The concept of short necked azhdarchids is yet to be explored in detail, despite the significance it has for our understanding of azhdarchid palaeoecology and disparity. The functional anatomy of the long, stiffened azhdarchid neck has been the most controversial element in discussions of azhdarchid lifestyles (e.g., Witton & Naish, 2015 ; Averianov, 2013 , and references therein), so understanding its variation and biomechanics is paramount to advancing palaeobiological appreciation of the group. Here, we investigate the radical morphological differences between EME 315 and other azhdarchid cervicals from two angles. Firstly, we attempt to estimate the probable neck length of EME 315 and other azhdarchids (both giant and smaller species) to assess possible variation in their proportions and form. Secondly, we assess the bending strength of two giant azhdarchid vertebrae (EME 315 and UJA VF1) to appreciate variation in structural properties and functionality, and relate these to contemporary ideas of azhdarchid behaviour and ecology. It is imperative to these studies that we also investigate the likely identity and vertebral position of EME 315, and this is also discussed below.

However, recent discoveries of two proportionally short, isolated azhdarchid cervical vertebrae from the Maastrichtian Sebeş Formation (Transylvanian Basin) of western Romania have prompted suggestions that some azhdarchids may have been proportionally short necked ( Vremir, 2010 ; Vremir et al., 2015 ). The first of these specimens, LPV (FGGUB) R.2395, was interpreted as a cervical IV from a small azhdarchid with an estimated 3 m wingspan ( Vremir et al., 2015 ). The second represents a gigantic azhdarchid: Transylvanian Museum Society (Cluj-Napoca, Romania) specimen EME 315 ( Fig. 1 ). This latter bone is proportionally short and wide, of robust construction and bears—for a pterosaur—remarkably thick bone walls. Details of bone structure and provenance led Vremir (2010) to suggest it may represent a cervical III from Hatzegopteryx , a giant azhdarchid described from the middle member of the Densuş-Ciula Formation, Maastrichtian of Vãlioara, northern Haţeg basin, deposits contemporary and adjacent to the Sebeş Formation. We discuss the taxonomic identity of the specimen further below. Vremir (2010) concluded that the size and shape of EME 315 is so distinct relative to that of other azhdarchids that it must reflect a departure from expected azhdarchid anatomy and lifestyle.

Azhdarchid cervicals are essentially hollow tubes with near-circular or elliptical cross sections ( Fig. 4 ), and are thus conducive to beam loading calculations to ascertain their strength. We modelled bending load capacity for both UJA VF1 (the holotype vertebra of Arambourgiania ) and EME 315 based on their minimal central diameters, and using both their preserved and estimated total lengths ( Table 2 ). Cortical thicknesses were measured from broken mid-shaft sections of each bone. To enhance comparability between these vertebrae, we also modelled a hypothetical Hatzegopteryx cervical V based on length projections from our azhdarchid neck dataset and the centrum dimensions of EME 315: we estimate this bone’s length as 413 mm. This also provides a minimum estimate of neck strength because, as noted above, cervical V is the longest bone in the azhdarchid neck and thus the most susceptible to distortion under loading. Vertebral sections were modelled as consistent along the vertebral length and internal supporting structures were not factored into our equations. Because the vertebrae in question are elliptical in cross-section, we modelled both dorsoventral and lateral bending resistance. To calculate second moment of area ( I , required to calculate section modulus for stress calculations) for each vertebral axis, we used: (1) I = π ∕ 4 R 1 R 2 3 − R 3 R 4 3 where R 1 and R 2 represents the total bone radii in perpendicular x and y axes (respective to loading regime), and R 3 and R 4 represent radii of the internal bone cavity. Bone stress was modelled using cantilever-style loading, where one end of the bone is fixed and the total length of the bone equals the moment arm. Stress values reflect those experienced at the supported end of the bone. Vertebrate bones are rarely loaded as true cantilevers in life but such a reductionist approach provides a quantified means of comparing bone structure and robustness ( Witton & Habib, 2010 ). We calculated stresses ( σ , Mpa) experienced at the supported end of the vertebrae during cantilevered loading: (2) σ = W L ∕ Z where L is bone length (mm), W (N) is the weight loaded onto the bone and Z is section modulus (second moment of area/distance to neutral surface of the vertebra). Calculating bone strength requires some assumptions about the Young’s modulus of pterosaur bone. We follow Palmer & Dyke (2010) in using 22 GPa—a value agreeing with several avian long bones—which seems a reasonable proxy for pterosaur bones. Following Currey (2004) and Palmer & Dyke (2010) , we used the relationship between Young’s modulus and yield stress in tension of 162 MPa. We modelled a range of values reflecting different upper limits for giant pterosaur body mass (180–250 kg) for W to demonstrate the sensitivity of our results and calculate Relative Failure Force (RFF; Witton & Habib, 2010 ) for each model. RFF is bone failure force, in bending, divided by total body weights. Although pterosaur axial elements were unlikely to ever bear a full loading of body mass in life, it provides a useful proxy by which we might compare the results here with those of other studies (e.g., Witton & Habib, 2010 ) and to compare strengths of pterosaur vertebra against their respective body masses.

Nevertheless, it is possible to provide a qualified assessment of the general size represented by this vertebra. EME 315 is the most robust pterosaur cervical yet reported and likely conforms to approximate size predictions for the Hatzegopteryx holotype, estimated to have a 10–12 m wingspan from the FGGUB R1083 humerus ( Buffetaut, Grigorescu & Csiki, 2003 ; Witton & Habib, 2010 ). The size of pterodactyloid cervical condyles and cotyles appears to be relatively uniform along the cervical series (e.g., Anhanguera ( Wellnhofer, 1991a ); Quetzalcoatlus sp. ( Witton & Naish, 2008 ); Azhdarcho (2010)), allowing us to assume that the 150 mm wide cotyle of EME 315 is similar to the condylar and cotylar dimensions present along the preceding part of the neck. In the reconstructed neck of Azhdarcho , and in completely known necks of Anhanguera , atlas cotyle width (assumed to correspond to the dimensions of the occipital condyle) is 30–40% of condyle and cotyle width in the remainder of the neck: the 55 mm wide occipital condyle of the H. thambema skull therefore corresponds to the 150 mm wide cotyle of EME 315. The unprecedented width and robust construction of EME 315 also corresponds with the unusually broad skull of H. thambema , estimated to span 500 mm across the quadrates ( Buffetaut, Grigorescu & Csiki, 2003 ). We take these rough comparisons to indicate that EME 315 probably represents an animal at the upper known limit of pterosaur size.

We refrain from providing a specific wingspan estimate for the EME 315 individual because the relationships between wingspans and cervical vertebrae are not reliably predicted using existing data. Disagreements over the wingspan of the individual represented by the Arambourgiania holotype cervical (stated as having a wingspan of 7–8 m wingspan by Suberbiola et al. (2003) and yet argued as 10 m or more by others— Frey & Martill, 1996 ; Steel et al., 1997 ; Martill et al., 1998 ) demonstrate the uncertainty surrounding size estimates of the largest pterosaurs known only from vertebral remains. Vremir (2010) indicated that the great width of EME 315 suggested a similarly expanded postcervical column and perhaps a much larger overall size than that of other giant azhdarchids. This interpretation is questionable as the cervical and anteriormost dorsal vertebrae of giant pterodactyloids are wider and more massive than the rest of the axial column ( Bennett, 2001 ; Kellner et al., 2013 ). A lack of study on proportional scaling of the pterosaur axial column further precludes reliable predictions of the dimensions of the dorsal column belonging to the animal represented by EME 315.

EME 315 thus possesses a combination of anatomical traits that are a good match for the posterior cervical vertebrae of at least two other azhdarchid taxa, and it differs markedly from the middle or anterior neck vertebrae of any taxon. We note particular similarity with cervical VII of Azhdarcho and hence provisionally consider a seventh cervical position most likely for EME 315, the caveat being that additional discoveries of azhdarchid posterior cervical vertebrae are needed to bolster our identification.

Strong similarity occurs between EME 315 and cervicals VII and VIII of Azhdarcho lancicollis (ZIN PH 138/44 and 137/44, respectively ( Averianov, 2010 ; Averianov, 2013 ), Figs. 2I – 2K ), with the most notable similarity pertaining to cervical VII. The cotyle heights of these vertebrae are characteristically shallower than their neural arches, and four times wider than high ( Averianov, 2010 ). The cotyle width:height ratio of EME 315 approximates this at ca. 3.7. Both EME 315 and Azhdarcho cervical VII possess hypapophyses, a contrast to cervical VIII of Azhdarcho where a hypapophysis is absent ( Averianov, 2010 ). Reconstructed length:width ratios of EME 315 and the posterior cervicals of Azhdarcho are similar (1.36 in Azhdarcho cervical VII, 1.06 in cervical VIII, versus 1.25 in EME 315; based on a reconstructed EME 315 length and width of 300 mm and 240 mm, respectively), as are the presences of pneumatic foramina dorsal to the neural canal. The relatively splayed prezygapophyses of cervicals VII and VIII in Azhdarcho also correspond well with EME 315, although they are much smaller in Azhdarcho cervical VIII. The articular faces in the latter are joined to the vertebral body via a constricted bony shaft, whereas the zygapophyses of EME 315 and Azhdarcho cervical VII are more massive overall. Cervical VII in Azhdarcho and EME 315 are also similar in having a tapered ‘waist’ mid-way along the length of the centrum. This feature is absent in cervical VIII of Azhdarcho which has, in contrast, subparallel lateral margins. The pneumatic foramina are larger than the neural canal in Azhdarcho ’s cervical VII, which contrasts with the condition in EME 315 and cervical VIII of Azhdarcho . EME 315 also lacks pneumatic foramina on the lateral surface of the centrum, in contrast to Azhdarcho ’s cervical VIII where they are present. The neural spines on the posterior cervicals of Azhdarcho are unknown, but those of the posteriormost cervicals of Phosphatodraco mauritanicus are proportionally tall and anteroposteriorly restricted ( Fig. 2J ; Suberbiola et al., 2003 ). This condition matches the one that appears to have been present in EME 315.

Azhdarchid cervicals IV and V can be up to eight times longer than wide ( Lawson, 1975 ; Howse, 1986 ; Frey & Martill, 1996 ). Their neural spines comprise low anterior and posterior ridges with a mid-length so reduced that they are confluent with the vertebral corpus, sometimes being represented by a faint, narrow ridge at best ( Figs. 2D – 2F ). EME 315 is not elongate relative to its width ( Fig. 1E ) and, though possessing a bifid neural spine, the breadth of the preserved neural spine bases suggests they were robust, tall structures. Azhdarchid cervical VIs seem similar to fourth and fifth elements, but have a proportionally tall posterior neural spine ( Figs. 2G – 2H ). EME 315 contrasts with most or all of these conditions, and thus likely pertains to a posterior section of the neck—that is, to cervicals VII or VIII.

Vremir (2010) considered EME 315 as a cervical III, but we consider this unlikely. The neural spines of cervical III in Azhdarcho lancicollis (Zoological Institute of the Russian Academy of Sciences, St. Petersburg, Russia, ZIN PH 131/44) and Quetzalcoatlus sp. (Texas Memorial Museum, Austin, USA, TMM 41544.16) extend for the length of the entire centrum and lack any obvious reduction in height at mid-length ( Fig. 2A ; Howse, 1986 ; Averianov, 2010 ), a significant contrast to the bifid neural spine of EME 315. Indeed, Howse (1986) reported that the Quetzalcoatlus cervical III neural spine is at its highest point mid-way along its length, a marked contrast to the condition in EME 315. The proportions of cervical III cotyles, which are approximately twice as wide as tall and subequal in height to the neural arch, also contrast with EME 315, as does the continuous tapering of cervical III zygapophyses when viewed in dorsal aspect. Cervical IIIs also seem generally longer-bodied than the proportionally short EME 315. We find greater similarity with other azhdarchid cervicals (below) and thus disagree with a cervical III identity for EME 315.

Isolated azhdarchid cervicals have typically been regarded as offering little insight to their position within the cervical series, except perhaps for cervical V, which appears distinctly elongate ( Frey & Martill, 1996 ; Martill et al., 1998 ). Recent work on relatively complete azhdarchid cervical skeletons indicates that their vertebrae may show consistent characteristics specific to the position in the cervical series ( Suberbiola et al., 2003 ( sensu Kellner, 2010 ); ( Averianov, 2010 ; Averianov, 2013 ) ( Fig. 2 ). Work in this area must be regarded as provisional given that complete azhdarchid necks, or even sufficient material to completely reconstruct entire cervical series, remain few in number. However, we consider known azhdarchid necks of consistent enough form that the likely vertebral position of well-preserved azhdarchid cervicals, such as EME 315, can be determined with some degree of confidence.

Results and Discussion