed a fenestra pseudorotunda, whereas derived sauropods lost it (see also5). It was suggested that within theropods, a fenestra pseudorotunda did not develop before the origin of coelurosaurs (as well as an additional independent acquisition in abelisauroids4). A fenestra pseudorotunda has been identified on the endosseous labyrinth of Giraffatitan and the titanosaur MGPIFD-GR 1186, 7. In the theropod dinosaur Irritator8 and in Europasaurus, the fenestra pseudorotunda is developed as a mainly anteroposteriorly oriented opening situated medially to the crista interfenestralis (Figs. 4, 6D; Supplementary Fig. 4). In both taxa, the medial wall of the fenestra pseudorotunda is incomplete (possibly from damage, but more likely due to a lack of ossification), producing a hiatus acusticus (Supplementary Fig. 4). This circumstance renders the opening, visible in lateral view of DFMMh/FV 581.1, DFMMh/FV 1077 and DFMMh/FV 466+205 (Figs. 3B, 5L; Supplementary Figs. 5A, 7F), posteriorly to the fenestra ovalis, the vagal foramen for CN IX-XI and the jugular vein. A posterior vagal foramen as in Irritator is missing8. The unclear pattern of the presence or absence of a fenestra pseudorotunda in dinosaurs may be due to a lack of sufficient fossil preparation or CT data. Alternatively, this aspect has been out of scope in some previous works (these reasons may also hold true for the number of CN XII openings in other taxa). Sobral & Müller4 and Sobral et al.9 suggest that in taxa without a fenestra pseudorotunda the pressure- relief function has been carried out by the metotic foramen. However, in dinosaurs like the thyreophoran Struthiosaurus austriacus, the inner ear seems relatively clear and widely separated from the metotic foramen, which renders a pressure-relief function at least in this taxon rather unlikely (or alternatively, because of other hints towards inferior auditory capacities in this taxon, redundant10).
The flocculus is part of the cerebellum and involved in the integration and translation of eye, head and neck movements (VOR, vestibulo-ocular reflex; VCR, vestibulo-collic reflex; see e.g.11). In many previous studies, the floccular recess has been treated as a proxy for the actual cerebellar structure, which induced ecological inferences in fossil taxa (e.g.3, 12, 13). However, the floccular recess seems not to be a reliable proxy for the size of the actual neural tissue, also containing e.g., vascular tissue11, making its potential use problematic14. Whereas most sauropod taxa seem not to spot even the slightest floccular recess on the endocast (see e.g.7, 15 and references therein), there are some exceptions16,17,18,19 including Giraffatitan20. In case the size of the floccular recess at least partly reflects the actual flocculus in fossil taxa, it potentially holds evidence for superior VOR and VCR in Europasaurus and other sauropods that possess this structure (Fig. 1A). Possibly, because of its – for a sauropod – small body size, Europasaurus used its neck in a more flexible manner than its large-bodied relatives (see also5, 21). Considered in an evolutionary frame, the flocculus seems to leave a perceivable trace on a given endocast rather variably. Seemingly, the more agile early sauropodomorphs still bore relatively large flocculi, which decreased later in size in larger taxa5, 21. The presence of a small floccular recess in the secondarily ‘small-bodied’ Europasaurus may show a certain evolutionary flexibility in size and, hence, impression on the braincase of the flocculus.
Just as potential implications of the floccular recess for VCR/VOR and agility, the morphology of the semicircular canals in respect to agility or lifestyle (e.g.22,23,24,25,26), and the orientation of the lateral semicircular canal in relation to the habitual head posture27,28,29, are far from straightforward. If considered as one hint towards a certain orientation of the skull in fossil taxa, the lateral semicircular canal may help to evaluate this issue in concert with aspects such as other osteological correlates and/or ecology (e.g.10, 29, 30). If the assumed manner of articulation between the neurocranium DFMMh/FV 581.1 and the rest of the skull is correct31 (Fig. 1A,B), the posteroventrally inclining articular facet of the occipital condyle and the horizontal orientation of the lateral semicircular canal of Europasaurus suggest an inclined snout of c. 25°, which is similar to some other large-bodied sauropod taxa (e.g.27, 32,33,34).
Geology
Among the most important Mesozoic vertebrate fossil localities in Europe are the marine limestone deposits of the Langenberg quarry near Goslar (Lower Saxony, northern Germany). The quarry on the northern Harz rim belongs to the “Classic Square Mile of Geology”. In this outcrop, evidence of 350 million years of earth history is visible.
The biostratigraphically well dated Jurassic sediments at the Langenberg quarry range from the late Oxfordian to the late Kimmeridgian (see35). The predominant lithologies are carbonate beds which are tilted (70 to 80 degrees) to a near-vertical, slightly overturned position during the Harz Mountains orogeny towards the end of the Cretaceous. Sediment composition and invertebrate faunal contents record changes in water depth and salinity, but there is no evidence of subaerial exposure. The limestone deposits are assigned to the Süntel Formation36, previously known as the Kimmeridge Formation (German: “Mittlerer Kimmeridge”).
Palaeogeographically, the Langenberg quarry is located in the Lower Saxony Basin which covered most of northern Germany during the Upper Jurassic and Lower Cretaceous and was surrounded by several large paleo-islands. The fossils of Europasaurus holgeri are assigned to the lower section of the Upper Kimmeridgian and are 154 million years old.
At least the rock layers 56, 73, and 8337 have yielded terrestrial vertebrates that were washed into shallow tidal flats or the sea from a nearby island, most of the other layers contain a partially or purely marine fauna. The finds offer unique insights in the Late Jurassic terrestrial island fauna of northern Germany.
Since 1999, the terrestrial fauna and flora of these paleo-islands have been intensively investigated (see38). The quarry is the type locality for the dwarfed basal macronarian sauropod dinosaur Europasaurus but also yielded remains of other dinosaurs, such as diplodocid sauropods and stegosaurs. Also, a variety of theropod groups was present including basal Tyrannosauroidea, Allosauroidea, Megalosauroidea cf. Marshosaurus, Megalosauridae cf. Torvosaurus, and probably Ceratosauria (see39,40,41). Non-dinosaurian terrestrial vertebrates include several 3D-preserved remains of pterosaurs, a paramacellodid lizard, and a new genus of atoposaurid crocodilians42. Microvertebrate remains recovered by screen-washing are dominated by teeth of fish and crocodyliforms but also included an astonishing range of mammal teeth43,44,45,46.
Taphonomy
The fossils of Europasaurus are found only in the bone-rich limestone layer 83, with remarkably few accompanying remains of other animals. With more than 20 individuals discovered so far, it is unlikely that the animals were swimming or that all carcasses were washed from the land into the sea47, 48. Instead, it appears likely that the animals lived together in a herd and were located in a tidal plain when they died. This is also supported by the different ontogenetic stages of the discovered Europasaurus individuals: from juveniles, subadults to adults. After their sudden death, the Europasaurus carcasses were exposed in the shallow water of an intertidal zone for several days. Before their final burial in lime mud, their bodies began to decay. During this decay, the skeletons not only disintegrated but were also chewed upon by small scavengers. Small visible bitemarks on the bone surfaces indicate scavenging by invertebrates, smaller fish, and/or small atoposaurid crocodiles. The absence of theropod bite marks could be an indicator that the sauropod carcasses were deposited in a tidal area inaccessible to large predators.
The excellent preservation of the Europsaurus fossils, some still as partly articulated skeletons, as well the presence of at last three articulated sauropod tooth rows indicate very little water movement and little post-mortem transport of the bones before their final embedding in soft mud. Some of the carcasses must have repeatedly lain on top of the tidal banks above the water surface. Exposed to the sun and salty air, the carcasses partially dried out and the spatulate teeth were pulled of the jaw bones by desiccation. The parched and skeletonized cadavers then slowly were covered with sediments.
Acknowledgements
We are extremely thankful towards Zeiss in Essingen (especially Bastian Zwick and Stephan Tomaschko), the Universitätsmedizin in Greifswald (especially Christopher Nell) for actuating their CT devices for the fossils of Europasaurus; further micro-computed tomographies were performed at the Imaging Center of the Department of Biology, University of Greifswald (DFG INST 292/119-1 FUGG; DFG INST 292/120-1 FUGG). We thank Michael ‘Ede’ Kenzler, Jakob Krieger, Georg Brenneis, Jennifer Legat, Steffen Harzsch and Ingelore Hinz-Schallreuter (all University of Greifswald, Germany), together with Benjamin Englich (Dinosaurierpark Münchehagen, Germany) and Serjoscha Evers (University of Fribourg) for their support and discussions. M.S. is supported by the Bogislaw scholarship, University of Greifswald.