• cranial kinesis;
  • pterosaur;
  • joint morphology;
  • streptostyly


  1. Top of page
  2. Abstract
  8. Acknowledgements
  10. Supporting Information

Based on comparative anatomical, morphological, and phylogenetic considerations the potential of pterosaurs for cranial kinesis is assessed. Our investigation shows that whereas skeletally mature derived pterodactyloids have completely fused, rigid and doubtlessly akinetic skulls, skeletally immature derived pterodactyloids and more basal pterosaurs possess key features in the morphology of their otic and basal joints that are suggestive of cranial kinesis, namely streptostyly. In addition, pterosaurs exhibit an evolutionarily informative trend in the degree of cranial ossification, where it is low in most nonpterodactyloids (here named bifenestratans), intermediate in Rhamphorhynchus and Archaeopterodactyloidea, and high in derived pterodactyloids. Incomplete fusion could also indicate loose connections between skull elements. However, another crucial anatomical requirement of a kinetic skull, the permissive kinematic linkage is absent in all pterosaurian taxa. The fact, that the presence of permissive kinematic linkages in the skull is also a prerequisite of all types of cranial kinesis, provides hard evidence that all members of Pterosauria had akinetic skulls. Thus, the presence of the morphological attributes indicative of intracranial movements in some pterosaurs must be explained on grounds other than real potential for cranial kinesis. It could either be of mechanical or ontogenetic importance, or both. Alternatively, it might be considered as the morphological remnant of a real, kinetic skull possessed by the diapsid ancestors of pterosaurs. Anat Rec, , 2011. © 2011 Wiley-Liss, Inc.


  1. Top of page
  2. Abstract
  8. Acknowledgements
  10. Supporting Information

Kinesis and Pterosaurs

The occurrence of cranial kinesis among a variety of tetrapods have long been recognized (see Frazzetta,1962 for references), but the conceptual definition was first provided by Versluys (1910,1912) who defined a kinetic skull as allowing any intracranial movements between the elements excluded that of the lower jaw. Cranial kinesis as a phenomenon, being present in the earliest tetrapods (movable palatoquadrates and palatal and facial elements; Iordansky,1989) and in some extant teleosts and amphibians (Rieppel,1978; Summers and Wake,2005), is generally considered a plesiomorphic character (Iordansky,1990) and is thought to be most prominent within archosaurs and lepidosaurs (Herrel et al.,1999). However, clear evidence of true cranial kinesis, which should be distinguished from slight movements occurring at many patent sutures and allowing dissipation of mechanical stresses, exists unambiguously only in some squamates and birds among amniotes (Holliday and Witmer,2008).

Nevertheless, some forms of cranial kinesis have been and probably will be suggested for numerous extinct vertebrates, particularly dinosaurs. In contrast to dinosaurs, the notion of intracranial movements in another archosauromorph group, the pterosaurs is not so common. Except for the work of two authors, Arthaber (1919) and Wild (1978,1984), who regarded the Early Jurassic Dorygnathus banthensis and the Upper Triassic Eudimorphodon ranzii, respectively, as having streptostylic quadrate, and Bennett (1996a) who used the term “metakinetic skull” as a streptostylic character suggestive of archosauromorph nature of pterosaurs in his phylogenetic analysis, thus accepting Wild's (1978,1984) concept for Eudimorphodon, this issue has largely been ignored. Hence, streptostyly, which refers to the anteroposterior rotation of the quadrate about the otic joint (for further information see Supporting Information), was the only form of kinesis ever suggested for pterosaurs. Most pterosaurologists have regarded the pterosaurian skull as universally akinetic (e.g., Wellnhofer,1978; Buffetaut et al.,2002; Fastnacht,2005).

In the light of the dominance of more derived pterosaurs with firmly fused skull bones in the fossil record, this attitude is easy to understand. On the other hand, based on the apparent, although sometimes debated close affinities of pterosaurs to dinosaurs (Hone and Benton,2008, and see Fig. 1 for the position of Pterosauria in a broader phylogenetic context), for which cranial kinesis has been proposed on several occasions (e.g., Colbert and Russell,1969; Galton,1974; Norman,1984; Norman and Weishampel,1985; Chiappe et al.,1998; Mazzetta et al.,1998, see Supporting Information), and on certain morphological attributes of some pterosaurian skulls it seems reasonable to pay more attention to the potential of intracranial movements in pterosaurs.

thumbnail image

Figure 1. Three levels (A, B, C) of diapsid phylogeny gradually focusing on the archosaurian clades (C). A, Interrelation of the major diapsid clades (after Lee,2001); B, division of archosauriformes (after Sereno,1991); C, two possible outcomes for the phylogenetic relationships among archosaurian clades focusing on the conspicuously different position of Pterosauria in the two cases (WST, Weighted Supertree; SM, Supermatrix Tree). Groups of special significance for the EPB evaluation of this study are boldfaced.

Download figure to PowerPoint

For the acquirement of the necessary theoretical background, Supporting Information is provided which contains detailed information on basic concepts such as the different forms, morphological correlates, functional significance, occurrence, origin, and evolution of cranial kinesis in other diapsid reptiles. In this Supporting Information, the extremely kinetic skull of Serpentes is not regarded.

Osteological Aspects of Kinesis in Extant and Extinct Taxa

To reveal features that are suggestive of cranial kinesis several methods have been in use mainly in extant taxa (Frazzetta,1962,1983; Smith and Hylander,1985; Patchell and Shine,1986; Condon,1987; Herring and Teng,2000; Metzger,2002; see Supporting Information). Among the most important features is the presence of morphological correlates which include the co-operating muscle, connective, and skeletal tissues assuring the proper functioning of the involved joint systems, and which can be assigned to certain types of kinesis (Bahl,1937; Bühler,1981; Rieppel and Gronowski,1981; Zusi,1984; Rieppel,1993; Arnold,1998; Metzger,2002; see Supporting Information). Nevertheless, it must be remembered that the absence of these morphological correlates can allow the exclusion of cranial kinesis, but the presence of them can only indicate the potential for movement and cannot definitively prove its presence invivo, thus they must be viewed with a measure of caution (Throckmorton,1976; Herrel and De Vree,1999; Metzger,2002; Holliday and Witmer,2008).

When it comes to extinct vertebrates, significant amount of information is lost due to the incompleteness or lack of preservation of soft tissues that must have had important role in intracranial movements. The only available data in most cases are the osteological features. Holliday and Witmer (2008) have defined four criteria or morphological correlates that are indispensible concerning inferences of powered cranial kinesis in fossil taxa.

The first two criteria regard the detectable presence of mobile joints in the otic (quadratosquamosal) and basal (basipterygopterygoid) regions of the skull (Holliday and Witmer,2008). They stated that the mobile joint type in these regions must be synovial. “Synovial joint,” the presence of which is often referred to as one of the most important criteria in kinetic bony connections, implies a noninterdigitate, finished, smooth joint with synovial capsule (Holliday and Witmer,2008). The osteological correlates of synovial joints are (1) the presence of convex and complementary concave joining surfaces of the participating elements; (2) the smooth articular surface indicative of hyaline cartilage covering; (3) rough, parallel striated zone and occasionally large pits distal to the smooth surface revealing the presence of the joint capsule and ligament attachments, respectively (Holliday and Witmer,2008). However, skull elements which are to form a mobile joint (mobility at least to the extent over which it can be referred to as kinetic joint), can also be connected in different ways, for instance via ligament (e.g., quadratopterygoid ligament), or in some special cases movement can occur even in a smooth/slightly interdigitating fibrous joint (e.g., frontal-parietal joint in mesokinesis of geckoes, see Supporting Information). Furthermore, flexibility can be ensured via inbuilt flexion zones formed by thin bony lamellae (e.g., craniofacial hinge in prokinesis of birds, see Supporting Information). If one of these features is present, similarly to synovial joints, it can assure mobility in the critical otic and basal regions of the skull.

The third criterion which has been cited by Holliday and Witmer (2008) as another morphological correlate of cranial kinesis is the state of development of the protractor muscles in the skull. They considered the presence of well-developed preotic and levator pendants as osteological indicators of protractor muscles (e.g., m. protractor pterygoideus) which could have operated powered intracranial movements (Holliday and Witmer,2008). The presence, reconstructed size, and attachment areas of most muscles in fossil groups are, however, obscure at best, and the functional significance of the protractor muscle group in extant taxa is sometimes also inconclusive (Gussekloo and Bout,2005).

The fourth criterion is referred to as permissive kinematic linkage which includes those taxon-specific features that permit observable intracranial movements in extant taxa possessing true kinetic skull. These are in general related to elimination or mobility-modification of bony elements surrounding the movement centers that would otherwise hinder the intracranial movements.

Furthermore, Holliday and Witmer (2008) defined three categories of inferred kinetic state, of which, obviously, only the first two criteria can be applied to extinct forms:

  • 1
    partially kinetically competent: the skull possesses key synovial joints and protractor muscles but lacks bony gaps permitting movement
  • 2
    fully kinetically competent: the skull possesses key synovial joints and protractor muscles as well as permissive bony linkages but lacks demonstrable movement in vivo
  • 3
    kinetic: the skull possesses key synovial joints, protractor muscles and permissive bony linkages as well as demonstrable movement in vivo.

Thus, extinct taxa, such as dinosaurs or pterosaurs may at most be fully kinetically competent. In extant diapsids, true cranial kinesis only occurs along with the reduction of certain cranial elements (lower temporal bar in lepidosaurs but also the postorbital bar in gekkotans and varanids; the supratemporal, postorbital, and lacrimal bar in birds, see Supporting Information), so it seems parsimonious to infer that some form of reduction of bones might also be necessary to acquire a kinetic diapsid skull.

Skulls of Pterosaurs in General

To discuss the issue of cranial kinesis in pterosaurs, a brief general description of pterosaurian skulls is necessary. The skull of pterosaurs is generally lightly built (fenestrated) and elongated, and they always have complete lower temporal arch formed by mainly the jugal and partially the quadratojugal.

Until recently there had been basically two morphological types of pterosaurs distinguished, the more basal nonpterodactyloid (generally referred to as “rhamphorhynchoid”) and the more derived pterodactyloid constructions, which have significant differences in their body architecture (Fig. 2). In contrast to “nonpterodactyloids” the term “pterodactyloids” implies not only a morphology-based category but forms a valid monophyletic group, as well. Two new pterosaur genera discovered in China, Darwinopterus and Wukongopterus (Lü et al.,2009 and Wang et al.2009, respectively), however, have challenged the concept of this morphology-based distinction by having a mixture of nonpterodactyloid and pterodactyloid characters in their skeleton. Accordingly, a modified concept is needed to define different pterosaurian morphotypes. Since the main object of this study is the skull, a new terminology was suggested on one hand by M. Witton (pers. com.) on the other hand by the authors of this study for distinguishing pterosaurian skull-constructions without regarding the phylogenetic position of the taxa concerned. This new, morphology-based concept is defined by virtue of the relation between the naris and antorbital fenestra: if they are separated, the skull is referred to as bifenestratan; if they are confluent, the applied term for the skull is monofenestratan (suggested by M. Witton). The bifenestratan and monofenestratan skull-morphotypes correspond to the former nonpterodactyloid and pterodactyloid + Darwinopterus (and possibly Wukongopterus, as well; M. Witton, pers. com.) constructions, respectively. However, since Darwinopterus and Wukongopterus for practical reasons (bad preservation and limited access) are not included in the current investigation, the taxonomical composition of the two new morphotype-groups is equivalent in this study with the former nonpterodactyloid–pterodactyloid concept. Nevertheless, the terms “bifenestratan” and “monofenestratan” are used here only in a morphotype-sense and do not imply real phylogenetic categories.

thumbnail image

Figure 2. Line drawing of the two skull-morphotypes based on the genera A, Rhamphorhynchus and B, Anhanguera representing the bifenestratan and monofenestratan morphotype, respectively. Note the length of the rostrum, the state of the naris (1) and antorbital fenestra (2), and the state of two palatal fenestrae (8, 9) as main differences between the two basic “bauplans.” Abbreviations: bpt, basipterygoid; ec, ectopterygoid; f, frontal; j, jugal; l, lacrimal; mx, maxilla; n, nasal; p, parietal; pl, palatine; pmx, premaxilla; po, postorbital; pt, pterygoid; q, quadrate; qj, quadratojugal; sq, squamosal; 1, naris; 2, antorbital fenestra; 3, orbit; 4, supratemporal fenestra; 5, lateral temporal fenestra; 6, choana; 7, suborbital fenestra; 8, pterygo-ectopterygoid fenestra; 9, subtemporal fenestra; 10, interpterygoid vacuity; 11, cranioquadrate opening.

Download figure to PowerPoint

The main differences between the two skull morphotypes can be summarized as follows: whereas bifenestratans (Fig. 2A) have a naris (1) and an antorbital fenestra (2) separated by a bony bar consisting of the conjunction of the maxillary process of the nasal and the nasal process of the maxilla, monofenestratans (Fig. 2B) usually have more elongate rostrum with a confluent and very large nasoantorbital fenestra (1+2). In addition, the confluence of certain palatal fenestrae (8+9, Fig. 2B) is also a characteristic of monofenestratans (Ősi et al.,2010). The basic “bauplan” of the skull of the two morphotypes is illustrated in Fig. 2. Some monofenestratans are edentulous, while all hitherto known bifenestratan pterosaurs have teeth and sometimes elaborate dentition.

Phylogenetic interrelationships of pterosaur genera (based on Dalla Vecchia,2009, and Andres and Ji,2008) without regarding the new problematic taxa, Darwinopterus and Wukongopterus are shown in Fig. 3.

thumbnail image

Figure 3. Pterosaur phylogeny based on the recent cladistical analyses. A, Interrelationships of bifenestratan pterosaur species with indication of their relation to the more derived Pterodactyloidea (modified from Dalla Vecchia,2009); B, interrelationships of the monophyletic Pterodactyloidea on family and generic level (modified from Andres and Ji,2008).

Download figure to PowerPoint

In this article, we investigate the morphological correlates of potential intracranial movements in pterosaurian skulls using the comparative strategy and evaluation applied by Holliday and Witmer (2008) for dinosaurs, and consider the results in the context of what we recently know about the phenomenon of cranial kinesis.

Institutional Abbreviations

AMNH, American Museum of Natural History, New York, USA; BMNH, British Museum of Natural History, London, England; BNM, Bündner Naturmuseum, Chur, Switzerland; BSPG, Bayerische Staatsammlung für Paläontologie und Geologie, München, Germany; BXGM, Benxi Geological Museum, Liaoning Province, China; CD, Desirée Collection of Rainer Alexander von Blittersdorff Rio de Janeiro, Brasil; CM, Carnegie Museum of Natural History, Pittsburgh, USA; DNPM MCT, Museu Ciencias da Terra, Setor de Paleontologia do Departamento Nacional de Producao Mineral, Rio de Janeiro, Brasil; GMV, Chinese Geological Museum, Beijing, China; GPIUB, Geologisch-Paläontologisches Institut, Universität Bonn; IGO, Instituto de Geología y Paleontología, La Habana, Cuba; IVPP, Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China; KUVP, Museum of Natural History, University of Kansas, Kansas, USA; MCSNB, Museo Civico di Scienze Naturali di Bergamo, Italy; MN, Museu Nacional, Rio de Janeiro, Brazil; MPUM, Dipartimento of Scienze della Terra dell'Università di Milano, Italy; MSFN, Museo Friulano di Storia Naturale, Udine, Italy; NSM, National Science Museum, Tokyo, Japan; PIN, Palaeontological Institute, Russian Academy of Sciences, Moscow, Russia; RGM, Naturalis (Nationaal Natuurhistorisch Museum), Leiden, The Netherlands; SMNF, Senckenberg Forschungsinstitut und Naturmuseum, Frankfurt, Germany; SMNK, Staatliches Museum für Naturkunde, Karlsruhe, Germany; SMNS, Staatliches Museum für Naturkunde, Stuttgart, Germany; TMM, Texas Memorial Museum, University of Texas, USA; WDC, Wyoming Dinosaur Center, Wyoming, USA; YPM, Peabody Museum of Natural History, Yale University, New haven, USA; ZMNH, Zhejiang Museum of Natural History, Zhejiang Province, China.


  1. Top of page
  2. Abstract
  8. Acknowledgements
  10. Supporting Information

In this study, pterosaurs are subjected for the first time to an investigation on their potential or incapacity for cranial kinesis. To infer the likelihood of cranial kinesis in pterosaurs in a phylogenetic context, we applied Extant Phylogenetic Bracket (EPB) method (Witmer,1995), since cranial kinesis involves unpreserved soft tissues to a high degree. Because of different interpretations of the phylogenetic position of pterosaurs, the two most widely accepted approaches have been used in the evaluation; (1) Pterosauria is the sister group to Dinosauria (Hone and Benton,2008, Fig. 1C, WST) being bracketed by birds and crocodiles (Fig. 1B); (2) Pterosauria is a basal Archosauromorpha (Bennett,1996a) being bracketed by lepidosauromorhs and archosauromorphs (Fig. 1C, SM).

The evaluation was based on the search for morphological correlates indicative of cranial kinesis and was carried out in 27 different pterosaur genera most of which had either almost complete skull material or crucial skull elements of good preservation. Of the 27 investigated genera, 13 can be assigned to bifenestratans and 14 to pterodactyloid monofenestratans. Among the 71 investigated specimens, 45 were available for personal examination (see Table 1). Twenty-six of the referred original specimens, which were not attainable for the authors, were assessed based on the related literature, casts, and published photos of high resolution (see Table 2). Where it was possible, all joints of the skull elements which might be relevant or might refer to any type of intracranial movements have been evaluated. Braincases, as expected to be fused in all adult specimens and putative circumorbital elements are not considered in the morphological investigation. Skeletally immature specimens have also been examined to identify possible changes in the biomechanical behavior of the skull during ontogeny.

Table 1. Examined specimens that were available for personal investigation with indication of their generally accepted or presumable ontogenetic stage by “i,” immature (juvenile or subadult); “m,” mature (adult) and “?,” uncertain
Taxa available for personal investigationInventor number of the specimenFeasible ontogenetic stage
Eudimorphodon ranziiMCSNB 2888m
Carniadactylus sp. (“Eudimorphodon ranzi” sensu Wild,1978)MPUM 6009m
Caviramus filisurensis (“Raeticodactylus filisurensis” sensu Stecher,2008)BNM 14524m
Dimorphodon macronyxBMNH 41212-13m
BMNH R 1035m
Dorygnathus banthensisBSPG 1938 I 49m
SMNS 18969m
SMNS 50164m
SMNS 50914m
SMNS 51827m
SMNS 55886m
Rhamphorhynchus muensteriBSPG AS VI 34m
BSPG 1867 II 2m
BSPG 1889 XI 1i
BSPG 1927 I 36m
BSPG 1929 I 69m
BSPG 1934 I 36i
BSPG 1938 I 503i
BSPG 1955 I 28m
BSPG 1989 XI 1m
SMNK PAL 6596?
SMNS 52338m
SMNS 56980m
Campylognathoides liasicusSMNS 18879m
SMNS 50735m
Campylognathoides zitteliSMNS 9787m
Scaphognathus crassirostrisSMNS 59395i
Austriadactylus cristatusSMNS 56342m
Pterodactylus antiquusBSPG AS I 739m
Pterodactylus kochi (P. antiquus sensu Bennett,1996b)BSPG AS V 29m
BSPG 1878 VI 1i
BSPG 1883 XVI 1m
BSPG 1937 I 18m
SMNF R 4072m
Pterodactylus micronyx (Gnathosaurus subulatus sensu Bennett,1996b)BSPG 1971 I 17i
Pterodactylus sp.BSPG 1936 I 50i
SMNF R 4074m
Germanodactylus cristatusBSPG 1892 IV 1m
Ctenochasma gracile (Ctenochasma elegans sensu Bennett,2007b)BSPG 1920 I 57m
Ctenochasma sp.SMNS 81803m
Anhanguera sp.SMNK uncataloguedm
Araripesaurus santanae (Santanadactylus araripensis sensu Bennett,1993)BSPG 1982. I. 90i
Tapejara wellnhoferiSMNK PAL 1137i
Table 2. Examined specimens that were evaluated on the basis of related literature, casts and published photos of high resolution
Taxa unattainable for personal investigationInvestigation based onInventor number of the specimenFeasible ontogenetic stage
  1. The generally accepted or presumable ontogenetic stage of the specimens is indicated by “i,” immature (juvenile or subadult); “m,” mature (adult) and “?,” uncertain.

Carniadactylus rosenfeldiDalla Vecchia,2009MSFN 1797m
Campylognathoides liasicusWellnhofer,1974CM 11424m
Scaphognathus crassirostriscast SMNS 80203GPIUB 1304m
Cacibupteryx caribensisGasparini et al.,2004IGO-V 208m
Batrachognathus volansRyabinin,1948; Dalla Vecchia,2002PIN 52-2m
Dendrorhynchoides curvidentatusDalla Vecchia,2002GMV2128m
Anurognathus ammoniBennett,2007a; high resolution photos by H.Tischlingeruncatalougedm
Rhamphorhynchus muensterihigh resolution photos by B. MuellerCM 11434m
Gegepterus changiWang et al.,2007IVPP V 11981i
Anhanguera bittersdorffiCampos and Kellner,1985MN 4805-Vm
Anhanguera piscatorKellner and Tomida,2000NSM-PV 19892i
Anhanguera sp.Kellner,1996MCT 1501-Ri
Coloborhynchus spielbergiVeldmeijer et al.,2006RGM 41880m
Istiodactylus latidensHooley,1913BMNH R 0176?
Istiodactylus sinensisAndres and Ji,2006NGMC 99-07-011m
Tapejara wellnhoferiWellnhofer and Kellner,1991AMNH 24440?
Kellner,1996MCT 1500-Ri
Sinopterus dongiWang and Zhou,2003IVPP V13363?
Huaxiapterus benxiensisLü et al.,2007BXGM V0011?
Pteranodon spBennett,2001KUVP 976m
 KUVP 2212m
 YPM 1177m
Zhejiangopterus linhaiensisCai and Wei,1994ZMNH M1330m
Quetzalcoatlus sp.Kellner and Langston,1996TMM 41961-1m
 TMM 41954-62m

The phylogenetic tree of Dalla Vecchia (2009) and that of Andres and Ji (2008) was used in the evaluation of results in a phylogenetic context. However, it must be taken into account that the tree of Dalla Vecchia (2009) differs from the results of most other phylogenetic analyses in the position of anurognathids, which group is considered a derived clade by Dalla Vecchia (2009) and a basal nonpterodactyloid group by Bennett (1996a), Kellner (2003), and Unwin (2003).


  1. Top of page
  2. Abstract
  8. Acknowledgements
  10. Supporting Information

EPB Evaluation

The EPB method (Witmer,1995) can indeed be very useful, since it provides the most parsimonious assumption to infer the likelihood of an unknown feature in an extant taxon. However, the reliability of EPB decreases significantly with increasing uncertainty of the phylogenetic relationships of the taxon in question. Furthermore, the higher taxonomic level the bracketing taxa represent, the higher the variability in the examined trait can be within the bracketing taxa themselves.

In pterosaurs, this problem is even worse due to their ambiguous phylogenetic position and the large distance between them and their presumed closest living relatives. The two main interpretations concerning their phylogenetic position can result in all three levels of inference depending on which group is considered within the extant components. Applying Bennett's (1996a) approach, the two ways of bracketing pterosaurs already give three different levels of inference. If the bracket is formed by lepidosauromorhs and archosauromorphs, both of which represent very high taxonomic levels, we can find kinetic, as well as akinetic representatives in both bracketing clades. Choosing Rhynchocephalia within Lepidosauromorpha for one extant component and Suchia within Archosauromorpha for the other gives Level III inference (decisive negative assessment) for cranial kinesis in pterosaurs, since all extant species of Rhynchocephalia (Sphenodon) and Suchia (Crocodilia) have akinetic skulls. However, using Squamata as one and Aves as the other component, in both clades of which intracranial movements are characteristic, cranial kinesis in pterosaurs is Level I inference (decisive positive assessment). Applying the same extant clades but in different combinations, e.g., Squamates—Suchia and Rhynchocephalia—Aves will both imply Level II inference (equivocal assessment) with one component exhibiting cranial kinesis and the other possessing akinetic skull. Using the phylogenetic interpretation of Hone and Benton (2008), EPB gives again a Level II inference of cranial kinesis in pterosaurs bracketing pterosaurs between akinetic crocodiles and kinetic birds. Thus use of the EPB in predicting the kinetic potential of pterosaur skulls is inconclusive.

Morphological Correlates

The morphological observations are subdivided into three main categories, namely joint morphology of skull elements, osteological correlates of protractor muscles, and ossification degree of the skull as a unit.

Joint morphology. 

In pterosaurian skulls, two characteristic types of joints can occur: fibrous joints (syndesmoses) and synovial joints (see Fig. 4A—D, and E,F, respectively). Thin portion of bony elements, which might be capable of flexion like the bending zones in birds, may also be present.

thumbnail image

Figure 4. Forms of joints occurring in the pterosaurian skull represented here by Dorygnathus banthensis SMNS 55886 (A, B), WDC-CTG-001 (C, D, F) and SMNS 51827 (E) specimens without considering complete fusion of elements. A, overlapping fibrous joint demonstrated by the postorbital-jugal connection in which the ascending process of jugal overlaps the descending process of postorbital; B, overlapping fibrous joint demonstrated by the lacrimal-jugal, jugal-maxilla, and nasal-maxilla connections in which the processes of jugal, maxilla, and nasal overlap the lacrimal, jugal, and maxilla, respectively; C, patent suture preceding interdigitating fusion state demonstrated by the dorsal aspect of contralateral frontals, parietals and the frontoparietal connections (dorsal view); D, interdigitating suture preceding fibrous fusion of elements demonstrated by the ventral aspect of the frontal-parietal connections; E and F, apparently synovial joints demonstrated by the distinct articular surfaces of the basipterygoid processes (E) and the cephalic and mandibular condyles of the quadrate (F). Black arrows point to the articulating areas. Abbreviations: bpt, basipterygoid; bs, basisphenoid; cc, cephalic condyle; f, frontal; fli, impression of the frontal lobes of the brain; ij, unfused fibrous joint with interdigitating suture; j, jugal; l, lacrimal; mc, mandibular condyles; mx, maxilla; n, nasal; oj, overlapping fibrous joint; p, parietal; pj, unfused fibrous joint with patent suture; pmx, premaxilla; po, postorbital; pt,pterygoid; q, quadrate; sj, synovial joint. Scale bar: 1 cm.

Download figure to PowerPoint

Fibrous joint can further be subdivided into two categories based on the articular surface morphology of the connecting elements. The first and most common fibrous joint is formed by overlapping bony processes (Fig. 4A,B) of the participating, mostly viscerocranial elements (see Table 3). This overlapping arrangement, which broadly speaking corresponds to the term scarf joint or sutura squamosa (Szentágothai and Réthelyi,2006), mostly implies broad, oblique contact areas between the bones that were joined by fibrous connective tissue. Table 3 summarizes the connecting skull elements that show this joint morphology and the overlapping-overlain relations of them detected in almost all referred specimens, where the preservation and incomplete fusion state allowed proper identification of joint morphology. The occurrence of overlapping fibrous joints between the referred skull elements is consistent and apparently universal among pterosaurs. The nature of connection between some palatal elements is ambiguous, because, apart from the few cases where significant information can be gained from specimens that are either exposed in palatal view or three dimensionally preserved (see Ősi et al.,2010), the palatal construction of most pterosaurian skulls is hypothetical at best. However, based on its long, narrow wing-like processes, the pterygoid is expected to have connected to the ectopterygoid, palatine, and maxilla via overlapping fibrous joint. This situation is found between the pterygoid and palatine in Dorygnathus banthensis SMNS 50702 and Pterodactylus sp. BSPG 1936 I 50. The same could have applied to the palatine-maxilla junction by virtue of the morphology of their contacting areas suggested by Ősi et al. (2010) and indeed seems to be the case in Dorygnathus banthensis BSPG 1938 I 49, SMNS 50914, WDC-CTG-001, Rhamphorhynchus muensteri SMNK PAL 6596, Pterodactylus sp. BSPG 1936 I 50. The ectopterygoid-maxilla junction is also overlapping in Rhamphorhynchus muensteri CM 11434.

Table 3. Skull elements forming overlapping joints with one another in the pterosaurian skull
Overlying elementOverlain element
  1. Abbreviations: f, frontal; j, jugal; l, lacrimal; mx, maxilla; n, nasal; p, parietal; pmx, premaxilla; po, postorbital; pt, pterygoid; q, quadrate; qj, quadratojugal; sq, squamosal.

pmxn, f
jmx, po, qj
nl, mx
pof, sq

The second fibrous joint category is the patent or interdigitating suture where the articulating parts of the elements are much more robust and distinct and do not become as thin as the overlapping bony processes (Fig. 4C,D). Patent (open) suture (sutura plana, Szentágothai and Réthelyi,2006, and see Fig. 4C) generally refers to an earlier developmental state of the interdigitating suture (Fig. 4D) and can be identified by the straight, noninterdigitating contact areas in skeletally immature specimens (Fig. 4C). These suture morphologies were present between the counter-elements of the frontal and parietal bones, in the frontoparietal suture, between the counterparts of the premaxillae, the premaxillae and nasals, and between some palatal elements such as the quadratopterygoid joint. Patent sutures were present between the counterparts of the frontals in Dorygnathus banthensis SMNS 18969, 50164, WDC-CTG-001 (Fig. 4C), Anurognathus ammoni (uncatalouged), Rhamphorhynchus muensteri BSPG 1938 I 503, Pterodactylus antiquus BSPG AS I 739, Pterodactylus kochi BSPG 1878 VI 1, Anhanguera piscator NSM-PV 19892, between the counterparts of the parietals in Dorygnathus banthensis SMNS 50164, WDC-CTG-001 (Fig. 4C), Campylognathoides liasicus SMNS 18879, Anurognathus ammoni (uncatalouged), and in the frontoparietal joint in Dorygnathus banthensis SMNS 18969, WDC-CTG-001 (Fig. 4C), Anurognathus ammoni (uncatalouged), Rhamphorhynchus muensteri BSPG 1938 I 503, Campylognathoides zitteli SMNS 9787, Campylognathoides liasicus SMNS 18879, Scaphognathus crassirostris GPIUB 1304, Pterodactylus kochi BSPG 1878 VI 1. The frontoparietal suture is often marked by a well-developed transversal ridge even in skeletally immature specimens with patent suture (e.g., Dorygnathus banthensis, WDC-CTG-001, Fig. 4C). Other specimens where the preservation and incomplete fusion state allowed the recognition of fibrous joints between the referred skull elements showed interdigitating sutures often with very faint suture lines (e.g., frontoparietal joint in Rhamphorhynchus muensteri 1934 I 36, Campylognathoides liasicus SMNS 50735, Scaphognathus crassirostris SMNS 59395, Pterodactylus kochi SMNF R 4074, Araripesaurus santanae BSPG 1982 I 90, etc.). Different fusion state on the dorsal and ventral side of the same elements also occurred; e.g., in Dorygnathus banthensis WDC-CTG-001 on the dorsal surface, the frontoparietal suture is apparently still open (Fig. 4C), whereas on the ventral surface it already shows an interdigitating appearance (Fig. 4D). In the very same specimen, the suture between the premaxillae is still visible on the dorsal surface, but there is no sign of it on the ventral surface. This might suggest an earlier fusion of the ventral or medial sides of the skull elements. Distinguishing overlapping and interdigitating suture morphology has proven to be difficult if the joint is completely fused.

Synovial joints are not frequently found in the skull of pterosaurs; however, there are some taxa and/or ontogenetic stages in which there is a seemingly synovial connection between the quadrate and squamosal (Figs. 4F, 5) and the basipterygoid and pterygoid bones (Figs. 4E, 6A). Among the investigated specimens, the bifenestratans Eudimorphodon ranzii MCSNB 2888, Austriadactylus cristatus SMNS 56342, Carniadactylusrosenfeldi MSFN 1797, Carniadactylus sp. MPUM 6009, Caviramusfilisurensis BNM 14524; Dimorphodon macronyx BMNH 41212-13 (Fig. 5E); Dorygnathus banthensis, WDC-CTG-001 (Fig. 7F), SMNS 18969, 50164, 55886, Campylognathoides liasicus SMNS 18879, Campylognathoides zitteli SMNS 9787 (Fig. 5A,B), Scaphognathus crassirostris GPIUB 1304, Rhamphorhyynchus muensteri BSPG 1938 I 503, and pterodactyloids Araripesaurus santanae, BSPG 1982. I. 90 (Fig. 5C), Anhanguera piscator NSM-PV 19892, Tapejara wellnhoferi SMNK PAL 1137 (Fig. 5D), AMNH 24440 most likely have had synovial quadrate-squamosal, i.e., otic joint. In these specimens, the quadrate has a distinct, well-developed condylus cephalicus on its ascending process (Fig. 5) which fits in the corresponding cotylus on the ventral side of the squamosal (Fig. 5B). The surface texture of condylus cephalicus is superbly preserved in Dorygnathus banthensis WDC-CTG-001 and undoubtedly indicative of hyaline cartilage covering (Fig. 5F). The nature of the basipterygoid-pterygoid, i.e., basal joint is ostensibly synovial in Eudimorphodon ranzii MCSNB 2888, Carniadactylusrosenfeldi MSFN 1797, Cacibupteryx caribensis IGO-V 208, Dorygnathus banthensis SMNS 18969, 50702, 51827 (Fig. 4E), Scaphognathus crassirostris GPIUB 1304, Rhamphorhynchus muensteri BSPG 1989 XI 1, SMNK PAL 6596, CM 11434 (Fig. 6A). In these specimens, the basipterygoid processes have distinct, blunt ending which articulate with the corresponding concave facet of the pterygoid (Fig. 6A). The expected rough surface structure distal to the presumably synovial articular surfaces (on the quadrate and basipterygoid) which would be suggestive of the presence of a synovial capsule is hardly discernible in any of the specimens either due to preservational or preparational artifacts. Acidic preparation for instance can result in destruction or modification of the original bone surface (e.g., Dorygnathus banthensis WDC-CTG-001), whereas transparent coating used to protect the fossils from chemical or mechanical effects might disguise important morphological attributes (e.g., Campylognathoides liasicus SMNS 18879, Dorygnathus banthensis SMNS 18969). Nevertheless, both the basal and otic joints are apparently synovial fulfilling two of the defined morphological criteria of cranial kinesis (Holliday and Witmer,2008).

thumbnail image

Figure 5. Examples for quadrates having distinct cephalic condyle (cc) at the proximal end of the ascending shaft which is indicative of synovial quadrate-squamosal (otic) joint. A, Campylognathoides zitteli SMNS 9787; B, Campylognathoides liassicus SMNS 18879; C, Araripesaurussantanae BSP 1982. I. 90; D, Tapejara wellnhoferi SMNK PAL 1137; E, Dimorphodon macronyx BMNH 41212-13; F, close up of the proximal view of cephalic condyle in Dorygnathus banthensis WDC-CTG-001 where the fine texture of the surface indicative of hyaline cartilage covering becomes apparent. Abbreviations: cc, cephalic condyle; q, quadrate; sqc, cotyle on squamosal. Scale bare of A, B, C, D: 1 cm; E: 0.5 cm.

Download figure to PowerPoint

thumbnail image

Figure 6. Joint types of three articulating palatal bones, basipterygoid (bpt), pterygoid (pt) and quadrate (q). A, The superbly preserved Rhamphorhynchus muensteri CM 11434 (“Carnegie specimen”) with in situ arrangement of these elements clearly shows that whereas the quadrate is fused to the pterygoid, the basipterygoid process forms an apparently synovial joint with the pterygoid (basal joint). B, Fused quadrate-pterygoid unit lying isolated on the slab of Campylognathoides liasicus SMNS 50735. Black and white arrows indicate the approximate or clear joining areas of the bones. Scale bar: 1 cm.

Download figure to PowerPoint

thumbnail image

Figure 7. Comparison of the ossification degree of the skull of A, a derived pterodactyloid, Anhanguera sp. (SMNK uncatalogued) and B, a bifenestratan, Dorygnathus banthensis (SMNS 55886). Note that whereas there are no visible suture lines between the skull elements of Anhanguera (A), the different skull elements of Dorygnathus (B) can easily be recognized due to the distinct suture lines (indicated by white arrows) that trace out the individual bone shapes.

Download figure to PowerPoint

As for possible “bending zones,” almost all viscerocranial elements of the pterosaurian skulls are considerably thin, and many of them are even lamella-like. However, on the medial surface they are always reinforced mechanically by a bracing system of thickened bony spars. For example in Dorygnathus banthensis WDC-CTG-001, the medial surface of the jugal is mechanically strengthened by a tetraradiate bracing system that run along the long axis of the four processes, whereas the maxilla is supported medially by a vertical lamina that enhances both the lateral nasal process and the ventral palatal plate (Ősi et al.,2010).

Protractor muscles. 

Following the criterion on the presence and development of protractor musculature defined by Holliday and Witmer (2008), the orbitotemporal part of the braincase has been investigated to search for possible attachment areas of musculus levator pterygoidei (mLPt) and musculus protractor pterygoidei (mPPt). These two muscle groups are generally considered as being of crucial importance in active kinesis: mLPt and mPPt are constrictor dorsalis muscles and play role in protraction of the kinetic system (the quadrate in the streptostylic movement), whereas the adductor musculature, m. adductor mandibulae externus and m. pterygoideus retract it (Herrel et al.,1999; Metzger,2002; Holliday and Witmer,2007,2008). Although the attachment areas can vary among different extant taxa, by and large mLPt originates on the ventral side of the parietal or on the fused laterosphenoid-prootic complex and inserts on the dorsal surface of the pterygoids; mPPt originates on the basisphenoid and/or prootic and inserts on the dorso-medial side of the pterygoid (Herrel et al.,1999; Metzger,2002; Holliday and Witmer,2007,2008).

The morphology of the pterygoid is well known in different pterosaurian taxa (for morphological description see Ősi et al.,2010). The corpus of this tetraradiate element is generally thin compared with its processes in bifenestratans (e.g., Dorygnathus banthensis SMNS 50164, Campylognathoides liasicus SMNS 50735, Rhamphorhynchus muensteri CM 11434) but might be more robust in monofenestratans (e.g., in Anhanguera sp. SMNK uncatalogued) without lateral process (see Ősi et al.,2010). In case protractor muscles were to attach on its surface, they probably would have inserted on the dorsal side of its corpus or near its posterior end which was more robust and connected to the basipterygoid and quadrate.

The orbitotemporal region of the pterosaurian skulls, however, is poorly known since the bones surrounding the endocranial cavity are pneumatic, thus badly crushed in most cases (Bennett,2001). In this respect, there are only handful examinable specimens, which bear reliable information for the adequate reconstruction of this skull region. These mostly three dimensional, well-prepared specimens (Tapejara wellnhoferi MCT 1500-R, AMNH 24440, Anhanguera sp. MCT 1501-R, Pteranodon sp. KUVP 976, 2212, YPM 1177, Coloborhynchus spielbergi RGM 401880) were not accessible for the authors of the recent article, thus the relevant braincase elements namely the basisphenoid, laterosphenoid, and prootic have been evaluated based exclusively on literature data (Kellner,1996; Wellnhofer and Kellner,1991; Bennett,2001; Veldmeijer et al.,2006). Detailed photos and explanatory figures of this region are found in Kellner (1996), Wellnhofer and Kellner (1991), and Bennett (2001).

The basisphenoid in pterosaurs is mostly elongated and anteroventrally directed in basal nonpterodactyloids as well as in the more derived pterodactyloids (Kellner,1996). Posteriorly, it contacts the basioccipital to which it is firmly fused with very faint or obliterated suture line, whereas anteriorly it forms the basipterygoid processes which articulate with the pterygoids. It borders the cranioquadrate opening medially, and its anterior end forms the posterior margin of the interpterygoid vacuity (Bennett,2001). In Tapejara wellnhoferi MCT 1500-R, the dorsal part of the basisphenoid is expanded but ventrally becomes thin. Anteriorly, it is connected to the interorbital septum by numerous bony struts, but its base is free of these trabeculae (Kellner,1996); the same condition that was found in Pteranodon (Bennett,2001). In AMNH 24440, the basisphenoid-parasphenoid complex is an expanded, somewhat concave bony plate (Wellnhofer and Kellner,1991). The basisphenoid of Pteranodon is an elongate element extending anteroventrally to contact the pterygoids via short but slightly expanded basipterygoid processes (Bennett,2001). In Coloborhynchus spielbergi RGM 401880, the basisphenoid narrows posteriorly, where it contacts the basioccipital.

The sutures of the laterosphenoid with the surrounding elements are mostly unclear, thus there are different interpretations concerning its extent in pterosaurs. Bennett (2001) considered it the element forming the interorbital septum, whereas Kellner (1996) regarded the interorbital septum as a separate element (pseudomesethmoid). Due to these (and probably also interspecific) differences, the contacts of the laterosphenoid are not alike in the two interpretations. According to Bennett (2001) in Pteranodon, it has a Y-shaped cross section dorsally, where it contacts the frontals, and ventrally it develops into a strut-meshwork reaching down to the basisphenoid. Anteriorly, its dorsal margin extends into the median pneumatic space. It has also lateral processes that extend from the anterodorsal corner and contact the lacrimals. The processes are not fused to the lacrimals but have blunt terminations. Posteriorly, the laterosphenoid may overlap the prootic and opisthotic. In contrast, Kellner (1996) described the laterosphenoid as being connected anteriorly to the frontal and via a medially directed process to the “pseudomesethmoid,” and posteriorly to the parietal and prootic in Tapejara wellnhoferi MCT 1500-R. In Anhanguera sp. MCT 1501-R, the laterosphenoid is expanded under the ventrolateral surface of the parietal and contacts the prootic posteroventrally (Kellner,1996).

The prootic along with the opisthotic and basioccipital form the walls and floor of the endocranial cavity. In Pteranodon, the prootic and opisthotic together form the otic capsule (Bennett,2001). The prootic has a complex morphology in Tapejara wellnhoferi MCT 1500-R, and lies between the laterosphenoid, parietal, and opisthotic in Anhanguera sp. MCT 1501-R (Kellner,1996).

All three braincase elements are pierced by foramina forming the passages of different cranial nerves. Elevated areas at the base of the laterosphenoid-prootic complex identified as the attachment areas for mLPt and mPPt in dinosaurs (Holliday and Witmer,2008) or muscle scars are not reported in any of the referred specimens, nor there is any other detailed study investigating skull musculature other than those which manipulate the mandible (Fastnacht,2005; Ősi,2010). Owing to the extensive free surface on the braincase and pterygoids, however, there are still remaining areas for potential protractor muscles to attach.

Degree of skull ossification. 

In the evaluation of fusion state of the skull, skeletally mature and immature specimens must be distinguished and ideally only mature specimens should be taken into account. Our investigation implies that most bifenestratans and derived monofenestratans (corresponding to Dsungaripteroidea in phylogenetic context [Kellner,2003]) seem to be consistently distinct in this regard (Fig. 7) with the derived, bifenestratan genus Rhamphorhynchus and basal monofenestratans (corresponding to Archaeopterodactyloidea in phylogenetic context [Kellner,2003]) occupying a fusion state somewhere between the two extremities. Most cranial elements of those bifenestratan pterosaur specimens that are generally considered adults are distinct (Eudimorphodon ranzii MCSNB 2888, Campylognathoides liasicus CM 11424, Carniadactylus sp. MPUM 6009, Caviramusfilisurensis BNM 14524, Dimorphodon macronyx BMNH 41212-13, Dorygnathus banthensis SMNS 50702, 51827, 55886 [Fig. 7B], Austriadactylus cristatus SMNS 56342, Anurognathus ammoni, uncatalouged), very often disarticulated or even scattered (Batrachognathus volans PIN 52-2, Dendrorhynchoides curvidentatus GMV2128, Dimorphodon macronyx BMNH R 1035, Dorygnathus banthensis SMNS 18969, 50164, 50914, BSPG 1938 I 49, WDC-CTG-001, Campylognathoides liasicus SMNS 18879, 50735, Campylognathoides zitteli SMNS 9787). In contrast, those specimens of derived monofenestratan pterodactyloids which are considered adults have completely ossified skulls with very faint or no suture lines (Anhanguera bittersdorffi uncatalouged holotype, Anhanguera sp. SMNK uncatalogued [Fig. 7A], Pteranodon sp. KUVP 976, 2212, YPM 1177, Tapejara wellnhoferi CD-R-080, Zhejiangopterus linhaiensis ZMNH M1330; Huaxiapterus benxiensis BXGM V0011 Quetzalcoatlus sp. TMM 41961-1, 41954-62) (Fig. 7A). An intermediate degree of skull ossification seems to be exhibited in almost all specimens of the derived bifenestratan Rhamphorhynchus muensteri (BSPG AS VI 34, 1867 II 2, 1927 I 36, 1929 I 69, 1934 I 36, 1955 I 28, 1989 XI 1, CM 11434, SMNK PAL 6596) and in monofenestratan archaeopterodactyloids (Pterodactylus antiquus BSPG AS I 739, Pterodactylus kochi BSPG AS XIX 3, 1937 I 18, SMNF R 4072, R 4074, Germanodactylus cristatus BSPG 1892 IV 1, Ctenochasma gracile BSPG 1920 I 57, Ctenochasma sp. SMNS 81803).

Figure 8 represents the summary of results, where the distribution of different morphological correlates, which might suggest potential for intracranial movements in pterosaurian skulls, is indicated in a phylogenetic context.

thumbnail image

Figure 8. The occurrence of different morphological correlates of potential cranial kinesis (see A, for symbol legend) in B, bifenestratan pterosaurs represented at genus level and C, pterodactyloid pterosaurs represented at genus and family level demonstrated in a phylogenetic context (modified from B, Dalla Vecchia,2009, and C, Andres and Ji,2008). Those taxa which have been examined by the authors personally are marked by asterisks, while data for the remainder have been taken from related literature. Taxa without symbols have not been investigated here. Note that all bifenestratans of well-known skull morphology except for Rhamphorhynchus have a quadrate with distinct cephalic condyle and possess an incompletely fused skull as adult. Low ossification degree of the skull is also characteristic of basal pterodactyloids (Archaeopterodactyloidea).

Download figure to PowerPoint


  1. Top of page
  2. Abstract
  8. Acknowledgements
  10. Supporting Information

Among the morphological features of pterosaurian skulls assessed in this study, there are some which seem to indicate intracranial movements, and others which apparently do not allow any mobility between the referred elements.

Joint Morphology and Mobility

The most common joint type, the overlapping joint (Fig. 4A,B) strongly resembles those found in dinosaurian skulls and has been considered by several authors to be capable of sliding motion (see Supporting Information). However, as Holliday and Witmer (2008) pointed out, there is no extant equivalent of such moveable joints; in fact this joint arrangement must have prevented any kind of motion between the joining elements. Nevertheless, there are synovial joints in which the participating elements do not show a typical convex condyle–concave cotyle morphology but rather both articular ends are straight, well defined and robust structures with smooth surfaces that can slide alongside each other like e.g., in the basipterygoid-pterygoid joint in the palate of birds (Zusi,1993) or Varanus (pers. obs.). The overlapping joints with elongated, tapering bony processes found in the pterosaurian and dinosaurian skulls, however, exhibit the morphological correlates of neither typical nor sliding synovial joints (see above). The morphology and structural arrangement of the overlapping joints in the pterosaurian skulls are rather indicative of syndesmoses or fibrous joints; something similar to the rigid scarf joints found in crocodiles (Ősi et al.,2010). In addition, the proposed sliding motion would have also been hampered by the immobility of adjacent bones. In agreement with Holliday and Witmer (2008) here, we reject the variety of intracranial movements via such “sliding” joints supposed for dinosaurs; thus the joints in the pterosaurian skulls in which the participating elements uniformly show this arrangement are regarded as being incapable of any significant movement. Hence, all the joints listed in Table 3 have been excluded from having potential for kinesis in pterosaurs.

Patent (Fig. 4C) or interdigitating fibrous joints (Fig. 4D) which are mostly completely fused without any traceable suture line in skeletally mature specimens indicate complete immobility between the connecting elements. For example in Dorygnathus banthensis SMNS 50164, the parietals are fused to the frontals, but the contralateral elements are not, which implies that these two elements fuse earlier during ontogeny than either the contralateral frontals or parietals to each other (in case there was a determinate order of fusion of cranial elements). This refers to the immobile nature of the frontoparietal joint already in earlier ontogenetic stage. However, in Campylognathoides liasicus SMNS 50735 the frontoparietal suture seems to be still open, whereas the contralateral elements are already fused without suture impression. Thus, either there is interspecific variation in the order of fusion of cranial elements or there is no determinate fusion order whatever. In any case, the transversal ridge indicating the frontoparietal suture in every ontogenetic stage would have prevented the mesokinetic dorsoventral rotation of the frontal along this suture, thus precluding the potential of the pterosaurian skull for mesokinesis (see Supporting Information). Based on the phylogenetic position of pterosaurs within Archosauromorpha (Fig. 1B,C after Sereno,1991; and Hone and Benton,2008, respectively), the absence of mesokinetic movements at the frontoparietal joint is to be expected. Fibrous joints found in other areas of the skull are also rigid and immobile.

The quadrate-squamosal joint with distinct condylus cephalicus on the quadrate (Fig. 5) that has a surface texture characteristic of hyaline cartilage covering (Fig. 5F) and with corresponding cotyle on the squamosal (Fig. 5B) suggests the presence of a synovial otic joint. The articular morphology found between the basipterygoid and pterygoid indicates the presence of synovial joint, too. With respect to function, it might seem obvious to presume that with such synovial morphology the quadrate must have been capable of anteroposterior rotation (streptostyly) along with the pro- and retraction of the basal unit via synovial basipterygoid-pterygoid joint. However, there is a serious problem with this assertion. This problem is related to other morphological constraints with which all concerned skull elements must be in accordance for the animal to achieve streptostyly. The animal either has to reduce some bony elements lateral and medial to the distal end of the quadrate or its connections to these bones must be significantly mobile (e.g., synovial or ligamentous connection) for it to be capable of anteroposterior rotation. In addition, if the basal joint was to be functional, too (pro- and retraction of the muzzle coupled with quadrate movement), the basal unit as well as the skull roof must have contained flexible regions. No reduction or mobility modification can be observed in the adjacent bones and skull regions in pterosaurs. The bones lateral to the quadrate form typical overlapping joints (quadratojugal overlaps the quadrate and is overlain by the jugal, see Table 3), and these bones are connected to all surrounding elements via overlapping joint, thus the position of them can be considered fixed. Hence they form a most probably immobile, rigid lower temporal arch which, along with the fused quadrate-pterygoid joint, would not allow the anteroposterior movement of the quadrate. In addition to that, the squamosal has a ventral process that overlaps the ascending process of the quadrate laterally which further fixes the position of the quadrate. Accordingly streptostyly can almost certainly be ruled out even in taxa such as Eudimorphodon ranzii (contrary to Ősi,2010), Dorygnathus banthensis, Tapejara wellnhoferi (juvenile), etc., where the form and construction of the quadrate-squamosal and basipterygoid-pterygoid regions are indicative of kinesis. In spite of their synovial morphology, the basal and otic joints were not to form movable joints, and this quasi-contradiction must be resolved. The term “synovial” is a structural joint category, which implies the morphology of the connecting elements but does not necessarily refer to a mobile (diarthrodial) joint (Holliday and Witmer,2008). Since many cranial elements, including the quadrate, ossify endrochondrally, i.e., hyaline cartilage is present during the ossification process (Dixon,1997), this articular surface structure can simply imply that these elements were connected by fibro- or hyaline cartilage thus forming a cartilaginous rather than real synovial joint. Cartilaginous joints or synchondroses are typically found between basicranial bones (connected by hyaline cartilage) and may ossify with age, or they form the intervertebral discs (hyaline + fibrous cartilage) (Szentágothai and Réthelyi,2006). Although the condyle-cotyle morphology is not usually found in cartilaginous joints, there is a significant variability and transition in the morphology of cartilaginous joints (Szentágothai and Réthelyi,2006), thus initially both of these types could have accounted for the described morphology in the basal and otic joints of pterosaurs. Nevertheless, if cartilage was present in these regions only to facilitate bone growth during earlier ontogenetic stages as it has already been suggested for the cranial bones of dinosaurs (Holliday and Witmer,2008), this morphology would only be present in skeletally immature specimens. Yet some bifenestratan specimens which show this feature are considered adults, thus skeletally mature (e.g., Eudimorphodon ranzii MCSNB 2888, Scaphognathus crassirostris GPIUB 1304, Campylognathoides liasicus SMNS 18879, Dorygnathus banthensis SMNS 50702, etc., see above). Hence, either the ontogenetic age of these specimens has to be re-defined or the cartilaginous covering, which adults also possessed, had a role other than simply providing places of bone growth. This leads us further to the problem of identifying ontogenetic stages in fossils and is discussed below.

The thin lamella-like elements, indeed, might have been relatively flexible and bending could have been structurally possible. However, even if the internal construction of the element itself had allowed bending in the thinner zones (e.g., the nasal does not have stiffening system), the arrangement of adjacent bones would not have allowed any bending movement. For instance, if there was any movement allowed along the thin region of the nasal, it would be a laterodorsal rotation relative to the dorsal process of the premaxilla. However, this motion must have been impeded by the adjacent but surely fixed bones (maxilla, lacrimal, frontal) to which it was connected via fibrous, immobile joints. Thus the exceptionally thin bone walls, which are so characteristic of the whole skeleton of pterosaurs, must have contributed to the lightness of the skull as well as postcranium rather than ensured structural flexibility.

Protractor Muscles and Mobility

The reconstruction of muscles in extinct animals is ambiguous at best. Reconstructions inferred from the presence of muscle scars, extensive bony surfaces, tubercles, etc., and/or from muscle arrangement found in the closest extant relatives (EPB) can be misleading for many reasons.

First, not all muscles leave muscle scars on their attachment areas. Muscle scars are to be expected in those muscles which connect to the bone via collagenous tendon, whereas muscles with fleshy attachment on the bone do not necessarily leave traces of their origination or insertion areas. On the other hand, surface modification on bones can be caused by other tissues, such as glands, neurovascular bundles, etc. (Witmer,1995), thus not necessarily by muscles. Even if the muscle most probably have had tendinous contact to the bone (concluded from EPB), the state of preservation, preparational artifact or the relatively hidden position of the bone (e.g., laterosphenoid, prootic) can all prevent the detection of muscle scars.

Second, the attachment areas need not be very extensive or distinct in any other way. In fact, free surface area on the bone, be it ever so limited, might provide places of attachment for smaller muscles.

Third, inferring from closest living relatives might be inherently dangerous in two ways. In the case of pterosaurs depending on the interpretation of their phylogenetic position (see for different phylogenies in Bennett,1996a; Hone and Benton,2008), the bracketing taxa in EPB might well be crocodiles, birds or lepidosauromorphs. These clades are very distinct morphologically as well as functionally (Schwarz et al.,2007) bearing relatively few common features and sometimes homology-relations in their skeleton and musculature are still not clear (Holliday and Witmer,2007). In addition, interspecific differences in the musculoskeletal system might be very high. For instance, regarding the skull of birds, some taxa exhibit passive cranial kinesis without any protractor muscle activity (rhynchokinesis in palaeognathous birds, Gusseklo and Bout,2005, see Supporting Information), while others (e.g., toucan) have completely akinetic skulls (for reference see Zusi,1993). Moreover, in the lepidosaur Sphenodon there is even intraspecific variance in the presence of the pro- and retractor muscles of the pterygoids, despite that they have completely akinetic skull (Metzger,2002).

In sum, the probability that pterosaurs possessed the protractor muscle system necessary for streptostyly cannot be estimated; their role in cranial kinesis, however, based on the evaluation of joint morphology, can be excluded.

Degree of Ossification and Mobility

The apparent incomplete ossification of the skull in most bifenestratan pterosaurs such as Eudimorphodon, Dorygnathus, Campylognathoides, etc., and the intermediate fusion state found in Rhamphorhynchus and archaeopterodactyloids like Pterodactylus or Ctenochasma, seem to occur irrespective of ontogenetic age and suggest loose connection between the cranial elements.

However, concerning fossil vertebrates, the terms adult, juvenile, skeletally mature, or immature often lead to confusion either because there is no consensus in their use or we do not know enough of the ontogeny of the extinct organism to define exactly what is meant by which (see Bennett,1995,1996b for a review). The small number of known specimens in most taxa further prevents the establishment of a more systematic terminology.

Although it seems to be true that most known bifenestratan pterosaurs and archeopterodactyloids have incompletely ossified skulls with at least distinct sutures, it still might be possible that all of these hitherto known specimens are skeletally immature. The continuous debate on whether the establishment of a new species is reasonable or the specimen only represents a different ontogenetic status of an already described species also illustrates this quandary (see Bennett,1996b,2007b; Dalla Vecchia,2002,2009). Those cases where the rest of the skeleton seems to be mature and only the skull indicates immaturity (e.g., Dorygnathus banthensis WDC-CTG-001, with fused syncarpals but isolated skull bones), raise an issue on whether there is a determined sequence of ossification process among different skeletal elements with the skull ossifying last.

On the other hand, the differences in the ossification degree of the skull and sometimes of other skeletal elements (e.g., carpals, scapulocoracoids) as well could refer to different ontogenetic strategies along the diverse evolutionary lineages of pterosaurs: whereas bifenestratan and archaeopterodactyloid pterosaurs could have grown a lifetime long with an accelerated development until reaching sexual maturity and after that a much more decelerated but still continuous growth (like modern crocodiles), derived pterodactyloids could have had determinate growth strategy. In this case, continuous growth would suggest the presence of open sutures a lifetime long, whereas derived pterodactyloids with determinate growth would have completely fused bones after reaching final body size. Bennett (1993) came to a very similar conclusion by suggesting indeterminate growth strategy for bifenestratan and more basal pterodactyloid pterosaurs after discussing characters that refer to different ontogenetic stages in pterosaurs. However, this interpretation contradicts to the results of the histological investigations on pterosaur bones which suggest that pterosaurs, even the more basal ones, had relatively fast and deterministic growth (de Ricqlès et al.,2000; Padian et al.,2004; Steel,2008; Chinsamy et al.,2008).

Another idea which might give an explanation for the differences includes biomechanical considerations. Stress-strain distribution and forces acting on a skull during feeding can be quite different when comparing a rigid, united skull (derived monofenestratans) with an incompletely fused and thus structurally more elastic skull (basal bifenestratan). In his biomechanical investigation, Fastnacht (2005) demonstrated that “butt-ended sutures resist compression but will fail in tension; scarf joints with oblique articulating surfaces accommodate tensile and compressive forces in all directions with usually only minor movement […]. Interdigitating contacts resist compressive and tensile forces and prevent slipping between adjacent bones” (pp. 31-32). He furthermore stated that most derived pterosaurs have fused skull with no sutural impression, which he referred to as “single unit skull.” In contrast, the Upper Triassic and Lower Jurassic pterosaurs possess a skull that consists of a cluster of bones that disarticulate post mortem, thus their cranium is a composite rather than a single unit skull (pp. 32). He also suggested that in brevirostrine taxa (e.g., anurognathids) the incomplete fusion of the skull elements may be a direct mechanical consequence of the high strains present in relatively short skulls (Fastnacht,2005, pp. 185). In this context, the issue of feeding strategy is of crucial importance: there could have been a principal difference in feeding behavior between basal and derived pterosaurs which was responsible for this alteration in ossification degree. Further evidence for different feeding mechanics stems from their probably different jaw musculature; an inference derived on one hand from the complexity of the basal pterosaur palates compared with those seen in some pterodactyloids (M. Witton, pers. com.), on the other from the difference in the inclination degree of the quadrate and the maximum gape (Ősi,2010).

Nevertheless, this field also abounds in uncertainties; hence it is not the most useful aspect to settle this question. Still, due to the aforementioned morphological features, the incomplete skull ossification of the considered specimens, regardless of whether they were adults or juveniles, skeletally mature, or immature, could not have resulted in cranial kinesis. Thus, if there indeed was a significant difference in the ossification degree and hereby in the mechanical behavior of the skull between these groups, this difference certainly did not lie in the potential of the more basal pterosaurs for cranial kinesis.

On the other hand, the incomplete fusion state of the skull could have been an ancestral heritage: although we know almost nothing about the origin of pterosaurs, it is almost certain that the ancestor must be envisioned as a small, arboreal, lizard-like diapsid reptile (Bennett,1997) which was most probably insectivorous (Ősi,2010). Since insectivory has been related to the evolution of cranial kinesis in amniotes (Bout and Zweers,2001), it is conceivable that the predecessors of pterosaurs indeed had kinetic skulls, which subsequently became rigid due to other, yet unknown mechanical constrains. Thus the unfused nature and other morphological features indicative of intracranial movements in the skull of basal pterosaurs can be considered as a residuum of a real kinetic skull which is already out of order. In this case, we might face the phenomenon called transfer exaptation which refers to the loss of original function of a certain feature (Arnold,1994).


  1. Top of page
  2. Abstract
  8. Acknowledgements
  10. Supporting Information

Our investigation shows that, based on morphological, comparative anatomical, phylogenetic, and ontogenetic considerations, the skull of most “adult” bifenestratan pterosaurs (e.g., Eudimorphodon ranzii, Dorygnathus banthensis, etc.) and “juvenile” pterodactyloid monofenestratan specimens (e.g., Tapejara wellnhoferi SMNK PAL 1137) is partially kinetically competent at best. Accordingly their skull possessed key synovial joints and probably the necessary protractor muscles but lacked bony gaps or additional mobile regions which would have permitted intracranial movements. Thus, the skull of bifenestratan pterosaurs as well as that of the skeletally immature individuals of derived pterodactyloids was virtually akinetic.

The presence of synovial joints and unfused sutures in the cranium of bifenestratan pterosaurs and archaeopterodactyloids has most probably phylogenetic roots. Among diapsids, there is a strong evidence of the plesiomorph nature of streptostyly, which secondarily became restricted to an immobile quadrate-squamosal joint in most archosaur clades. Currently, only birds have demonstrably streptostylic quadrate among archosaurs, but this is almost certainly a secondarily regained trait rather than a retained plesiomorphic character. The vestige of the streptostylic arrangement in other archosaurs, including bifenestratan and skeletally immature pterodactyloid pterosaurs, might well have represented cartilaginous regions that permitted and facilitated cranial growth during ontogeny and/or ensured that the skull could bear relatively high stress and strain loads. Thus the morphological features indicative of cranial kinesis in some pterosaurian taxa might well be related to the phenomenon called transfer exaptation. Equally possible is the assumption that these characters represent a functionless residuum of a real kinetic skull possessed by the hitherto unknown diapsid ancestor of pterosaurs.


  1. Top of page
  2. Abstract
  8. Acknowledgements
  10. Supporting Information

The authors wish to thank M. Witton (University of Portsmouth, Portsmouth) and the anonymous Reviewer for their useful comments that highly improved the standards of the manuscript; R. Böttcher and R. Schoch (Staatliches Museum für Naturkunde, Stuttgart), R. Brocke and T. Emmel (Senckenberg Forschungsinstitut und Naturmuseum, Frankfurt), O. Rauhut (Bayerische Staatsammlung für Paläontologie und Geologie, München) and E. Frey (Staatliches Museum für Naturkunde, Karlsruhe) for access to material and helpful assistance; B. Mueller (Texas Tech University, Texas), M. Lamanna (Carnegie Museum of Natural History, Pittsburgh), R. Elgin, and V. Griener (Staatliches Museum für Naturkunde, Karlsruhe) for providing pictures of indispensible pterosaur specimens; D. Schwarz-Wings (Museum für Naturkunde, Berlin), G. Zboray, and L. Makádi (Eötvös Loránd University, Budapest) for access to relevant literature and useful discussions.


  1. Top of page
  2. Abstract
  8. Acknowledgements
  10. Supporting Information
  • Andres B, Ji Q. 2006. A new species of Istiodactylus (Pterosauria, Pterodactyloidea) from the Lower Cretaceous of Liaoning, China. J Vert Paleont 26: 7078.
  • Andres B, Ji Q. 2008. A new pterosaur from the Liaoning Province of China, the pylogeny of the Pterodactyloidea, and convergence in their cervical vertebrae. Palaeontology 51: 453469.
  • Arnold E. 1994. Investigating the origins of performance advantage: adaptation, exaptation and lineage effects. In: EggletonP, Vane-WrightRI, editors. Phylogeny and ecology. London: Academic Press. p 123168.
  • Arnold E. 1998. Cranial kinesis in lizards: variations, uses, and origins. In: HechtM, MacintyreR, CleggM, editors. Evolutionary biology. New York: Plenum Press. Vol 30: p 323357.
  • Arthaber G. 1919. Studien über Flugsaurier auf Grund der Bearbeitung des Wiener Exemplares von Dorygnathus banthensis Theod. sp. Denkschr Akad Wiss Wien math.-nat Kl 97: 391464.
  • Bahl KN. 1937. Skull of Varanus monitor. Rec Ind Mus 39: 133174.
  • Bennett SC. 1993. The ontogeny of Pteranodon and other pterosaurs. Paleobiology 19: 92106.
  • Bennett SC. 1995. A statistical study of Rhamphorhynchus from the southern limestone of Germany: year classes of a single large species. J Vert Paleont 69: 569580.
  • Bennett SC. 1996a. The phylogenetic position of the Pterosauria within the Archosauromorpha. Zool J Linn Soc 118: 261308.
  • Bennett SC. 1996b. Year classes of pterosaurs from the Solnhofen Limestone of Germany: taxonomic and systematic implications. J Vert Paleont 16: 432444.
  • Bennett SC. 1997. The arboreal leaping theory of the origin of pterosaur flight. Hist Biol 12: 265290.
  • Bennett SC. 2001. The osteology and functional morphology of the Late Cretaceous pterosaur Pteranodon. Part II. Functional morphology. Paläontographica 260A: 113153.
  • Bennett SC. 2007a. A second specimen of the pterosaur Anurognathus ammoni. Paläontol Z 81: 376396.
  • Bennett SC. 2007b. A review of the pterosaur Ctenochasma: taxonomy and ontogeny. N Jb Geol Paläont Abh 245: 2331.
  • Bout RG, Zweers GA. 2001. The role of cranial kinesis in birds. Comp Biochem Physiol 131A: 197205.
  • Buffetaut E, Girgorescue D, Csiki Z. 2002. A new giant Pterosaur with a robust skull from the latest Cretaceous of Romania. Naturwissenschaften 89: 180184.
  • Bühler P. 1981. Functional anatomy of the avian jaw apparatus. In: KingAS, McLellandJ, editors. Form and function in birds. New York: Academic Press. Vol 2: p 439468.
  • Cai Z, Wei F. 1994. Zhejiangopterus linhaiensis gen. et sp. nov. (Pterosauria) from the Upper Cretaceous of Linhai, Zhejiang, China” (In Chinese). Vertebrat Palasiatic 32: 181194.
  • Campos DA, Kellner AWA. 1985. Panorama of the flying reptiles in Brazil and South America (Pterosauria|Pterodactyloidea|Anhangueridae). An Acad Bras Cienc 57: 141142, 453–466.
  • Chiappe LM, Norell MA, Clark JM. 1998. The skull of a relative of the stem-group bird Mononykus. Nature 392: 275278.
  • Chinsamy A, Codorniú L, Chiappe L. 2008. Developmental growth patterns of the filter-feeder pterosaur, Pterodaustro guinazui. Biol Lett 4: 282285.
  • Colbert EH, Russell DA. 1969. The small Cretaceous dinosaur Dromaeosaurus. Am Mus Nov 2380: 149.
  • Condon K. 1987. A kinematic analysis of mesokinesis in the Nile monitor (Varanus niloticus). Exp Biol 47: 7387.
  • Dalla Vecchia FM. 2002. Observations on the non-pterodactyloid pterosaur Jeholopterus ningchengensis from the early Cretaceous of northeastern China. Nat Nasc 24: 827.
  • Dalla Vecchia FM. 2009. Anatomy and systematic of the pterosaur Carniadactylus gen. n. rosenfeldi (Dalla Vecchia, 1995). Riv Ital Paleont Stratigr 115: 159188.
  • de Ricqlès A, Padian K, Horner JR, Francillon-Viellot H. 2000. Paleohistology of the bones of pterosaurs (Reptilia: Archosauria): anatomy, ontogeny and biochemical implications. Zool J Linn Soc 129: 349385.
  • Dixon AD. 1997. Prenatal development of the facial skeleton. In: DixonAD, HoyteDAN, RönningO, editors. Fundamentals of craniofacial growth. London: CRC Press LLC. p 6089.
  • Fastnacht M. 2005. Jaw mechanics of the pterosaur skull construction and the evolution of toothlessness. PhD Thesis. Johannes Gutenberg Universität, Mainz, p 3132, 180–185.
  • Frazzetta TH. 1962. A functional consideration of cranial kinesis in lizards. J Morph 111: 287319.
  • Frazzetta TH. 1983. Adaptation and function of cranial kinesis in reptiles: a time–motion analysis of feeding in alligator lizards. In: RhodinAGJ, MiyataK editors. Advances in herpetology and evolutionary biology: essays in honor of E.E. Williams. Cambridge: Museum of Comparative Zoology Publication. p 222244.
  • Galton PM. 1974. The ornithischian dinosaur Hypsilophodon form the Wealden of the Isle of Wight. Bull Brit Mus Nat His 25: 1152.
  • Gasparini Z, Fernández M, de La Fuente M. 2004. A new pterosaur from the Jurassic of Cuba. Palaeontology 47: 919927.
  • Gussekloo SWS, Bout RG. 2005. Cranial kinesis in palaeognathous birds. J Exp Biol 208: 34093419.
  • Herrel A, De Vree F. 1999. Kinematics of intraoral transport and swallowing in the herbivorous lizard Uromastix acanthinurus. J Exp Biol 202: 11271137.
  • Herrel A, De Vree F, Delheusy V, Gans C. 1999. Cranial kinesis in gekkonid lizards. J Exp Biol 202: 36873698.
  • Herring S, Teng S. 2000. Strain in the braincase and its sutures during function. Am J Phys Anthropol 112: 575593.
  • Holliday CM, Witmer LM. 2007. Archosaur adductor chamber evolution: integration of musculoskeletal and topological criteria in jaw muscle homology. J Morph 268: 457484.
  • Holliday CM, Witmer LM. 2008. Cranial kinesis in dinosaurs: intracranial joints, protractor muscles, and their significance for cranial evolution and function in diapsids. J Vert Paleont 28: 10737088.
  • Hone DWE, Benton MJ. 2008. Contrasting total-evidence and supertree methods: the origin of the pterosaurs. Zitteliana B 28: 3560.
  • Hooley RW. 1913. On the skeleton of Ornithodesmus latidens; an Ornithosaur from the Wealden Shales of Atherfield (Isle of Wight). Q J Geol Soc 96: 372422.
  • Iordansky NN. 1989. “Jaw apparatus of perennibranchiate urodelans and some problems of heterochronous evolution,” (in Russian). Zool Zhur 73: 8799.
  • Iordansky NN. 1990. Evolution of cranial kinesis in lower tetrapods. Neth J Zool 40: 3254.
  • Kellner AWA. 1989. A new edentate pterosaur of the Lower Cretaceous from the Araripe Basin, Northeast Brazil. An Acad Bras Cienc 61: 439446.
  • Kellner AWA. 1996. Description of the braincase of two early Cretaceous pterosaurs (Pterodactyloidea) from Brazil. Am Mus Nov 3175: 134.
  • Kellner AWA. 2003. Pterosaur phylogeny and comments on the evolutionary history of the group: In: BuffetautE, MazinJM, editors. Evolution and palaeobiology of Pterosaurs. Geological Society Special Publication, no. 217, p 105137.
  • Kellner AWA, Langston W. 1996. Cranial remains of Quetzalcoatlus (Pterosauria, Azhdarchidae) from late Cretaceous sediments of Big Bend National Park, Texas. J Vert Paleont 16: 222231.
  • Kellner AWA, Tomida Y. 2000. Description of a new species of Anhangueridae (Pterodactyloidea) with comments on the pterosaur fauna from the Santana Formation (Aptian -Albian), Northeastern Brazil. Nation Sci Mus Monogr 17: 1135.
  • Lee MSY. 2001. Molecules, morphology, and the monophyly of diapsid reptiles. Contrib Zool 70: 122.
  • Lü J, Gao Y, Xing L, Li Z, Ji Q. 2007. A new species of Huaxiapterus (Pterosauria: Tapejaridae) from the early Cretaceous of western Liaoning, China. Acta Geol Sin 81: 683687.
  • Lü J, Unwin DM, Jin X, Liu Y, Ji Q. 2009. Evidence for modular evolution in a long tailed pterosaur with a pterodactyloid skull. Proc Roy Soc, doi: 10.1098/rspb.2009. 1603.
  • Mazzetta GV, Farina RA, Vizcaino SF. 1998. On the palaeobiology of the South American horned theropod Carnotaurus sastrei Bonaparte. In: Pérez-MorenoBP, HoltzTR, SanzJL, Jr., MoratallaJJ, editors. Aspects of theropod paleobiology. Gaia Special Volume No 15. Lisbon: Museu Nacional de História Natural. p 185192.
  • Metzger K. 2002. Cranial kinesis in Lepidosaurs: skulls in motion. In: AertsP, AoutKD, HerrelA, Van DammeR, editors. Topics in functional and ecological vertebrate vertebrate morphology. Maastricht: Shaker Publishing. p 1546.
  • Norman DB. 1984. On the cranial morphology and evolution of ornithopod dinosaurs. Symp Zool Soc 52: 521547.
  • Norman DB, Weishampel DB. 1985. Ornithopod feeding mechanisms: their bearing on the evolution of herbivory. Am Nat 126: 151164.
  • Ősi A. 2010. Feeding related characters in basal pterosaurs: implications for dental function, jaw mechanism and diet. Lethaia, DOI: 10.1111/j.1502-3931.2010.00230.x.
  • Ősi A, Prondvai E, Frey E, Pohl B. 2010. New interpretation of the palate of pterosaurs. Anat Rec 293: 243258.
  • Padian K, Horner JR, de Ricqles A. 2004. Growth in small dinosaurs and pterosaurs: the evolution of archosaurian growth strategies: J Vert Paleont 24: 555571.
  • Patchell FC, Shine R. 1986. Feeding mechanisms in pygopodid lizards: how can Lialis swallow such large prey? J Herpet 20: 5964.
  • Rieppel O. 1978. The phylogeny of cranial kinesis in lower vertebrates, with special reference to the Lacertilia. N Jb Geol Paläont Abh 156: 353370.
  • Rieppel O. 1993. Patterns of diversity in the reptilian skull. In: HankenJ, HallBK editors. The skull: patterns of structural and systematic diversity. Chicago: University of Chicago Press. p 344390.
  • Rieppel O, Gronowski RW. 1981. The loss of the lower temporal arcade in diapsid reptiles. Zool J Linn Soc 72: 203217.
  • Ryabinin AN. 1948. “Remarks on a flying reptile from the Jurassic of the Kara-Tau” (In Russian). Akad Nauk, Paleont Inst, Trudy, Moscow and Leningrad 15: 8693.
  • Schwarz D, Frey E, Meyer C. 2007. Novel reconstruction of the orientation of the pectoral girdle in sauropods. Anat Rec 290: 3247.
  • Sereno PC. 1991. Basal archosaurs: phylogenetic relationships and functional implications. J Vert Paleont 11( Suppl): 153.
  • Smith KK, Hylander WL. 1985. Strain gauge measurement of mesokinetic movement in the lizard Varanusexanthematicus. J Exp Biol 114: 5370.
  • Stecher R. 2008. A new Triassic pterosaur from Switzerland (Central Austroalpin, Grisons), Raeticodactylus filisurensis gen. et sp. nov. Swiss J Geosci 101: 185201.
  • Steel L. 2008. The palaeohistology of pterosaur bone: an overview. Zitteliana B 28: 109125.
  • Szentágothai J, Réthelyi M. 2006. “Functional Anatomy I” (In Hungarian). RéthelyiM editor, 8th ed. Budapest: Medicina Press. p 375399.
  • Summers AP, Wake MH. 2005. The retroarticular process, streptostyly and the caecilian jaw closing system. Zoology 108: 307315.
  • Throckmorton G. 1976. Oral food processing in two herbivorous lizards, Iguana iguana (Iguanidae) and Uromastix aegypticus (Agamidae). J Morphol 148: 363390.
  • Unwin DM. 2003. On the phylogeny and evolutionary history o pterosaurs. In: BuffetautE, MazinJM, editors. Evolution and Palaeobiology of Pterosaurs. Geological Society Special Publication, no. 217, p 139190.
  • Veldmeijer AJ, Meijer HJM, Signore M. 2006. Coloborhynchus from the Lower Cretaceous Santana Formation, Brazil (Pterosauria, Pterodactyloidea, Anhangueridae); an update. Vert Paleont 3: 1529.
  • Versluys J. 1910. Streptostylie bei Dinosauriern, nebst Bemerkungen über die Verwandtschaft der Vögel und Dinosaurier. Zool Jb Anat 30: 175260.
  • Versluys J. 1912. Das Streptostylie-Problem und die Bewegungen im Schädel bei Sauropsiden. Zool Jb Anat( Suppl 15): 545716.
  • Wang X, Kellner AWA, Jiang S, Meng X. 2009. An unusual long-tailed pterosaur with elongated neck from western Liaoning of China. An Acad Bras Ciênc 81: 793812.
  • Wang X, Kellner AWA, Zhou Z, Campos D de A. 2007. A new pterosaur (Ctenochasmatidae, Archaeopterodactyloidea) from the Lower Cretaceous Yixian Formation of China. Cretac Res 28: 245260.
  • Wang X, Zhou Z. 2003. A new pterosaur (Pterodactyloidea, Tapejaridae) from the Early Cretaceous Jiufotang Formation of Western Liaoning, China and its implications for biostratigraphy. Chinese Sci Bull 48: 1623.
  • Wellnhofer P. 1974. Campylognathoides liasicus (Quenstedt), an Upper Jurassic pterosaur from Holzmaden—The Pittsburgh specimen. Ann Carnegie Mus 45: 534.
  • Wellnhofer P. 1978. Handbuch der Paläoherpetologie. Teil 19. Pterosauria. Stuttgart: Gustav Fischer Verlag.
  • Wellnhofer P, Kellner AWA. 1991. The skull of Tapejara wellnhoferi Kellner (Reptilia: Pterosauria) from the Lower Cretaceous Santana Formation of the Araripe Basin, Northeastern Brazil. Mitt Bayer Staatsslg Paläont Hist Geol 31: 89106.
  • Wild R. 1978. Die Flugsaurier (Reptilia, Pterosauria) aus der Oberen Trias von Cene bei Bergamo, Italien. Boll Soc Paleont It 17: 176256.
  • Wild R. 1984. Flugsaurier aus der Obertrias von Italien. Naturwissenschaften 71: 111.
  • Witmer LM. 1995. The Extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. In: ThomasonJJ, editor. Functional morphology in vertebrate paleontology. New York: Cambridge University Press. p 1933.
  • Zusi RL. 1984. A functional and evolutionary analysis of rhynchokinesis in birds. Smithson Contrib Zool 395: 140.
  • Zusi RL. 1993. Patterns of diversity in the avian skull. In: HankenJ, HallBK, editors. The skull: patterns of structural and systematic diversity. Chicago: University of Chicago Press. p 391437.

Supporting Information

  1. Top of page
  2. Abstract
  8. Acknowledgements
  10. Supporting Information

Additional Supporting Information may be found in the online version of this article.

AR_21376_sm_suppinfo.doc159KSupporting Information.

Please note: Wiley Blackwell is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.