Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 5 (2002) 239-263 10.11.2002

On the systematic relationships of CearadactyZus atrox, an enigmatic Early Cretaceous pterosaur from the Santana Formation of Brazil

David M. Unwinl

With 6 figures

Abstract

Cearadactylus atrox, a large pterodactyloid pterosaur represented by an incomplete skull and lower jaw from the Lower Cretaceous Santana Formation of Brazil, is a valid species. Diagnostic characters include a mandibular symphysis with a transversely expanded ‘spatulate’ anterior end that is considerably wider than the rostral spatula, and a third rostral tooth that has a basal diameter more than three times that of the fifth tooth. Additional diagnostic characters, contingent upon assign- ment of Cearadactylus atrox to the Ctenochasmatidae, include: anterior ends of jaws divaricate and containing 7 pairs of rostral teeth and 6 pairs of mandibular teeth; marked dimorphodonty, with an abrupt change in tooth morphology; and a “high cheek”. ‘Ceurudactylus? ligubuei’ Dalla Vecchia, 1993, based on an incomplete skull, also from the Santana Formation, is not related to Cearadactylus utrox, exhibits several ornithocheirid synapomorphies and is referred, tentatively, to Anhun- gueru. Ceurudactylus atrox exhibits various synapomorphies of the Ctenochasmatidae (rostrum anterior to nasoantorbital fe- nestra greater than half total skull length, teeth in anterior part of dentition relatively elongate and pencil-shaped, premaxilla has at least 7 pairs of teeth), the defining synapomorphy of the Gnathosaurinae (rostrum with dorsoventrally compressed laterally expanded spatulate anterior expansion), and shares two synapomorphies with the Chinese gnathosaurine Huanhep- terus quingyangensis (anterior tips of jaws divaricate, teeth restricted to anterior half of mandible). Two elongate cervical vertebrae, also from the Santana Formation and previously assigned to ‘Suntunadactylus brusilensis’, are tentatively referred to Ceuruductylus. Reconstruction of the temporal history of the Ctenochasmatidae suggests that while ctenochasmatines became increasingly specialised for filter feeding, gnathosaurines changed from sieve feeding to piscivory, acquiring several cranial characters that are similar to those of ornithocheirids, a group that also includes large aerial piscivores that used a terminal tooth grab for prey capture.

Key words: Pterosaur, Lower Cretaceous, Brazil, Cearaductylus, Ctenochasmatidae.

Zusammenfassung

Cearadactylus atrox aus der Santana-Formation (Unterkreide, NO-Brasilien) ist eine valide Art. Eine Revision des Taxons, von dem ein unvollstandiger Schadel mit Unterkiefer vorliegt, ergab folgende diagnostische (autapomorphe) Merkmale. Die Symphyse hat ein transversal verbreitertes spatelformiges Vorderende, das deutlich breiter ist als das Schnauzenende. Der dritte rostrale Zahn erreicht einen basalen Durchmesser, der jenen des fiinften Zahns um das Dreifache ubertrifft. Hinzu kommen Merkmale, die C. atrox mit der Ctenochasmatidae gemein hat, darunter die vorn auseinanderklaffenden Kieferran- der, sieben rostrale Zahnpaare, sechs Unterkieferzahnpaare, eine ausgepragte Dimorphodontie sowie eine hohe Wangenre- gion. ‘Cearadactylus ? Zigubuei‘ Dalla Vecchia 1993, ebenfalls mit einem unvollstandigen Schadel belegt, ist nicht naher mit C. atrox venvandt. Im Gegensatz zu letzterem zeigt ‘C. ? Zigubuei’ signifikante Ahnlichkeiten mit den Omithocheiridae. Unter Vorbehalt wird er hier der Gattung Anhanguera zugeordnet. C. atrox hat neben eindeutigen Synapomorphien der Ctenochas- matidae, z. B. erreicht das Rostrum anterior des nasoantorbitalen Fensters mehr als die halbe Schadellange, die vordersten Zahne sind verlangert und stiftformig und die das Pramaxillare tragt mindestens sieben Zahnpaare. Daneben besitzt C. atrox auch noch die entscheidende Synapomorphie der Gnathosaurinae, namlich ein Rostrum mit dorsoventral komprimierter vor- derem Auswuchs. AuBerdem ist C. atrox gekennzeichnet durch zwei Autapomorphien des Gnathosaurinen Huanhepterus quin- gyungensis aus China: divergierende Schnauzenenden und Zahne begrenzt auf vordere Kieferhalfte. SchlieBlich werden zwei lange Halswirbel, die auch aus der Santana Formation stammen und bislang zu Suntunadactylus brusiliensis gerechnet wurden, unter Vorbehalt zu Ceuruductylus gestellt. Die Evolutionsgeschichte der Ctenochasmatidae ist durch eine zunehmende Spezia- lisierung auf filternde Ernahrungsweise gekennzeichnet. Die Gnathosaurinen dagegen stellten sich von der filternden auf eine piscivore Ernahrung um, wobei sie eine Reihe von Schadelmerkmalen erworben haben, die den Ornithocheiriden konvergent ahnlich ist.

Schliisselworter: Pterosaurier, Unter-Kreide, Brasilien, Ornithocheiridae, Ctenochasmatidae.

Museum fiir Naturkunde der Humboldt-Universitat, Institut fur Palaontologie, Invalidenstr. 43, D-10115 Berlin, Germany. Received April, accepted July 2002 240 Unwin, D. M., Cearadactylus from the Santana Formation

Introduction from other deposits. Two distinct approaches are discernable. Some workers (e.g. Price 1971, The Romualdo Member of the Lower Cretaceous Wellnhofer 1977, 1985, BuisonjC 1980, Kellner Santana Formation of Brazil has yielded a re- 1984, Campos & Kellner 1985, Leonardi & Bor- markably well preserved and diverse pterosaur as- gomanero 1985, Kellner 1989) have erected new semblage (e.g. Campos & Kellner 1985, Wellnho- genera and even families for Santana pterosaurs, fer 1985, 1987, 1991a, b, c, Unwin 1988, Kellner subsequently assigning similar forms from other 1990, Martill 1993, Kellner & Tomida 2000). Un- Cretaceous deposits to these taxa (e.g. Kellner & like most fossils of pterosaurs, skeletons are often Tomida 2000). Others (e.g. Fastnacht 2001, Un- preserved uncrushed (e.g. Wellnhofer 1988, win 2001) have argued that some species of San- 1991c), although they are rarely complete (Kell- tana pterosaurs belong within previously estab- ner & Tomida 2000), and some examples of soft lished genera such as Ornithocheirus Seeley, tissue preservation have also been reported 1869 and Coloborhynchus Owen, 1874, both (Campos et al. 1984, Martill & Unwin 1989, Mar- based on material from the late Lower Cretac- till et al. 1990, Kellner 1997). A surprising aspect eous of England (see Unwin 2001). The situation is the apparent diversity of this assemblage: 17 is even more confused at higher taxonomic le- species distributed among 9 genera representing vels with, for example, some authors continuing at least 3 families have been reported so far to use the name Anhangueridae Campos & Kell- (Kellner & Tomida 2000: table 9). This excludes ner, 1985, even though as I have noted else- taxa from the Crato Formation which has been where (Unwin 2001) the content and diagnosis included in the Santana Formation (e.g. Maisey of this family is practically identical to that of 1991), but is now recognised as a distinct unit the Ornithocheiridae Seeley, 1870, an older and (Martill & Wilby 1993), perhaps as much as thus senior synonym. 10 million years older, although with a rather simi- Revision of the taxonomy and relationships of lar pterosaur assemblage (Frey & Martill 1994, Santana pterosaurs is needed if the potential of Martill & Frey 1998,1999, Saygo & Kellner 2000). this important assemblage for understanding the Various workers (e.g. Wellnhofer 1987, 1991c, anatomy, functional morphology, ecology and Unwin 1988, 2001, Kellner & Tomida 2000) have evolutionary history of pterosaurs is to be fully suggested that the apparent species diversity of realised. Here, attention is focused on one of the the Santana Formation assemblage may have earliest and most unusual pterosaurs to be de- been inflated by excessive taxonomic splitting, scribed from the Santana Formation, Cearadacty- leading to a situation that closely resembles early lus, currently represented by two species: Ceara- stages in the development of the taxonomic un- dactylus atrox Leonardi and Borgomanero, 1985 derstanding of other pterosaur assemblages such and ‘Cearadactylus? ligabuei’ Dalla Vecchia, as the Solnhofen Limestone (Wellnhofer 1970, 1993, although the latter is only tentatively as- 1975a) and the Cambridge Greensand (Welln- signed to this genus. This study set out to answer hofer 1978, Unwin 2001). In the case of the San- four questions: (1) Is Cearadactylus atrox a dis- tana Formation, oversplitting can be partially at- tinct, diagnosable and valid taxon? (2) Can the tributed to the non-comparability of some relationship of ‘Cearadactylus? ligabuei’ to C. species because of incomplete preservation atrox be resolved? (3) What are the relationships (Wellnhofer 1987, 1991c, Kellner & Tomida of C. atrox to other pterosaurs? (4) Can any 2000). More problematic, however, has been the other fossil material from the Santana Formation assignment of decisive taxonomic value to ques- be assigned to C. atrox? tionable characters such as size, the degree of Two circumstances allow these questions to be fusion of skeletal elements and, most controver- answered. First, recent systematic revisions of sially, the morphology and position of cranial Santana pterosaurs (e.g. Fastnacht 2001) and re- crests. The latter are widely distributed among lated assemblages such as that from the Cam- Santana pterosaurs and have often been cited as bridge Greensand (Unwin 2001), together with key diagnostic features (e.g. Campos & Kellner work now underway on other undescribed speci- 1985, Kellner & Tomida 2000), even though their mens, are helping to resolve the taxonomy of variation and distribution are still poorly under- Cretaceous pterosaurs and provide a clearer and stood, and their function unclear (Plieninger more robust taxonomic framework against which 1907, Bennett 1993, 2002). C. atrox and ‘C.? ligabuei’ can be more effec- A second problem concerns the relationships tively assessed. Secondly, recent studies of the of Santana pterosaurs to each other and to taxa interrelationships of pterosaurs (Howse 1986, Mitt. Mus. Nat.kd. Berl.. Geowiss. Reihe 5 (2002) 241

Bennett 1989, 1994, Unwin 1992a, 1995, in press, first valid use of the name, accompanied by a Unwin & Lu 1997, Unwin et al. 2000, Kellner detailed description and illustrations of the holo- 1996, Peters 1997, Viscardi et al. 1999), have type, an incomplete skull and lower jaw, ap- greatly improved our understanding of pterosaur peared two years later (Leonardi & Borgoma- phylogeny and can be used to reassess the rela- nero 1985). This was the fifth pterosaur species tionships of Cearadactylus. to be described from the Santana Formation, but In this work, paraphyletic taxa are denoted by only the second based on skull material, and the enclosure in double quotation marks. Invalid first represented by an associated rostrum and taxonomic names or those of doubtful validity mandibles. To date, and despite the large num- are indicated by citation in single quotation ber of pterosaur remains reported from the San- marks. Notwithstanding the remarks above, the tana Formation since 1985, no further material, Santana Formation pterosaur Anhanguera still cranial or postcranial, has been referred to this presents a particular taxonomic problem. Using species. new material, Fastnacht (2001) has convincingly According to Leonardi & Borgomanero (1983, demonstrated that ‘Tropeognathus’ robustus 1985), features such as the spatulate ends of the Wellnhofer, 1987, also from the Santana Forma- rostrum and mandibular symphysis, the he tero- tion, should be assigned to Coloborhynchus. Frey dont dentition and the absence of a cranial crest & Martill (in press) point out that the holotype distinguished C. atrox from all previously de- and only known specimen of ‘Anhanguera pisca- scribed pterosaurs, including the two forms to tor’ (NSM-PV 19892) is identical to the two spe- which it was most similar, Gnathosaurus subula- cimens representing Coloborhynchus robustus, tus H. v. Meyer, 1834 and Huanhepterus quin- an opinion which is supported here. ‘Anhanguera gyangensis Dong, 1982. Leonardi & Borgoma- piscator’ Kellner & Tomida, 2000 is thus treated nero (1985) were unable to make any direct here as a junior synonym of Coloborhynchus ro- comparisons with the first three pterosaurs to be bustus (Wellnhofer, 1987). Additionally, since described from the Santana Formation: Araripe- other species of Anhangera are similar to C. ro- saurus castilhoi Price, 1971, based on an incom- bustus, this raises the possibility that Anhanguera plete right forelimb; Araripedactylus dehmi Well- may be a junior synonym of Coloborhynchus nhofer, 1977, a wing-finger phalanx, and (Frey & Martill in press). Until this issue is re- Suntunadactylus brasilensis BuisonjC, 1980, repre- solved, however, I prefer to retain Anhanguera, sented by an incomplete shoulder girdle and as- at least for the reception of A. blittersdorfi and sociated humerus described together with two as- other nominal species including A. araripensis sociated cervicals from another individual and (Wellnhofer, 1985) and A. santanae (Wellnhofer, almost certainly not from the same taxon (Kell- 1985). ner & Tomida 2000, see also below). This left open the possibility that the holotype of C atrox might belong to one of these three taxa. In addi- Institutional abbreviations tion, Leonardi & Borgomanero (1985) did not mention Brasileodactylus araripensis, described BSP, Bayerische Staatssammlung fiir Palaontologie und Geo- the previous year by Kellner (1984) on the basis logie, Munich, Germany; CSRL, Centro Studi e Ricerche Li- gabue, Venice, Italy; DNPM, Departamento Nacional Pro- of an anterior portion of a mandibular symphy- duqlo Mineral, Brazil; F-PV, Borgomanero Collection, Rua sis. However, in his account of this pterosaur Almirante Tamandark 915, 8000 Curitiba PR, Brazil; GIUA, Kellner (1984) noted various features, including Geological Institute, University of Amsterdam, The Nether- lands; IMCF, Iwaki Coal and Fossil Museum, Iwaki, Japan; the absence of divaricate jaw tips, that appeared NSM, National Science Museum, Tokyo, Japan. to distinguish it from Cearadactylus atrox. The following year, Campos & Kellner (1985) described another new Santana pterosaur, An- A history of the study of Cearadactylus atrox hanguera blittersdorfi, based on a complete skull lacking mandibles. According to these authors, The name Cearadactylus atrox was first intro- C. atrox was clearly distinct from A. blittersdorfi duced by G. Leonardi and G. Borgomanero in because it lacked a sagittal crest, and had divari- 1983, for a new pterosaur from the Lower Cre- cate jaw tips and a differently shaped nasoantor- taceous Santana Formation of Brazil, although bital fenestra. In the same year, Wellnhofer the circumstances of its publication, in an ab- (1985) described a series of new species from the stract of the 7th Brazilian Congress of Paleontol- Santana Formation, two of which, Santanadacty- ogy, rendered the name a nomen nudum. The lus araripensis Wellnhofer, 1985 and Araripe- 242 Unwin, D. M.. Cearadactvlus from the Santana Formation saurus santanae Wellnhofer, 1985, were repre- taxon to date and its status has only been dis- sented by cranial remains, but in this work no cussed by Kellner & Tomida (2000). These comparisons were made with C. atrox. Addi- authors raised the possibility that the holotype tional material, including a complete skull of An- might be a composite specimen and dismissed hanguera santanae was later described by Welln- nearly all the proposed diagnostic characters of hofer (1991c), but again comparisons with other the species because they could be found in other Lower Cretaceous taxa omitted any discussion of pterosaurs, were not considered significant, or C. atrox. The same occurred in 1987, when Well- were questionable because of poor preservation. nhofer erected another new genus, ‘Tropeog- This still left two putatively diagnostic features: nathus’, containing two species, ‘T’ mesembrinus, the relatively large size of the rostrum and the based on a complete skull and lower jaw, and relatively large number of teeth (22) in the jaw ‘T’ robustus, represented by an incomplete lower anterior to the nasoantorbital fenestra. Kellner jaw, even though, apart from the sagittal crest, and Tomida (2000) also cast doubt on all three the latter is rather similar to C. atrox. Later, characters used to assign ‘C.? ligabuei’ to Ceara- Fastnacht (2001) described further material of dactylus and concluded that the two species did ‘T’ robustus, but assigned this species to Colo- not share any unique features. borhynchus, and noted that although C. atrox Ideas regarding the systematic affinities of “has a very similar heterodont dentition and lat- Cearadactylus also have a chequered history. In eral expansion of the anterior parts of the upper the initial description Leonardi & Borgomanero and lower jaw” it could be distinguished from C. (1983) tentatively assigned Cearadactylus to the robustus by the absence of a medial crest on the Ornithocheiridae, but later abandoned this idea upper and lower jaw, the different orientation of and cited the taxon as Pterodactyloidea indet. the first pair of teeth and the “festoonation” of (Leonardi & Borgomanero 1985: 75). This was the upper jaw. followed by later workers (e.g. Wellnhofer Further new Santana Formation taxa, Tupux- 1991b), until Wellnhofer (1991~)erected a sepa- uara (Kellner & Campos 1988) and Tapejara rate family, the Cearadactylidae, for this ptero- (Kellner 1989), were described in the late 1980s, saur (see also Wellnhofer 1991a). This proposal but these forms, with their edentulous jaws, were was adopted by Dalla Vecchia (1993), but not by immediately distinguishable from Cearadactylus Unwin (1992b, 2001) who assigned Cearadactylus atrox. Recently, another toothed species was to the Gnathosaurinae, which, together with the added to the register of Santana Formation pter- Ctenochasmatinae, forms the monophyletic tax- osaurs, with the description of ‘Anhanguera pis- on Ctenochasmatidae (see also Unwin et al. cator’ Kellner & Tomida, 2000, represented by 2000: 197, table 4). Kellner & Tomida (2000) re- an almost complete skeleton including a superbly jected all previous classifications, however, and preserved skull and lower jaw. In this paper the identified Cearadactylus as a member of the authors also discussed Cearadactylus atrox, and Pteranodontoidea (sensu Kellner 1996) and clo- concluded that it could be distinguished from sely related to, though not a member of, the An- other Santana taxa, but only by virtue of a single hangueridae (= Ornithocheiridae). character; the greater lateral expansion of the In summary, while Cearadactylus atrox is gen- rostra1 portion of the dentary compared to the erally accepted to be a distinct and valid species, premaxilla. Kellner & Tomida (2000) also noted few diagnostic characters have yet been identi- that, in many respects, C. atrox was similar to fied and comparisons with other taxa from the other Santana forms, especially Brasileodactylus Santana Formation and deposits of a similar age araripensis (see also Saygo & Kellner 2000). are highly variable. The validity of ‘Cearadacty- In 1993 a new pterosaur, ‘Cearadactylus? liga- lus? ligabuei’ seems rather more doubtful be- buei’, based on a fragmentary rostrum (CSRL cause the two remaining putatively diagnostic 12692/12713) from the Santana Formation, Cha- characters recognised by Kellner & Tomida pada do Araripe, Brazil, was described by Dalla (2000) are variable in other pterosaurs, and Vecchia and tentatively assigned to Cearadacty- might simply be related to the relatively large lus. In support of this decision, the author cited size of the specimen (see below). Moreover, the concave outline of the anterior part of the there is no clear evidence, at present, to support maxilla, the relatively large size of the premaxil- the assignment of this species to Cearadactylus lary teeth, the long, low shape of the skull with a (Kellner & Tomida 2000). spatulate rostrum and absence of a sagittal crest. No further material has been assigned to this Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 5 (2002) 243

Systematic review Inc 1u d e d t axa : Gnathosaurinae and Cteno- chasmatinae. Pterosauria Kaup, 1834 D i a g n o s is : Rostrum anterior to nasoantorbital Pterodactyloidea Plieninger, 1901 fenestra forms more than half the total length of the skull (tip of rostrum to occipital condyle). Ctenochasmatoidea Unwin, 1995 Anterior end of rostrum dorsoventrally com- pressed and rounded (Wellnhofer 1970, 1978). Rem a r k s : Kuhn (1967: fig. 24d) first indicated At least 25 teeth per side in the rostrum. Seven, that the “Pterodactylidae” and the Ctenochasma- or more, pairs of teeth in the premaxillae. Teeth tidae may be more closely related to each other project laterally from the dental border of the than to other pterosaurs. Unwin (1995) formally rostrum at least in the anterior part of the denti- proposed the name Ctenochasmatoidea for the tion (Wellnhofer 1970, 1978, Buisonj6 1981). clade “Pterodactylidae” + Ctenochasmatidae, Teeth in anterior part of dentition relatively noting that the “Pterodactylidae” was probably elongate with a long cylindrical crown of even paraphyletic. Apomorphies supporting the clade width and a short, tapering, distal tip (BuisonjC Ctenochasmatoidea include: quadrate oriented in 1981, Knoll 2000). Metatarsal I11 more than one an almost horizontal position; occiput faces ven- third the length of the tibia (Unwin et al. 2000: trally; and the squamosal lies level with or below fig. 6a). the orbit. Unwin & Lu (1997) gave further de- Remark s : Nopcsa (1928) proposed the subfam- tails of these characters and added a fourth char- ily Ctenochasmatinae for the reception of Cteno- acter, elongation of the cervical vertebrae, chasma and Gnathosaurus. Kuhn (1967) pro- although Cycnorhamphus, a basal ctenochasma- moted this taxon to the Ctenochasmatidae, but toid that has relatively short cervicals (Quenstedt omitted Gnathosaurus, although the latter was 1855, Plieninger 1907, Bennett 1996) shows the subsequently reassigned to this family by Well- primitive state for this character. Unwin (in nhofer (1970, 1978). Pterodaustro also clearly be- press) gives a detailed discussion of all four char- longs within this taxon (e.g. Wellnhofer 1978), acters and a formal definition of the Ctenochas- and shares a closer relationship to Ctenochasma matoidea (Cycnorhamphus suevicus, Pterodaus- than to any other pterosaur (Kellner 1997, tro guinazui, their most recent common ancestor, Chiappe et al. 2000). The Pterodaustridae is thus and all its descendants). Additionally, Unwin a junior synonym of the Ctenochasmatidae et al. (2000: fig. 6) noted two morphometric char- (Nopcsa 1928) and should be abandoned. Dong acters, the relative elongation of the third meta- (1982) assigned Huanhepterus to the Ctenochas- tarsal compared to the tibia, and the relative matidae, as has been accepted by later workers elongation of the ulna compared to the femur, (e.g. Wellnhofer 1991a, Howse & Milner 1995). that were characteristic of ctenochasmatoids, but Plataleorhynchus, a form similar to Gnatho- only members of the Ctenochasmatinae (Cteno- saurus, was referred to the Ctenochasmatidae by chasma, Pterodaustro and Eosipterus) clearly Howse & Milner (1995), and Unwin (1992b), show the derived condition. Unwin & Lii (1997) and Unwin et al. (2000) A new analysis of pterosaur phylogeny (Un- have suggested that Cearadactylus also belongs win in press), based on 20 taxa and 60 charac- within this clade. Eosipterus (Ji & Ji 1997) may ters, confirmed the monophyly of the Ctenochas- also belong within the Ctenochasmatidae (Un- matoidea, but modified the content of this taxon. win et al. 2000), a proposal that is supported by The Lonchodectidae, a poorly known group of a new, more complete specimen recently recov- Cretaceous pterodactyloids (Unwin 2001), were ered from the Yixian Formation (Lii pers. comm. found to nest within this clade, either in a tri- 2002). chotomy with Pterodactylus and the Ctenochas- Not all taxa included within the Ctenochasmati- matidae, or as a sister taxon to the Ctenochas- dae necessarily exhibit all apomorphies of the matidae. group. Huanhepterus and Cearadactylus, for ex- ample, have fewer than 25 teeth per side in the Ctenochasmatidae Nopcsa, 1928 rostrum, but exhibit other apomorphies of the clade. In addition, some taxa not included in the D e fin i ti o n : Gnathosaurus subulatus, Ptero- Ctenochasmatidae exhibit apomorphies of the daustro guinazui, their most recent common an- group. Pterodactylus kochi and l? antiquus, for cestor and all descendants of that ancestor. example, have third metatarsals that are more 244 Unwin, D. M., Cearaductylus from the Santana Formation than one third the length of the tibia and Cy- Cearadactylus atrox Leonardi & Borgomanero, cnorhamphus has a rostrum that is dorsoven- 1985 trally compressed. Notably, however, these oc- currences of the derived condition appear in H o 1o t y p e : F-PV-93, incomplete skull with taxa closely related to ctenochasmatids and mandibles partially enclosed in concretions, Leo- further strengthen support for monophyly of the nardi & Borgomanero 1983, 1985: figsl-2, Ctenochasmatoidea. Wellnhofer 1991a: 127; Kellner & Tomida 2000: figs 64-65. A plastotype is deposited in the De- partment of Paleontology, DNPM, Rio de Ja- Gnathosaurinae Unwin, 199213 neiro, Brazil. Type 1 o c a I it y : Araripe plateau, possibly from the eastern D e fini ti o n : Gnathosaurus subulatus, Huan- end (Leonardi & Borgomanero 1985), Ceari, Brazil. hepterus quingyangensis, their most recent com- mon ancestor and all descendants of that ances- Hor i z o n : Santana Formation, Araripe Group, tor. Lower Cretaceous, Albian. Berthou et al. (1990) and Pons et al. (1990) have dated the Crato For- I n c 1u d e d t ax a : Gnathosaurus, Plataleor- mation as Upper Aptian to Lower Albian which hynchus, Huanhepterus, Cearadactylus. means that the overlying Santana Formation is D i a g n o s i s : Rostrum with rounded, dorsoven- at least Middle to Upper Albian, or possibly trally compressed, laterally expanded spatulate, even younger (Martill & Wilby 1993). anterior expansion. R e f e r r e d m a t e r i a 1 : Two associated cervical Rem a r k s : Gnathosaurines are distinguished vertebrae (GIUA M 4895; Buisonj6 1980: fig. 5, from other ctenochasmatoids by the transverse plate 2) also from the Santana Formation, Brazil, expansion of the anterior tip of the rostrum and are tentatively assigned to this species. the mandibular symphysis into a rounded spatula Diagnosis: As for the genus. from which teeth project to form a distinct ro- sette that probably functioned as a grab for trap- ping or catching prey. All other ctenochasma- Description toids, with the possible exception of Ctenochasma porocristata which has a slightly ex- Published information and additional illustra- panded jaw tip (Buisonj6 1981), have jaw tips tions kindly supplied by G. Leonardi show that that are not transversely expanded anteriorly the holotype (Fig. 1A-D) consists of a rostrum and taper to a rounded termination. Anteriorly with parts of the cheek region (jugal, quadratoju- expanded jaws also occur in, and are diagnostic gal and quadrate) and an associated, complete of, the Ornithocheiridae (see Unwin 2001). How- lower jaw. The specimen is three dimensional, ever, the condition in ornithocheirids differs but has not been completely prepared from the from that in gnathosaurines in that the anterior matrix. The left side appears to be almost fully expansion usually contains only a few pairs of articulated, but on the right side the cheek re- teeth, is abruptly terminated anteriorly, with a gion has been displaced somewhat ventral to the relatively flat anterior face and, unlike the dorso- rostrum. The cortical bone is often in poor con- ventrally compressed condition evident in dition (e.g. Kellner & Tomida 2000: fig. 65) and gnathosaurines, the spatula is at least as deep bone sutures are difficult to trace. The tips of (dorsoventrally) as it is wide (transversely). some of the teeth have been restored (Kellner & Tomida 2000: fig. 64), especially in the anterior part of the dentition on the left side. Cearadactylus Leonardi & Borgomanero, 1985 The preserved part of the skull is 536 mm long and the mandible is 482mm in length. Wellnho- D i a g n o s is : Expanded, spatulate anterior end fer (1991b) calculated that the original length of of mandibular symphysis considerably wider the skull was approximately 570mm. In other than corresponding expansion of the rostrum ctenochasmatids represented by complete skulls (see also Kellner & Tomida 2000); basal dia- (Ctenochasma gracile, Gnathosaurus subulatus, meter of third rostra1 tooth more than three Pterodaustro guinazui) the portion of the skull times the basal diameter of the fifth tooth. corresponding to that preserved in Cearadactylus I n c 1u d e d s p e c i e s : Cearadactylus atrox Leo- atrox occupies 89-93% of total skull length. An nardi & Borgomanero, 1985. average of 91% yields a complete skull length Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 5 (2002) 245

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Fig. 1. Cearadactylus atrox (F- PV-93) from the Romualdo Member, Santana Formation, 12 11 10 9 8 654 3 21 of Brazil. Cranium and mand- ible in (A) left lateral and (B) right lateral view. Sketch of the anterior ends of the jaws in (C) left lateral and (D) slightly oblique dorsolateral 12 34567 9 view. Incomplete or broken f: edges indicated by a dotted ,...) ,/ line, restored margins by a :,:' :,:' dashed line. Abbreviations: d, dentary; g, groove; hc, high cheek; j, jugal; m, maxilla; naot nasoantorbital fenestra; d 56 pm, premaxilla; pop, postorbi-

123 456 7 tal process of jugal; st, step; 1-15, tooth positions. Scale C - D - bar = 50 mm. for C. atrox of 589mm. Other pterosaurs with directed caudally and only slightly dorsally, the skulls of a similar size, for example, Colobor- caudal extrapolation continuing at a somewhat hynchus robustus (Kellner & Tomida 2000), have shallower angle than shown in previous recon- wingspans of 4-5 m, and although this is slightly structions of the skull (Leonardi & Borgomanero larger than the 3-4m suggested by Leonardi & 1985: fig. 2c, Wellnhofer 1987: fig. 1, Dalla Vec- Borgomanero (1985) a wingspan in this size chia 1993: fig. 7, Kellner & Tomida 2000: range is also likely for C. atrox. fig. 70a). This suggests that the cranium was somewhat lower than in these reconstructions, a Cranium: The rostrum is remarkably long and supposition that is supported by other features, low. In lateral view (Fig. lA, B) the dorsal profile discussed below. of the anterior portion (equivalent to the first se- The anterior part of the rostrum has a spatu- ven dental alveoli) is slightly convex, while caudal late outline in dorsal aspect (Fig. 1D). The spatu- to this region the profile is gently concave. An la has a narrow oval shape, is widest at a point unusual feature is the development of a groove, level with the fourth pair of dental alveoli then between the left and right premaxillae on the dor- gradually narrows caudally, the greatest constric- sal surface (Kellner & Tomida 2000: fig. 64b; tion of the rostrum occurring at a point between Fig. lD), that extends from the anterior tip of the the seventh and eighth pair of alveoli. Anterior jaw to a point above the anterior end of the na- to its widest point the spatula gently narrows, soantorbital fenestra (Leonardi & Borgomanero then is truncated, with a rather flat anterior pro- 1985). The significance of this structure is unclear, file. A notable feature of the spatula, typical of although one possibility is that in life it accomo- gnathosaurines, is its marked dorsoventral com- dated the base of an unossified sagittal crest. pression, such that its transverse width is consid- Seen from the left or right side, the bar that erably greater than its depth. Posterior to the forms the dorsal boundary of the nasoantorbital spatula the rostrum shows a pronounced in- fenestra, composed of the fused premaxillae, is crease in depth (Fig. lA, B). This marked "step", 246 Unwin, D. M., Cearadactylus from the Santana Formation evident on both left and right sides of the speci- skull (Fig. 2A). Consequently, the orbit had a men and which appears to represent the relatively much flatter and longer (antero-posterior) basal abrupt anterior termination of the maxilla, is an margin, than the constricted outline shown in re- unusual feature in pterosaurs and only clearly constructions so far (Fig. 2B-D). It also indi- seen in one other form, Huanhepterus quingyan- cates that the lower temporal fenestra extended gensis (Dong 1982: fig. 1). Usually, in pterosaurs, forward beneath the orbit, rather than being lar- the ventral margin of the skull follows a smooth gely confined to a position behind this opening. continuous course with no steps, or notches An unusual feature of the jugal is the degree (Wellnhofer 1978: figs 2, 4-5). One consequence to which the angle between the lacrimal and of the condition in C. atrox, which is mirrored in postorbital processes has been infilled with bone. the lower jaw, is the development of a prominent Many pterodactyloids, including most ctenochas- divergence between the anterior tips of the jaws, matoids, show the primitive condition with little such that even at full occlusion there was a large or no infilling - termed here the “low cheek”. gap between the anterior ends of the rostrum and Several taxa (Dsungaripterus, derived ornitho- the mandibular symphysis. Presumably, the pri- cheiroids, Cearadactylus) exhibit the “high mary role of this opening was to accommodate cheek” condition, wherein the angle between the the first four pairs of teeth, which are highly en- postorbital and lacrimal processes is filled by a larged and fang-like (Fig. 2A). thin sheet of bone, raising the ventral border of The nasoantorbital fenestra appears to have the orbit above the ventral margin of the na- had a triangular outline, as is typical for derived soantorbital fenestra, and markedly increasing pterosaurs but, with the exception of Ornitho- the depth of the “body” of the jugal. This devel- cheirus mesembrinus (Wellnhofer 1987: fig. 2a), it opment, probably related to mechanical strength- is more elongate than in any other pterodacty- ening of the skull to withstand relatively heavy loid. A notable feature is the right-angled inter- or sudden loading of the jaws, would appear to nal posteroventral corner formed by the lacrimal be homoplastic within pterodactyloids because it and maxillary processes of the jugal. Unlike the occurs in at least three unrelated groups each of condition in the Ornithocheiroidea, as shown, for which has sister taxa (Germanodactylus, Istiodac- example, by Anhanguera (Wellnhofer 1985: tylus and Gnathosaurus) exhibiting the primitive figs 3, 32) and Pteranodon (Bennett 2001: figs 7, “low cheeked’ condition. Furthermore, the argu- 11-12), there is no rounded, bony infilling of ment for homoplasy is strengthened by the dif- this angle. ferent pattern of development in Dsungaripterus, As is typical for pterodactyloids the jugal has where the infilling begins through the ossifica- four processes. The maxillary process extends tion of a bony bar isolating a distinct lower forwards to unite with the jugal process of the opening that is gradually infilled (Young 1973: maxilla in an extraordinarily long and slender figs 1-3). By contrast, in ornithocheiroids, and bar of bone that bounds the ventral border of presumably in Cearadactylus, a single lamina is the nasoantorbital fenestra. The lacrimal process developed in the same position. is directed vertically, but its contact with the la- The slender rod of bone forming the ventral crimal is not preserved. Only the base of the margin of the lower temporal opening is com- postorbital process of the left jugal is preserved, posed of the quadrate, the quadrate process of but a longer, slightly tapering portion is present the jugal and possibly a small contribution from in the right jugal. Published drawings (Leonardi the quadratojugal (Leonardi & Borgomanero & Borgomanero 1985: fig. 2a) and reconstruc- 1985: fig. 2a), although bone contacts are difficult tions (Leonardi & Borgomanero 1985: fig. 2c, to distinguish (Kellner & Tomida 2000). As Leo- Wellnhofer 1987: fig. 1, Dalla Vecchia 1993: nardi & Borgomanero (1985: fig. 2a) and Kellner fig. 7, Kellner & Tomida 2000: fig. 70a) of the & Tomida (2000: fig. 70) show, the quadrate and postorbital process show it standing in a subver- associated bones lie at a remarkably shallow an- tical position, but it is clear from the preserved gle (20”) to the ventral margin of the skull, part of the right cheek region (e.g. Leonardi & whereas in other reconstructions (Wellnhofer Borgomanero 1985: fig. lc) that this process only 1987, Dalla Vecchia 1993; Fig. 2C) this structure diverged at a low angle from the quadrate is oriented more steeply than is evident in the (Fig. 1A). Combining evidence from the right original material. The remarkably low angle of and left sides of the skull thus shows that the the quadrate is an important character of cteno- postorbital process was directed at an angle of chasmatoids (although it appears homoplastically approximately 45” to the ventral margin of the in other pterodactyloids including Zhejiangop- Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 5 (2002) 241 terus and Quetzalcoatlus) and is directly related An unusual feature of the mandibles is that to the relatively low cranium in this clade (Un- they appear, in lateral view, to achieve their win & Lu 1997, Unwin in press). maximum height toward the caudal end of the Another derived character of the suspensor- symphysis, and are somewhat lower, though of ium is the ventral position of the quadrate articu- about even height, from this point to the articu- lation, well below the line of the dental margin lar region. Moreover, as Leonardi & Borgoma- of the rostrum (Fig. lA, B). The primitive condi- nero noted (1985), at this point the mandibles tion, in which the quadrate articulation lies at are distinctly deeper than the corresponding re- the same level as the ventral margin of the skull gion of the rostrum, a proportion that is differ- is evident in basal pterosaurs including dimor- ent from the typical condition in pterosaurs phodontids and campylognathoidids (Wellnhofer where the rostrum is usually the deeper of the 1978), and in some pterodactyloids such as Tu- two (e.g. Wellnhofer 1978). puxuara (IMCF 1052) where it presumably According to Leonardi & Borgomanero represents a reversal to the primitive state. Or- (1985) the angular is well developed and extends nithocheiroids, ctenochasmatoids and dsungarip- forwards to a point only a little short of the cau- teroids all show the derived state, to some dal end of the tooth row. The situation in other degree, but it is most clearly developed in cteno- pterosaurs is not always clear because individual chasmatids, for example in Gnathosaurus bones forming the mandible are often difficult to (Wellnhofer 1970) Ctenochasma (Wellnhofer distinguish, but generally in pterodactyloids the 1978), and Pterodaustro (Bonaparte 1971, San- angular is confined to the caudal end of the chez 1973, Chiappe et al. 2000). C. atrox shows a mandible and only ctenochasmatids such as similar marked ventral displacement of the quad- Gnathosaurus (Wellnhofer 1970) and Ctenochas- rate articulation, associated with a distinctive ma (Wellnhofer 1978) show a condition that is downward curvature of the ventral outline of the more similar to that in C. atrox. According to skull anteroventral to the cheek region. Kellner & Tomida (2000: 25) in the holotype of ‘Anhanguera piscator’ (= Coloborhynchus robus- Mandibles: Each mandible consists of a long, tus) an exceptionally well preserved ornitho- narrow, deep tube, united anteriorly in a short cheirid that, unusually for pterosaurs, has distinc- symphysis (Fig. 1A, B). Notably, the mandibles tive bone sutures, the angular has an elongate are almost perfectly straight, in lateral aspect, as process that extends forward at mid-height and in some ctenochasmatoids such as Pterodactylus is bounded ventrally by the dentary. If this antiquus (Wellnhofer 1970) and Ctenochasma unusual arrangement is typical of ornithocheir- gracile (Wellnhofer 1978: fig. 5), but unlike most ids then the construction of the mandible in pterosaurs wherein the mandibles tend to exhibit this clade is markedly different from that in some curvature especially toward the anterior or C. atrox. posterior end (Wellnhofer 1978: figs 2, 4-5). The symphysis occupies only 30% of the total Dentition: The dentition is not well pre- length of the lower jaw, essentially the plesio- served. More than half the teeth are missing and morphic condition for pterodactyloids. The sym- those present are rarely complete. In several physial region broadens to form a spatula, simi- cases the dental alveoli are poorly preserved and lar to that of the rostrum, also strongly difficult to distinguish and in some putative posi- compressed dorsoventrally and with the poster- tions the presence or absence of a particular al- ior constriction, approximately level with the veolus cannot be determined. Leonardi & Bor- eighth dental alveolus, aligned with the point of gomanero (1985) reported 15 or 16 pairs of teeth maximum constriction of the skull. The mandibu- in the rostrum, seven or, at most, eight in the lar spatula is much broader, however, its trans- premaxilla and eight in the maxilla, although verse width reaching almost twice that of the their figures (ibid. fig. 2a-c) show six or seven rostra1 spatula (Fig. lD), a feature that has not, pairs of teeth in the premaxilla and seven or so far, been reported in any other pterosaur eight in the maxilla. The total count described (Kellner & Tomida 2000). Posterior to the spatu- here is based on both sides of the skull. la there is a marked step in the dorsal profile of The left premaxilla clearly contains seven the mandible between the sixth and seventh den- tooth positions (Fig. lA, C), although the se- tal alveoli, corresponding exactly to the step in venth lies on the contact with the maxilla. The the rostrum and defining the posterior termina- seventh position, represented by a fragmentary tion of the divergence between the jaw tips. tooth, is evident on the anterior end of the right 248 Unwin, D. M., Cearadactylus from the Santana Formation maxilla (Fig. 1B) and what is presumed to be the six on the left side and three and four on the tenth position is also represented, on both left right side of the mandibular symphysis, together and right sides, by a fragmentary tooth. Conse- with other less complete examples, show that the quently, what appears to be the eroded remains anterior teeth where the jaw tips diverge, had of an alveolus midway between the eighth and pencil-shaped crowns of almost the same width tenth positions on the left side presumably repre- throughout and only tapering at their tips sents the ninth position. A poorly preserved al- (Fig. 2A). Moreover, they exhibit little or no veolus in the left maxilla appears to represent antero-posterior curvature, except at the tips. It the eleventh position, while positions twelve and can be also deduced, from the morphology of thirteen are clearly evident on the same side. the jaws, that the fang-like teeth had roots that Continuing on the left side, two indistinct alveoli were relatively short and less than half the with approximately the same spacing as previous length of the crown. positions follow the thirteenth alveolus, but the Teeth in the posterior half of the dentition are dental margin on the right side is too poorly pre- much shorter, with a crown height of only one to served to confirm this. In sum, the maxilla con- two times the basal diameter, and crowns that tains at least six and possibly as many as eight are triangular in outline, tapering from the base pairs of teeth, which, combined with the seven to the tip (Leonardi & Borgomanero 1985: teeth in the premaxilla yields a minimum tooth fig. la, b; Fig. 1C). Occasionally, the tips are re- count for the rostrum of 13 pairs, possibly ran- curved, otherwise the crowns are straight and ging up to a maximum of 15. the teeth stand perpendicular to the jaw. The anterior region of the mandibular sym- Patterns of variation in tooth size and spacing, physis contains six tooth positions, evident on determined primarily on the basis of the antero- both sides of the lower jaw, and represented by posterior diameter of the base of the tooth incomplete tooth crowns (Fig. 1B-C). Further- crown and the size of the gap between succes- more, the left mandible preserves positions seven sive teeth (also determinable from dental alveoli to ten, represented by remains of alveoli, some- where teeth are missing or not fully erupted) can times containing part of the tooth crown as, for provide important data for pterosaur systematics example, in position seven. On the right side (Unwin & Heinrich 1999, Fastnacht 2001) and only position 10, represented by an alveolus, is this is certainly true for Cearadactylus atrox. In clearly distinguishable. Positions 11 and 12 are the rostrum the first four teeth are relatively evident on the right side, but barely distinguish- large, with an increase in size from the first to able on the left. An alveolus at position 13 con- third, while the fourth is smaller and similar in tains the base of a tooth on the left side, but size to the first (Fig. 1C). The fifth tooth is re- beyond this the dental margin is too poorly pre- markably small, approximately only one third served to determine if further alveoli were pre- the basal diameter of the third tooth, while the sent. On the right side, position 13 is barely dis- sixth and seventh teeth are slightly larger, tinguishable, but seems to be followed by the though still small in comparison to the first four remains of a tiny alveolus, level with the anterior teeth. The remaining teeth (positions 8-15) are end of the nasoantorbital fenestra and represent- larger than the preceding three, and their seems ing position 14. In summary, there would appear to a slight increase in size to the tenth tooth, to be at least 13 and possibly 14 pairs of teeth in which, although perhaps the largest in the maxil- the lower jaw. la, is still only approximately 75% the size of the A distinctive feature of C. atrox is the develop- fourth tooth (Fig. 1A, B). Beyond the tenth ment of two different tooth morphologies. Teeth tooth there seems to be a decrease in size, the within the anterior part of the jaws are elongate fourteenth and fifteenth (if correctly identified) and fang-like (Kellner & Tomida 2000: fig. 64a; being only slightly larger than the fifth to se- Fig. lC), while those further to the rear are short venth. In terms of spacing, the first four teeth and squat. Most of the anterior teeth are incom- are closely packed and separated by less than a plete and have been restored so that they appear single crown base diameter. The remaining teeth to be gently recurved and taper from the base of are fairly evenly spaced, but the gap between the crown to its tip, a morphology that is empha- them is much larger and approximately equiva- sised in the restorations (Leonardi & Borgoma- lent to twice the crown base diameter. nero 1985: fig 2c). However, virtually complete The size and spacing of the mandibular denti- teeth in position two on the right and six on the tion complements that of the rostrum. Tooth left side of the rostrum, and positions five and numbers two, three and four are of similar size Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 5 (2002) 249 and markedly larger than the rest of the mandib- ture. In Cearadactylus atrox the remaining teeth, ular dentition (Fig. 1C) but, unlike the condition in the upper and lower jaws, were directed verti- in the rostrum, the first tooth is considerably cally, with no lateral divergence. smaller than the succeeding three and less than Restoration of the skull of Cearadac- half their basal diameter. Teeth in the fifth and tylus atrox: A new restoration of the skull of sixth positions are much reduced compared to this pterosaur, based directly on the left lateral the preceding three, although to a lesser degree aspect of the cranium and incorporating some than the equivalent teeth in the rostrum, and are features from the right side, is presented here of a similar size to the first tooth. The remaining (Fig. 2A). Although no attempt was made to re- teeth (7-14) are somewhat larger than the fifth construct the posterodorsal region of the skull it and sixth, but only reach, at most, approximately seems likely that the general morphology of this 75% the basal diameter of tooth pairs two to region corresponded to that in other ctenochas- four (Fig. lA, B). As in the rostrum, teeth in the matids such as Gnathosaurus and Ctenochasma. midpart of this section (10-11), seem to be lar- This restoration differs in some respects from ger than preceding or succeeding teeth, the cau- previous restorations by Leonardi and Borgoma- dal-most, if correctly identified, being the smal- nero (1985: fig. 2c; Fig. 2B), Wellnhofer (1987: lest tooth in the entire mandible, but exact fig. 1; Fig. 2C, refigured in Wellnhofer 1991a: details (e.g. whether the increase or decrease in 127, 1991b: 369, Martill 1993: fig. 5.2, reversed in size is steady, or stepped) cannot be determined Dalla Vecchia 1993: fig.7) and Kellner & Cam- because of poor preservation. Tooth spacing clo- pos (2000: fig. 70a; Fig. 2D). Most importantly, sely matches that in the rostrum. The first four all previous restorations show extrapolated por- teeth are closely packed, and separated by less tions of the premaxillae and the postorbital pro- than a single crown base diameter. The remain- cess of the jugal with a steeper inclination than ing teeth are fairly evenly spaced and separated is supported by the holotype. Moreover, Welln- by at least twice the crown base diameter. hofer (1987) reconstructed the quadrate in a Patterns of tooth orientation are similar in the rostrum and the mandibles. In lateral aspect the first two pairs of teeth are partly procumbent: directed downward, but also somewhat forward at an angle of 25" from the vertical. The remain- ing teeth are generally directed vertically, although several (fifth to seventh) may show a A slight anterior inclination. In the mandibles, by contrast, the first four pairs of teeth are procum- bent, the first markedly so, inclined at 30" from the vertical. The fourth tooth is only slightly pro- cumbent and the remaining teeth stand more or B .-<<-- L less vertical. A remarkable feature of the denti- tion, in both the upper and lower jaws, is that while most of the larger anterior teeth are pro- cumbent (when viewed laterally), in anterior or -- dorsal view (Fig. 1D) these teeth show only a small degree of lateral divergence. Thus, the ros- tral teeth are directed downward and only slightly outward. The mandibular teeth show a C somewhat greater degree of lateral divergence, so that their tips lie somewhat further out from the sagittal plane, but this can be partly attribu- ted to the lateral curvature of these teeth. This is strikingly different from the situation in other pterosaurs that have dental "fish grabs" such as D rhamphorhynchids (Wellnhofer 1975b: fig. 4b) and ornithocheirids (Fastnacht 2001: figs 3a, 5a) Fig. 2. Restorations of the cranium and mandible of Ceara- dactylus atrox. (A) this paper, (B) Leonardi & Borgomanero where the anterior fang-like teeth show a much (1985), (C) Wellnhofer (1987), and (D) Kellner & Tomida greater degree of lateral divergence and recurva- (2000). Scale bar = 50 mm. 250 Unwin, D. M., Cearadactylus from the Santana Formation steeper orientation than evident in the fossil. sion of the jaws, to form spatulae, occurs in These interpretations imply a relatively tall cra- gnathosaurines (Wellnhofer 1970, Dong nium, projecting well above the rostrum, with a 1982, Howse & Milner 1995) and ornitho- subvertical lower temporal opening located lar- cheirids (Unwin 2001), but in both these gely behind the orbit, and a relatively tall, nar- clades the spatulae are of similar widths. row, often pear-shaped orbital opening, with an Extreme reduction in size of the fifth rostral acute ventral angle. Wellnhofer (1987) also at- tooth compared to the third rostral tooth. tempted to reconstruct the entire cranium which, Size variation in the dentition is common in judging by the shape of the parietal region and pterosaurs (e.g. Wellnhofer 1978, 1991a), but the outline of the orbit, was based on Anhan- a sharp size difference between the third and guera santanae (Wellnhofer 1985), even though fifth pairs of teeth in the rostrum, compar- Leonardi & Borgomanero (1985) and Wellnho- able to that evident in C. atrox, is only found fer (1991~)specifically excluded any relationship in ornithocheirids (e.g. Fastnacht 2001). In between C. atrox and the Ornithocheiridae, or the latter clade, however, the basal diameter synonymous equivalents such as the Anhanguer- of the third tooth does not reach more than idae. Available evidence suggests that C. atrox 2.5 times the basal diameter of the fifth had a relatively low cranium, with a subcircular tooth (e.g. Fastnacht 2001: table 1). By con- orbit that had a relatively wide base, and an in- trast, in C. atrox the basal diameter of the clined lower temporal opening that extended be- third tooth is more than three times that of neath the orbit. the fifth. Previous restorations of the dentition Evidence is presented below to show that (Fig. 2B-D) are also inconsistent in some re- C. atrox is a member of the Ctenochasmatidae. spects with the fossil material. Leonardi & Bor- On this basis the following characters distinguish gomanero (1985: fig. 2c) appear to have omitted C. atrox from other ctenochasmatids and, the fourth rostral tooth, while teeth at positions although found in some non-ctenochasmatids, six and seven in the rostrum and five and six in must have evolved independently in C. atrox: the mandible appear to be relatively larger than they are in the fossil. Wellnhofer (1987: fig. 1; A groove extending along the dorsal contact Fig. 2C) also appears to have omitted the fourth of the premaxillae (Leonardi & Borgoma- rostral tooth, the wide spacing of the teeth ante- nero 1985). This structure has not been re- rior to this position is quite unlike that in the ported in any ctenochasmatid, although ap- fossil and the teeth in the posterior half of the parently it is present in an undescribed dentition in both the upper and lower jaws are anhanguerid (Kellner & Tomida 2000). relatively tall and narrow, de-emphasising the At the posterior end of the symphysis the morphological heterogeneity of the teeth evident mandibles are deeper than the correspond- in the holotype. Finally, in the restoration by ing region of the rostrum (Leonardi & Bor- Kellner & Tomida (2000: fig. 70) the first four gomanero 1985). In all other ctenochasma- tooth pairs in the rostrum are shown as consider- tids the rostrum is deeper than the ably smaller than pairs two to four in the mand- mandibles at this point, as is generally the ible, although they appear to be of similar size in case in pterosaurs, although in a few highly the fossil (Kellner & Tomida 2000: fig. 64). This derived taxa including Pteranodon (Bennett also means that the size difference between ros- 2001), Nyctosaurus (Miller 1972) and Dsun- tral tooth pairs five and six and the preceding garipterus (Young 1964, 1973) the reverse is three pairs is much smaller in the drawing than true. evident in the fossil. Mandibles deepest at the posterior end of the symphysis. In most pterosaurs, including all ctenochasmatids, except for C. atrox, the Is Cearadactylus atrox distinct mandibles are deepest at the articular end from other pterosaurs? and taper anteriorly (Wellnhofer 1978: figs 2, 4-5). Exceptions include Pteranodon (Ben- Two characters appear to distinguish Cearadacty- nett 2001) and Nyctosaurus (Miller 1972), lus atrox from all other pterosaurs: where the posterior end of the symphysis is (1) The anterior expansion of the mandibular much deeper than the mandibular rami. symphysis is almost twice as broad as the Jaw tips divaricate and containing seven rostral expansion (Fig. 1D). Anterior expan- pairs of rostral teeth and six pairs of mandib- Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 5 (2002) 251

ular teeth. Divaricate jaw tips are also pre- (Gnathosaurus, Plataleorhynchus, Ctenochas- sent in the gnathosaurine, Huanhepterus ma), or vertically (Huanhepterus, Pterodaus- (Dong 1982: fig. l), but in this pterosaur the tro). C. atrox is distinguished by its obliquely gap is filled with at least 21 pairs of rostral procumbent teeth, although a similar ar- and 13 pairs of mandibular teeth. A tooth- rangement is observed in several ornitho- filled gap is found in several ornithocheirids, cheiroids (e.g. Anhanguera, Coloborhynchus). but in this clade it results from a gentle di- (9) “High cheek”. The base of the orbit between vergence of the anterior ends of the upper the lacrimal and postorbital processes of the and lower jaws (e.g. Kellner & Tomida 2000: jugal is partially filled by a bony lamina. This fig. ll), so the divarication has a narrow, type of development occurs in other ptero- horizontal “v” shape, rather than the slot-like saurs, notably most ornithocheiroids (e.g. outline evident in Cearadactylus atrox and Wellnhofer 1985: figs 3, 32), and Dsungarip- Huanhepterus. terus (Young 1973), but is not present in cte- Marked dimorphodonty, with abrupt change nochasmatids, or other ctenochasmatoids. in tooth morphology in both upper and low- Leonardi & Borgomanero (1985: 75) presented er jaws. Other ctenochasmatids are homo- diagnoses for the genus and for the species (see dont, often strikingly so (e.g. Broili 1924, also Wellnhofer 1991b: 368), but as only one spe- 1936, Wellnhofer 1970, 1978, Buisonje 1981). cies was described these diagnoses can be com- The only exception is Pterodaustro, but in bined (see also Wellnhofer 1991b), yielding six- this case tooth morphology varies between teen distinct characters. Those not already the upper and lower jaws (Bonaparte 1971, mentioned above are discussed here approxi- Sanchez 1973, Chiappe et al. 2000). Dimor- mately in the order that they were presented in phodonty is not uncommon in pterosaurs the original paper: and the particular type of heterogeneity evi- dent in C. atrox, with teeth that are long and “Large pterosaurian, but not a giant one (wing fang-like anteriorly, but short and squat pos- span about 4 m in the adult)”. Size is not diag- teriorly, occurs in various groups including nostic for pterosaurs. Within a single species dimorphodontids (Owen 1870, Wild 1978), osteologically mature individuals can exhibit a campylognathoidids (Wild 1978), rhamphor- large size range (e.g. Bennett 1993). More- hynchids (Wellnhofer 1975b) and ornitho- over, individuals of various species including cheirids (Kellner & Tomida 2000). Usually, toothed forms such as Anhanguera santanae, however, there is a gradual change in tooth that are generally similar to C. atrox, have di- shape from one morphology to the other, mensions that are approximately the same as and the abrupt switch evident in C. atrox, those of C. atrox (see also Kellner & Tomida otherwise only seen in dimorphodontids and 2000: 111). Eudimorphodon, is unique among pterodac- “[Plreyer” [= predator]. Not diagnostic (Kell- tyloids. ner & Tomida 2000). Most, if not all known Short, squat, triangular teeth in the posterior pterosaurs, including ctenochasmatids, were half of the dentition. In other ctenochasma- predators (Wellnhofer 1991a). tids the teeth are thin and needle-like, even “[S]kull long and low”. Not diagnostic (Kell- at the caudal end of the dentition, although ner & Tomida 2000). Most pterodactyloids in- teeth like those of C. atrox occur widely in cluding all ctenochasmatoids, all ornithocheir- other groups of pterosaurs (Wellnhofer oids and some azhdarchoids had long low 1978). skulls (Wellnhofer 1978, 1987, 1991b, Unwin & No more than 15 pairs of teeth in the ros- Lu 1997). trum and 14 in the mandibles. The tooth “[Gleneral outline, in zenithal view, elongated count is greatly reduced in C. atrox com- birsoyd, with rostral end spatulated”. Not diag- pared to other ctenochasmatids, which have nostic. In dorsal view all gnathosaurines at least 25 pairs of teeth in the rostrum (Wellnhofer 1970, Dong 1982, Howse & Mil- (Huanhepterus),often many more. ner 1995) and some ornithocheiroids (Campos Procumbent position of the first two pairs of & Kellner 1985, Wellnhofer 1985, 1987, 1991c, teeth in the rostrum and the first three pairs Kellner & Tomida 2000, Fastnacht 2001) have in the mandibular symphysis. In ctenochas- skulls that exhibit the same general shape and matids the teeth in the anterior end of the also have spatulate anterior terminations to tooth row are directed horizontally the jaws. 252 Unwin, D. M., Cearadnctylus horn the Santana Formation

“[A]lveolar borders of the of the premaxillary do “Length of the symphysis equal to nearly one not occlude with the jaw, leaving a wide gap”. third of the mandible”. Not diagnostic (Kellner See discussion of divaricate jaw tips above. & Tomida 2000). Symphyses of similar length “Premaxillary dentition very long and, except are found in various pterodactyloids including the most anterior teeth, obliquously outward the ctenochasmatid Gnathosaurus macrurus stretched and curved”. See discussion of tooth (Howse & Milner 1995: fig. 1). orientation and dimorphodonty above. “Mandibular ramus deeper than the rostra1 por- “[M]axillary teeth spaced, short, conical, not tion of the skull”. See discussion above. very sharp and slightly stretched backward”. “Anterior end of the mandible spatulated”. Not See discussion of maxillary teeth above. diagnostic in this formulation. All other “All teeth alternate in the upper and inferior gnathosaurines and some ornithocheirids rows, so that they interfinger, while in the occlu- (Anhanguera, Coloborhynchus) also have a sion the lower ones lie external to the maxillary, mandibular symphysis with a spatulate ante- and the upper ones lie external to the man- rior termination. dible’’. Not diagnostic. This occurs in many In summary, Cearadactylus atrox can be pterosaurs including most ctenochasmatids clearly distinguished from all other pterosaurs (Wellnhofer 1978). by characters of the jaws and dentition, and “Antorbital fenestra (fused with the external from other ctenochasmatids by a further nine naris) very long, with the posterior border cranial and dental characters. forming an angle of about 90 degrees with the lower border”. The nasoantorbital fenestra ‘Cearadactylus? ligabuei’ shown in the restoration (Fig. 2A) has a slightly greater length to height ratio (1 :4.24) Dalla Vecchia (1993) proposed three characters than other ctenochasmatids such as Pterodaus- that apparently support a close relationship be- tro (1 :4.0) and Gnathosaurus (1 :3.69), but un- tween ‘Cearadactylus? ligabuei’ (Fig. 3) and certainty regarding the exact shape of the na- Cearadactylus atrox. soantorbital fenestra means that this distinction is unreliable. The shape of this fe- “alveolar margin of the anterior part of the nestra is the same as that in many pterodacty- maxilla is concave, leaving, in the occlusion loids including all ctenochasmatoids (Welln- with the lower jaw the gap cited by Leonardi hofer 1970, 1978, 1991b). and Borgomanero”. An unusual feature of “The antero-superior border of the antorbital the rostrum of ‘Cearadactylus? ligabuei’ fenestra is formed only by the premaxilla”. Ex- (CSRL 12962/12713) is a short recessed sec- clusion of the maxilla from the upper margin tion of the dental margin of the maxilla, cor- of the nasoantorbital fenestra is unusual in responding to tooth positions four to eight, pterosaurs, but seems to occur in the cteno- that in lateral view exposes the palatal sur- chasmatid Pterodaustro (Chiappe et al. 2000) face of the jaw (Dalla Vecchia 1993: fig. la, and the ctenochasmatoid Cycnorhamphus (e.g. b; Fig. 3A). Dalla Vecchia suggested that this Wellnhofer 1978). structure was homologous with the divari- “Long groove along almost the entire length of cate jaw tips evident in C. atrox, but the ar- the suture between premaxillae”. See discussion gument is not convincing. Although the max- above. illa is slightly recessed, the ventral outline of “Sagittal crest lacking, at least until the first the skull continues in a straight line from the third part of the antorbital opening”. Not diag- tip of the rostrum posteriorly, at least to a nostic. Many pterosaurs do not have a cranial point level with the nasoantorbital fenestra, sagittal crest (Wellnhofer 1978, 1991a). and there is no “step” as in C. atrox. More- “Base of the temporal region (between the over, in the latter species the divarication is quadrate and the posterior border of the antor- confined to the premaxillae and involves bital fenestra) narrow and funnel shaped’. Not tooth pairs one to seven. Furthermore, it diagnostic as formulated here, moreover the would seem from the construction of the ros- construction of this region in C. atrox is similar trum in ‘Cearadactylus? ligabuei’ that, at full to that in most non-ornithocheiroid pterodac- occlusion, there would be little or no gap be- tyloids (e.g. Wellnhofer 1978), although the tween the premaxillae and the maxillae on morphology of the jugal is distinct from that the one hand, and the mandibular symphysis of other ctenochasmatids (see above). on the other. Finally, exactly the same struc- Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 5 (2002) 253

12 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 202122 A-

B-

12 3 45 6 7 6 9 10 11

Fig. 3. ‘Cearadactylus? hgabuez’ (CSRL 12962/12713) from the Romualdo Member, Santana c- Formation, of Brazil. Cranium in (A) left lateral and (B) dorsal view. Anterior end of rostrum in ventral view (C) and left jugal in lateral view (D). Tooth with re- placement tooth (E), from posi- tion six, left side of the rostrum. Redrawn from Dalla Vecchia (1993). Abbreviations as for Fig. 1 except: in, infilling of pos- teroventral angle of nasopreorbi- tal fenestra; mr, median ridge; r, recess. Scale bar = 50mm (A, D- E- B), 10 mm (C, D), 5 mm (E).

ture, a recession of the dental margin ex- portantly, considerably smaller than any of tending from tooth pairs five to eight, occurs the first four pairs of teeth. Moreover, as in the rostrum of Coloborhynchus robustus Dalla Vecchia (1993) also noted, the premax- (Fastnacht 2001, fig. 2a, b). illa of ‘Cearadactylus? ligabuei’ contains four (2) “The premaxillary teeth are considerably lar- teeth (Fig.3A), as is typical for pterosaurs, ger than the other ones.” As Dalla Vecchia but in C. atrox it has seven tooth positions, a noted (1993) in his discussion of this charac- highly unusual character otherwise only ter, there is a marked disparity in size be- found in ctenochasmatids. tween the teeth in the anterior and posterior (3) “The skull is long and low, without a sagittal sections of the premaxilla of C. atrox, that is crest on the snout and its anterior end is spa- similar to the condition in ‘Cearadactylus? tulate.” These four characters do not unite ligabuei’. At a general level this is correct, ‘Cearadactylus? ligabuei’ and C. atrox. A but the two species differ in some important long, low skull occurs in various ctenochas- details. In ‘Cearadactylus? ligabuei’ there is a matids (Ctenochasma, Gnathosaurus, Plata- steady increase in tooth size from the first to leorhynchus) and also in many ornitho- the fourth pair, while tooth pairs five to se- cheirids (Anhanguera, Coloborhynchus, ven are of approximately the same size and Ornithocheirus). Aside from the problems slightly larger than tooth pair one (Fig. 3A, associated with ‘absence’ characters, absence C). By contrast, in C. atrox the third tooth is of a sagittal crest on the snout is common in larger than the fourth, tooth pairs five to se- pterosaurs and plesiomorphic for Pterodac- ven are more uneven in size and, more im- tyloidea. A spatulate anterior end of the ros- 254 Unwin, D. M., Cearudacfylus from the Santana Formation

trum is found in all gnathosaurines and also with C. atrox and Huanhepterus within the in some ornithocheirids (Anhanguera, Colo- Gnathosaurinae, and there are only four pairs of borhynchus). teeth in the maxillae (Fig. 3A). The teeth do not project horizontally from the dental border in This analysis thus confirms the conclusion the anterior part of the dentition which, again, reached by Kellner and Tomida (2000), that could be argued to be a character shared with none of the three characters proposed by Dalla Huanhepterus and C. atrox, except that, unlike Vecchia (1993) supports a close relationship be- the latter two taxa, in ‘Cearadactylus? ligabuei’ tween ‘Cearadactylus? ligabuei’ and C. atrox. teeth in positions two to seven are directed ven- This also seems to be the case with regard to the trolaterally rather than vertically. Furthermore, 11 characters recognised here as diagnostic for the teeth taper from the base to the tip of the C. atrox and thus potential synapomorphies of crown (Fig. 3E), rather than having a long cy- Cearadactylus. The relative size of the mandibu- lindrical crown of even width and a short taper- lar spatula is unknown in ‘Cearadactylus? liga- ing distal tip as in ctenochasmatids. In the re- buei’, but while the fifth rostral tooth is smaller storation by Dalla Vecchia (1993: fig. 7a), the than the third, it is still considerably more than posterodorsally directed posterior continuation half the basal diameter of the third tooth of the premaxillae and the steeply oriented post- (Fig. 3C), rather than less than one third, as in orbital process of the jugal (Fig. 3D) all suggest C. atrox. There is no groove extending along the that ‘Cearadactylus? ligabuei’ had a relatively dorsal margin of the rostrum in ‘Cearadactylus? high cranium, unlike the low cranium and asso- ligabuei’, and there is no distinct anterior divari- ciated characters typical of ctenochasmatoids. Fi- cation of the jaw tips or marked dental dimor- nally, the maxilla forms part of the dorsal border phodonty. Furthermore ‘Cearadactylus? ligabuei’ of the nasoantorbital fenestra, unlike the condi- has 22 pairs of teeth located between the tip of tion in Cearadactylus atrox and some other cte- the rostrum and the anterior termination of the nochasmatoids (see above) where it is entirely nasoantorbital fenestra, compared to just 13-15 excluded from the dorsal border. pairs in C. atrox. Procumbent teeth are present Comparisons of ‘Cearadactylus? ligabuei’ with in ‘Cearadactylus? ligabuei’, but this appears to other pterosaurs, reveal a number of derived affect at least tooth pairs one to six (Fig. 3A), characters shared with ornithocheirids. The ex- rather than just the first two pairs as in C. atrox. panded anterior end of the rostrum is remark- More significantly, the teeth of ‘Cearadactylus? ably similar to that of Anhanguera blittersdorffi ligabuei’ show a marked lateral divergence af- (Campos & Kellner 1985: fig. 1) including the fecting at least the first six pairs of teeth gradual narrowing of the rostrum posteriorly to (Fig. 3B), which is quite unlike the subvertical a point between the tenth and eleventh tooth arrangement of the dentition in C. atrox. One positions, unlike Cearadactylus atrox where the character that these species do share in common rostrum is narrowest between tooth positions se- is the development of a high cheek (cf. Figs lA, ven and eight. Moreover, the patterns of size, 3D), but this feature also occurs in other ptero- spacing and orientation of the teeth in ‘Ceara- saurs including most ornithocheiroids and some dactylus? ligabuei’ closely match those of Anhan- dsungaripterids. guera blittersdorffi (Campos & Kellner 1985: ‘Cearadactylus? ligabuei’ also exhibits the pri- fig. l), Anhanguera santanae (Wellnhofer 1991c: mitive state for all synapomorphies of the fig. 2) and Coloborhynchus robustus (Kellner & Gnathosaurinae or the Ctenochasmatidae, cast- Tomida 2000: figs4, 5, Fastnacht 2001: figs2, 3), ing further doubt on the likelihood of any close and also correspond to one of the derived char- relationship with C. atrox. Thus, although ‘Cear- acter states supporting the Ornithocheiridae adactylus? ligabuei’ has a rostral spatula, it is not (Unwin 2001). In addition, ‘Cearadactylus? Ziga- dorsoventrally compressed as in gnathosaurines, buei’ also exhibits a rounded bony infilling of the but is almost as deep as it is wide, as in ornitho- angle between the lacrimal and maxillary pro- cheirids. Unlike ctenochasmatids, the rostrum cesses of the jugal (Fig. 3D), and a relatively nar- anterior to the nasoantorbital fenestra forms less row, deep ventral margin of the orbit (Dalla than half the total reconstructed length of the Vecchia 1993: fig.7). Both of these features are skull, and its anterior end is not dorsoventrally typical of ornithocheirids, although not abso- compressed and rounded. There are fewer than lutely confined to this clade. The palatal surface 25 teeth per side in the rostrum, although this of the rostrum of ‘Cearadactylus? ligabuei’ bears could be argued to be a derived character shared a broad, deep median ridge lateral to which the Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 5 (2002) 255 palate is transversely concave (Dalla Vecchia The relationships of Cearadactylus atrox 1993: fig. 2), similar to the condition in ornitho- to other pterosaurs cheirids (Wellnhofer 1985, 1991c), but unlike that in ctenochasmatids, where the median ridge Methods and materials: A two stage phy- is small and sharp and bordered by wide flat pa- logenetic analysis was carried out to establish the latal shelves (Howse & Milner 1995). In many relationships of Cearadactylus atrox to other other respects, including tooth morphology, the pterosaurs. In the first stage, C. atrox was added shape of the nasoantorbital fenestra and a pro- to a data set of 20 taxa, including all main clades minent groove originating from the anterior of pterosaurs, and 67 characters, nearly all binary apex of the nasoantorbital fenestra, ‘Cearadacty- and evenly split between cranial and postcranial lus? ligabuei’ compares closely with Anhanguera morphology (Unwin in press). In the original santanae (Wellnhofer 1985, 1991c) and other or- analysis (Unwin in press) the Ctenochasmatidae nithocheirids, although these characters also oc- was treated as a terminal taxon, consequently, in cur in other pterodactyloids. The absence of a this study, apomorphies of this clade (listed in sagittal crest on the rostrum does not exclude the diagnosis, above) were incorporated into the ‘Cearadactylus? ligabuei’ from the Ornithocheiri- main data set in order to test the hypothesis dae, because this putatively secondary sexual (Unwin 1992, 2001, Unwin et al. 2000) that Cear- character is highly variable and lacking in some adactylus is more closely related to the Cteno- taxa that clearly belong within this clade inclu- chasmatidae than to any other taxon. ding Brasileodactylus araripensis (Kellner 1984), The data matrix (see Unwin, in press) was Coloborhynchus sedgwicki (Unwin 2001) and a analysed using PAUP 3.1. 1 (Swofford, 1993), new ornithocheirid from the Crato Formation of with the branch and bound search option, and Brazil (Frey & Martill in press). addition sequence ‘furthest’. Runs were executed In conclusion, ‘Cearadactylus? ligabuei’ does using both ACCTRAN and DELTRAN settings. not share any unique characters in common with Multiple state characters were always treated as Cearadactylus atrox and there are no grounds for unordered. Three different outgroups were used: retaining this species within Cearadactylus. There basal ornithodirans, basal archosaurs and prola- is some weak evidence in favour of a relation- certiforms. Pterosaur skeletal anatomy is so de- ship with gnathosaurines, but this is strongly con- rived, however, that selection of any particular tradicted by the absence of key apomorphies of group had no effect on character polarity be- the Gnathosaurinae and the Ctenochasmatidae. cause, in almost all cases, the plesiomorphic con- By contrast, ‘Cearadactylus? ligabuei’ exhibits a dition is the same in each group. The analysis key apomorphy of the Ornithocheiridae and generated six trees, differing only in the position shows many similarities to crania currently as- of Pterodactylus and Lonchodectes with respect signed to various species of Anhanguera. For the to the Ctenochasmatidae + Cearadactylus, and present, this species is tentatively assigned to An- the relationship of the Dsungaripteroidea to the hanguera as Anhanguera? ligabuei, with the pro- Ctenochasmatoidea or the Azhdarchoidea. One viso that the taxonomic validity and relationships of the six trees, which has the same topology as of this pterosaur require further study. the strict consensus tree, is shown in Fig. 4A to-

Table 1 List of characters used in the analysis of species relationships within the Ctenochasmatidae.

Cranium 1. Rostrum anterior to nasoantorbital fenestra: less than [O], or greater than [l]half total length of the skull. 2. Anterior end of rostrum dorsoventrally compressed: absent [O], present [l]. 3. Anterior tips of jaws divaricate: absent [O], present [l]. 4. Anterior end of rostrum and mandibular symphysis with expanded, spatulate profile: absent [O], present [l]. 5. Symphysis less than [O], or greater than [l]half the total length of the lower jaw.

Dentition 6. Less [O], or more [l]than 24 pairs of teeth in the rostrum. 7. Teeth in anterior part of dentition taper from base of crown to tip [O], or are relatively elongate with a long cylindrical crown of even width and a short tapering distal tip [l]. 8. Teeth in anterior half of dentition project vertically from dental margin [O], or horizontally [l]. 9. Premaxilla has less [O], or seven or more [1] pairs of teeth. 10. Less [O], or more [l] than 50 pairs of teeth in the rostrum. 11. Teeth restricted to anterior half of mandible: absent [O], present [l]. 256 Unwin, D. M., Cearadactylus from the Santana Formation

Outgroup outgroup taxon (Rhamphorhynchus). The data Preondactylus matrix (Table 2) is 98% complete (only two Dirnorphcdontidae missing entries) and all characters are binary. Anurognathidae Carnpylqnathoididae The data matrix was analysed in exactly the Scaphognathinae same way as for the first stage and resulted in a Rharnphorhynchinae single most parsimonious tree (Fig. 4B). lstiodactylus IOrnithocheiridae 1 Results and discussion: The results of the Pteranodontidae first analysis confirm that Cearaductylus is a pter- A Nyctosaurus m odactyloid (presence of a nasoantorbital fenes- Cycnorhamphus tra) and support a relationship within the Cteno- Pterodactylus chasmatoidea (quadrate oriented in a Lonchodectidae ] subhorizontal position). Both analyses indicate Ctenochasmatidae Cearadactylus strong support for the assignment of Cearudacty- Germanodactylus lus to the Ctenochasmatidae (Cearadactylus exhi- Dsungaripteridae bits the derived state for characters 1, 2, 7 and 9, 7Tapeiara.. see Table 2). Within the Ctenochasmatidae Ceur- Steps: 139 Tupuxuara CI: 0.70 HI: 0.44 aductylus shares one unambiguous synapomor- 0.81 RCI: 0.57 ?@- Azhdarchidae RI: phy with gnathosaurines (rostrum with rounded, dorsoventrally compressed, spatulate, anterior a, Rhamphorhynchus .z expansion), but no characters in common with + Pterodactylus 2 ctenochasmatines. Leonardi & Borgomanero B Cycnorhamphus 5 (1985) doubted that Cearadactylus shared a close relationship with Gnathosaurus and Huanhep- Pterdaustro terus because it lacked a sagittal crest on the ros- trum. This structure is highly variable in its dis- Gnathosaurus Steps: 14 CI: 0.79 HI: 0.21 tribution in pterosaurs, even within a single RI: 0.85 RCI: 0.67 species (e.g. Germanodactylus rhumphastinus), 6 and so its phylogenetic significance is uncertain. It should also be noted that other ctenochasma- Fig. 4. Cladograms showing (A) phylogenetic relationships of Cearadactylus to other maior clades of pterosaurs and (B) to Ctenochasma gracile and Ptero- other species of the Ctenochasmatidae. Bootstrap values daustro guinazui also lack bony sagittal crests. shown at nodes. Abbreviations: CI, consistency index; HI, Huanhepterus and cearadactylus form a sub- homoplasy index; RCI, Rescaled consistency index; RI, Re- tention index. clade within the Gnathosaurinae, united by one unambiguous synapomorphy ( anterior tips of gether with bootstrap values (1000 replicates) jaws divaricate (see also Leonardi & Borgoma- and other statistical data. nero 1985)), one ambiguous synapomorphy The second stage of the analysis focused on a (teeth restricted to anterior half of mandible) data set consisting of 11 characters, five concern- which also appears in Cycnorhamphus, and one ing the cranium and six describing the dentition character reversal (teeth vertically oriented). (Table l), and nine terminal taxa (Table 2): six An alternative possibility is that Cearuductylus ctenochasmatids, two ctenochasmatoids and an shares a close relationship with the Ornithocheir-

Table 2 Distribution of character states (0, 1) among the terminal taxa used in the analysis of species relationships within the Cteno- chasmatidae. Uncertainty because of incomplete preservation is indicated by '?'.

123 4 5 6 7 8 9 10 11

Rhamphorhynchus muensteri 00000000000 Cycnorhamphus suevicus 01000000001 Pterodactylus kochi 00000000000 Gnathosaurus subulatus 11010111100 Plataleorhynchus streptophorodon ?101?111100 Huanhepterus quingyangenszs 11110110101 Cearadactylus atrox 11110010101 Ctenochasma gracile 11001111110 Pterodaustro guinazui 11001110110 Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 5 (2002) 251 idae (Kellner & Tomida 2000), or may even be- cheirids where the roots are long and often of long within this family. In this analysis Cearadac- similar length to the crown (e.g. Fastnacht 2001: tylus was found to share one putative synapo- fig. 4). morphy with the Ornithocheiroidea (“high If Cearadactylus is an ornithocheirid, all the cheek’) and two with the Ornithocheiridae (ex- synapomorphies that it shares with Huanhep- panded anterior end of the rostrum, relatively terus, gnathosaurines and ctenochasmatids, must large size of the first three pairs of teeth in the have evolved independently in this pterosaur be- rostrum). The development of a high cheek is cause Istiodactylus, which is basal to ornitho- not confined to ornithocheiroids (also present in cheirids, within the Ornithocheiroidea (Unwin Dsungaripterus), so this is not an unambiguous 1995, in press, Unwin & Lii 1997, Unwin et al. synapomorphy. Comparisons between ornitho- 2000), does not have these synapomorphies. For cheirids such as Anhanguera (Campos & Kellner the same reason, characters such as the absence 1985, Wellnhofer 1991c) and Coloborhynchus of a concave posterior margin of the nasoantor- (Kellner & Tomida 2000, Fastnacht 2001) with bital fenestra, absence of a distinct vascular Cearadactylus show that the rostral and mandib- groove extending forward from the anterior tip ular spatulae of the latter are quite different in of the nasoantorbital fenestra, and the presence shape from those of the former. They have an of “straight” mandibles, all present in Cearadac- oval outline, are widest in the mid part of the tylus, but representing the plesiomorphic condi- spatula, terminate just caudal to the seventh tion within the Ornithocheiroidea, must be char- tooth position in the rostrum and are strongly acter reversals in Cearadactylus, because all dorsoventrally compressed. By contrast, the spa- other ornithocheiroids exhibit the derived condi- tulae in ornithocheirids are highly asymmetrical tion. Thus, within the context of the phylogenetic anteroposteriorly (e.g. Fastnacht 2001: figs 2b, analyses conducted here, only five additional 3c), widest at or near the anterior tip of the jaw character state changes are needed to accommo- and taper to a point between the ninth and tenth date Cearadactylus within the Gnathosaurinae, tooth positions. In addition, they are usually as compared to 14 changes if it is an ornithocheirid. deep, measured in the sagittal plane, as they are At present, therefore, character state distribu- wide, in order to accommodate the long roots of tions strongly support the inclusion of Cearadac- the anterior fang-like teeth. tylus within the Gnathosaurinae, as a sister taxon Variation in tooth size along the jaw in or- to Huanhepterus. nithocheirids is clearly similar to that of Ceara- dactylus, but, in the latter, the fifth to seventh rostral teeth are far smaller than the third tooth, Cearadactylus and its possible association and of similar size to one another. In ornitho- with other pterosaur material cheirids (e.g. Fastnacht 2001), the fifth tooth is from the Santana Formation approximately half the diameter of the third, but beyond this position there is a steady increase in Considering the diagnostic features of Cearaduc- tooth size up to the ninth or tenth tooth. More- tylus atrox listed above it would seem that none over, in the lower jaw of ornithocheirids there is of the other pterosaur specimens so far de- a steady increase in tooth size from the first to scribed from the Santana Formation, that include the third position, the fourth tooth is smaller a rostrum or mandibles (Kellner, 1984, 1989, than the first and about two thirds the size of Campos & Kellner 1985, 1997, Wellnhofer 1985, the third, after which there is a steady increase 1987, 1991b, c, Kellner & Campos 1988, 1994, in size from the fifth to the ninth tooth (Kellner Kellner & Tomida 2000) can be assigned to & Tomida 2000). This is distinct from Cearadac- Cearadactylus. This still leaves a number of spe- tylus where pairs two to four are of similar size cimens that are not directly comparable with and much larger than the first pair, the fifth pair C. atrox because they lack the cranium and low- is much less than half the diameter of the third er jaws. If it is accepted that Cearadactylus is a pair and the remaining eight pairs are of similar ctenochasmatid then many of these remaining size. In addition, the anterior teeth of Cearadac- specimens (Price 1971, Wellnhofer 1977, 1985, tylus have relatively short roots compared to 1991b, c, Leonardi & Borgomanero ‘1987, Well- crown length, as in ctenochasmatids (e.g. nhofer et al. 1983, Dalla Vecchia & Ligabue Gnathosaurus macrurus Howse & Milner 1995, 1993) can be excluded from consideration be- Ctenochasma porocristata BuisonjC 1981: figs lb, cause features such as the twisted deltopectoral 2a) and a different shape from that of ornitho- crest of the humerus (Padian 1984, 1986, Ben- 258 Unwin, D. M., Cearadactylus from the Santana Formation nett 1989), diameter of the shaft of the radius specimen may prove, however, to be a tapejarid, less than half that of the ulna (Kellner & Tomida but in any case the cervicals described by Bui- 2000), details of the wrist bones (Unwin 1995, in sonjC (1980) are proportionately shorter than press) and the morphology of the proximal end those of true azhdarchids (width to length ratio of the wing-phalanx 1 (Unwin unpub. data), of >8), have a distinct neural arch and centrum, show that they are ornithocheiroids. Interest- unlike the condition in azhdarchids where these ingly, this includes the holotype and only known structures are merged into a single tube (Nesov specimens of Araripesaurus castilhoi (DGM 1984, Padian 1984, Howse 1986), pneumatic for- 529R) and Araripedactylus dehmi (BSP 1975 I mina located on the lateral sides of the vertebral 166) thus Cearadactylus atrox is not a junior sy- centrum and a low, but well developed neural nonym of either of these species. crest, contrasting with the absence of these struc- Four of the five remaining specimens only tures in azhdarchids (Nesov 1984, Howse 1986). known from postcrania (Campos et al. 1984, Cearadactylus is the only ctenochasmatoid Wellnhofer 1985 [BSP 1980 I 121, BSP 1982 I known from the Santana Formation and it can 931, Kellner 1995 [DNPM CD-R-019]), might be- be inferred from the presence of elongate cervi- long to C. atrox, but there is no positive evi- cal vertebrate in all other ctenochasmatids where dence to support this referral because they all the neck is preserved: Ctenochasma (Broili 1924, exhibit characters typical of most non-ornitho- 1936, Wellnhofer 1970); Pterodaustro (Bonaparte cheiroid pterodactyloids and it is equally possible 1970, Wellnhofer 1991a); and Huanhepterus that they belong to Tapejara (as Kellner has pro- posed for DNPM CD-R-019), or Tupuxuara, the two non-ornithocheiroid taxa described so far from the Santana Formation. There is, ,however, some indirect evidence to support the idea that the fifth specimen, two as- sociated cervical vertebrae (BuisonjC 1980), could be referred to Cearadactylus. The verteb- A rae (UMGI M4895, Fig. 5), probably the third and fourth cervicals, possibly the fourth and fifth, were described by Buisonjk (1980) under the name of ‘Santanadactylus bradensis’, but were not found in association with the holotype of this species, an incomplete scapulocoracoid I and proximal end of the humerus (BuisonjC Pf 1980: figs 2-4), representing an indeterminate B ornithocheiroid, and are presently treated as Pterodactyloidea indet. (Kellner & Tomida 2000). Low, elongate cervical vertebrae occur in two distinct pterodactyloid clades: ctenochasma- toids and azhdarchoids (Kellner 1995b, Unwin 1995, in press, Unwin & Lu 1997). In the Santa- na Formation, azhdarchoids are represented by Tupuxuara, which has short, relatively blocky cervical vertebrae (e.g. IMCF 1052) and Tape- C jara, a relatively small pterosaur that has low, elongate vertebrae (Wellnhofer & Kellner 1991), approximately twice as long as their minimum width, although they are proportionally shorter than those described by BuisonjC (1980) which D E have a length to minimum width ratio of 1:2.84. Fig. 5. Cervical vertebrae (GIUA M 4895) in (A) dorsal, (B) A putative azhdarchid has been reported from right lateral, (C) ventral, (D) anterior and (E) posterior the Crato Formation (Martill & Frey 1999), views, from the Romualdo Member of the Santana Forma- which, if confirmed, would indicate that this tion, Brazil, originally described by BuisonjC (1980) under the name ‘Santanadactylus brasilensis’, and tentatively as- clade probably existed in South America during signed here to Cearadacrylus. Redrawn from Buisonje (1980). the deposition of the Santana Formation. This Abbreviations: pf, pneumatic foramen. Scale bar = 50 111111. Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 5 (2002) 259

(Dong 1982) that it too probably had elongate probably a small to medium-sized pterosaur, and cervicals. The cervicals described by BuisonjC rather similar in morphology to Pterodactylus, (1980) have a maximum width across the zyga- although with a larger tooth count. Subsequent pophyses of just over 50mm, which in compari- evolution within the two subclades appears to son with pterosaurs known from more complete have proceeded in different directions. In the remains and with vertebrae of similar dimen- Ctenochasmatinae, the jaws became even more sions, indicates a wingspan in the region of 4m. elongate and acquired a distinctive curvature, This corresponds reasonably well with the likely while the teeth became finer, more numerous size of the individual represented by the holo- and shifted to a vertical orientation within the type of C. atrox. Because it is the only pterosaur jaw. Unlike many other clades of pterodacty- known from the Santana Formation that is likely loids, ctenochasmatines appear to have remained to have had cervicals similar to those of UMGI of a relatively modest size throughout their his- M4895, and is also represented by an individual tory: Pterodaustro and the similarly sized Eosip- of corresponding size, these cervicals are tenta- term are only slightly larger than Ctenochasma. tively assigned to Cearadactylus. Only more com- In the Gnathosaurinae, by contrast, the tooth plete specimens will enable this problem to be count was reduced, Huanhepterus an early Low- resolved further. er Cretaceous form (Dong 1984) has only 25 pairs compared to 30-32 pairs in the Late Juras- sic forms Gnathosaurus (Wellnhofer 1970) and Cearadactylus and the evolutionary history Plataleorhynchus (Howse & Milner 1995), while of ctenochasmatid pterosaurs Cearadactylus has, at most, 15 pairs in the ros- trum. In addition, the teeth were relatively lar- An outline of the temporal history and palaeo- ger than those of basal gnathosaurines, more biogeography of the Ctenochasmatidae (Fig. 6) widely spaced and, in Cearadactylus, variable in was reconstructed by combining data on the stra- morphology. Moreover, in the Gnathosaurinae, tigraphic and geographic distribution of cteno- later forms such as Huanhepterus are larger than chasmatid pterosaurs (Wellnhofer 1991a, Unwin the earliest known taxa and the stratigraphically et al. 2000) with the phylogenies presented in youngest form, Cearadactylus, is even larger than Fig. 4. To set this history within a general con- Huanhepterus. text, the temporal ranges of the other main The trends noted above may reflect ecological clades of pterodactyloid pterosaurs, based on a changes related to diet. Ctenochasmatines ap- detailed analysis of pterosaur phylogeny (Unwin pear to have become increasingly specialised for in press) are also shown. filter feeding (Wellnhofer 1978, 1991a), whereas It seems likely that the Ctenochasmatidae ori- in gnathosaurines, although basal forms seem to ginated before the Tithonian, since representa- have been sieve feeders (Wellnhofer 1970, tives of both main clades, the Ctenochasmatinae Howse & Milner 1995) preying on invertebrates, and the Gnathosaurinae are known from the there seems to have been a shift toward larger Solnhofen Limestone of Bavaria (Wellnhofer prey items leading ultimately, in the case of 1970). Both clades persisted throughout the Cearadactylus, to a change to fish-catching Lower Cretaceous, but neither is known from (Leonardi & Borgomanero 1985, Wellnhofer the Upper Cretaceous (Fig. 6A). Pterodaustro, 1991a: 127). These changes in diet might also be the last record for the Ctenochasmatinae, is Al- related to the phyletic size increase evident in bian, as is Cearadactylus, the last record for the gnathosaurines. Gnathosaurinae. So far, Jurassic ctenochasmatids Cearadactylus thus represents a striking exam- have only been reported from Europe (Fig. 6B), ple of morphological convergence, with many but in the Cretaceous this group achieved a near features related to fish-catching that also appear global distribution (Fig. 6C), and both main sub- in ornithocheirids, but not in other ctenochasma- clades were also widely distributed. The proxi- toids. Such features include tooth dimorpho- mity of all the major land masses in the Late donty, the remarkable similarity in the size, spa- Jurassic (Smith et al. 1994) doubtless aided dis- cing and to some extent orientation of the teeth persal, although these flying animals probably in both upper and lower jaws, and the strength- had little difficulty crossing the usual barriers to ening of the skull (e.g. by deepening the mand- distribution such as seaways, or mountains. ibles and infilling the base of the orbit) to with- The most recent common ancestor of the Cte- stand relatively large loads rapidly applied to the nochasmatinae and the Gnathosaurinae was anterior ends of the jaws. 260 Unwin, D. M., Cearadactylus from the Santana Formation

Jurassic Cretaceous Middle 1 Upper Lower Upper JBj IBalCalOxIKiITt BelValHalBrl Ap I Al ICelT1 11 Cm I Ma I Iktiodactylus .....- Ornithocheiridae

I LI..l.l.l.ll.m Pteranodontidac ...... - - Azhdarchidae Tupuxuara

Tapejara

Cycnorharnphus - -Lonchodectidae Pterodactylus i--.II = ICtenochasmatinae A Gnathosaurinae

Fig. 6. Evolutionary history (A) of the Ctenochasmatidae and other pterodactyloid pterosaurs, reconstructed using the phylo- genies shown in Fig. 4 and the known stratigraphic distribution of taxa representing the various clades (Wellnhofer 1991a, Unwin et al. 2000, Unwin 2001). Palaeogeographic distribution of the Ctenochasmatidae in (B) the Upper Jurassic and (C) the Lower Cretaceous showing fossil localities that have yielded gnathosaurines (circles) and ctenochasmatines (triangles). Maps based on Smith et al. (1994). Abbreviations: Al, Albian; Ap, Aptian; Ba, Bathonian; Be, Bemasian; Bj, Bajocian; Br, Barremian; C, Cearadactylus; Ca, Callovian; Ce, Cenomanian; Cm, Campanian; E, Ctenochasrna; G, Gnathosaurus; Ha, Hau- terivian; Ki, Kimmeridgian; Ma, Maastnchtian; Ox, Oxfordian; P, Pterodaustro; Tt, Tithonian; T, Turonian; Va, Valanginian.

Acknowledgements vided illustrations and information on the holotype of Ceara- dactylus atrox. I thank N. Bakhurina, C. Bennett, M. Benton, I am very grateful to the following museums and institute M. Fastnacht, E. Frey, Junchang Lii, A. Kellner, D. Martill staff for giving me access to their collections, loaning materi- and P. Wellnhofer, for their helpful discussions of pterosaur al and providing much useful information: A. Milner and S. systematics, the Department of Zoology, Reading University, Chapman, The Natural History Museum, London, England; Department of Earth Sciences, Bristol University and the C. Forbes, S. Etchells-Butler, D. Norman and the late D. Royal Society for funding aspects of this work and the staff Price, Sedgwick Museum, Cambridge, England; P. Wellnho- of the Institut fiir Palaontologie, Museum fiir Naturkunde, fer, Bayerische Staatssammlung fur Palaontologie und Geolo- Berlin for all their help and assistance. R. Soler-Gijon kindly gie, Munich, Germany; G. Viohl, Jura Museum, Eichstatt, translated various Portugese texts and I am especially grate- Germany; M. Manabe and Y. Tomida, National Science Mu- ful to M. Benton, J. Dunlop, C. Bennett, D. Martill and seum, Tokyo, Japan; S. Nabana, Iwaki Museum of Coal and D. Naish for their comments on earlier versions of the text, Fossils, Iwaki, Japan; and E. Frey, Staatssammlung fiir Natur- R. Schoch for his translation of the abstract and Gloria Arra- kunde, Karlsruhe, Germany. G. Leonardi very kindly pro- tia for her editorial work on the MS. Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 5 (2002) 261

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