The Largest Flying Reptile from the Crato Formation, Lower Cretaceous, Brazil

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Historical Biology An International Journal of Paleobiology

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The largest flying reptile from the Crato Formation, Lower Cretaceous, Brazil

Xin Cheng, Renan A. M. Bantim, Juliana M. Sayão, Alexander W. A. Kellner, Xiaolin Wang & Antônio Á. F. Saraiva

To cite this article: Xin Cheng, Renan A. M. Bantim, Juliana M. Sayão, Alexander W. A. Kellner, Xiaolin Wang & Antônio Á. F. Saraiva (2018): The largest flying reptile from the Crato Formation, Lower Cretaceous, Brazil, Historical Biology, DOI: 10.1080/08912963.2018.1491567 To link to this article: https://doi.org/10.1080/08912963.2018.1491567

Published online: 04 Jul 2018.

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ARTICLE The largest ﬂying reptile from the Crato Formation, Lower Cretaceous, Brazil Xin Chenga,b, Renan A. M. Bantima, Juliana M. Sayãoc, Alexander W. A. Kellnerd, Xiaolin Wangb,e and Antônio Á. F. Saraivaa aLaboratório de Paleontologia, Universidade Regional do Cariri, Crato, CE, Brazil; bKey Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences (CAS), Beijing, China; cLaboratório de Paleobiologia e Microestruturas, Centro Acadêmico de Vitória, Universidade Federal de Pernambuco, Vitória de Santo Antão, PE, Brazil; dLaboratory of Systematics and Taphonomy of Fossil Vertebrates, Department of Geology and Paleontology,Museu Nacional/UFRJ, Rio de Janeiro, RJ, Brazil; eUniversity of Chinese Academy of Sciences, Beijing, China

ABSTRACT ARTICLE HISTORY The Early Cretaceous deposits of the Araripe Basin in northeast Brazil has yielded numerous vertebrate Received 24 April 2018 fossils, in which pterosaurs are the predominant tetrapods. Almost all specimens of this extinct group of Accepted 17 June 2018 ﬂ ying reptiles recovered from this basin come from two stratigraphic units, the Crato and Romualdo KEYWORDS Formations, with the pterosaurs from the former being usually small to middle-sized and large individuals Anhangueridae; Pterosauria; (with a maximized wingspan over 5 m) being only found in the latter. Here we report on a new specimen bone histology; Crato (MPSC R 1221) composed of a partial right wing, which is the largest pterosaur discovered from the Crato Formation; Cretaceous; Formation so far, having an estimated maximized wingspan of 5.5 m. Despite the incompleteness of this Brazil material, MPSC R 1221 can be referred to the Anhangueridae based on the length ratio between the metacarpal IV and the ﬁrst wing phalanx. According to the osteohistological study and the degree of fusion, MPSC R 1221 represents a sub-adult individual, showing that the animal had not reached the maximum size before its death. The present study shows that large-sized pterosaurs were also present in the Crato Formation and that their rarity might be an artefact of preservation.

Introduction 2013), which was recovered from the Romualdo Formation. It Pterosaurs are a group of extinct flying reptiles that became the has a wingspan of about 1.8 times larger than Arthurdactylus first vertebrates to developed powered flight (e.g., Wellnhofer conandoylei (SMNK 1132 PAL) whose wingspan was estimated 1991a; Kellner 2006;Chengetal.2017). The Araripe Basin being about 4.6 m (Frey and Martill 1994).Thelatterwassofarthe shows several important localities that yielded some of the best largest pterosaur from that stratigraphic unit. pterosaur material known worldwide (e.g., Wellnhofer 1985, Here we report on a partial right wing (MPSC R 1221) of the 1991b; Kellner and Tomida 2000). Several other fossils have largest pterosaur recovered from the Crato Formation so far, with been recorded in this region along the years (e.g., Kellner 1987; anestimatedwingspanexceeding5m.Wehavealsoperformed Maisey 1991), but flying reptiles predominate among tetrapods osteohistological sections to further assign the bone maturity of (e.g., Maisey 1991; Saraiva et al. 2014). Since the first specimen this new specimen. reported by Price (1971), over twenty-seven pterosaur species have been described up to now (e.g., Wellnhofer 1987;Freyand Institutional Abbreviations Martill 1994; Kellner and Campos 2002, 2007;Freyetal.2003a, AMNH-American Museum of Natural History, New York, USA. 2003b;Witton2009; Kellner 2013;Bantimetal.2014; Pêgas et al. 2016) some having exceptionally well preserved soft tissue (e.g., MN-Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil. Kellner 1996). Despite the controversy of taxonomic assignment of some taxa (e.g., Fastnacht 2001; Veldmeijer 2003;Rodrigues MPSC-Museu de Paleontologia Plácido Cidade Nuvens, and Kellner 2008; Martill and Unwin 2012; Pinheiro and Universidade Regional do Cariri, Santana do Cariri, Ceará, Brazil. Rodrigues 2017), two pterosaur groups, the toothed anhanguerids SMNK-Staatliches Museum für Naturkunde, Karlsruhe, and the toothless tapejarids, predominate (e.g., Campos and Germany. Kellner 1985; Kellner 1989;VilaNovaandSayão2012). Almost all these materials were discovered from two distinct UP-University of Portsmouth School of Earth and Environmental Sciences, UK. stratigraphic units: the Crato (Aptian) and the Romualdo (Aptian/ Albian) Formations (Pons et al. 1990; Kellner and Campos 1999; Neumann and Cabrera 1999; Valença et al. 2003; Kellner et al. Material and methods 2013), with only one exception (Martill 2008)whoseprovenance needstobeconfirmed. Among the most interesting findsisthe The specimen (MPSC R 1221) is composed of an incomplete right largest pterosaur species of Gondwanan deposit (Kellner et al. wing with the first wing phalanx exposed in ventral view. It was

Published online 04 Jul 2018 2 X. CHENG ET AL. discovered by Plácido Cidade Nuvens, former director of the local Specimen paleontological museum at a quarry situated close to the town MPSC R 1221, partial front limb housed in the Santana do Cariri (Ceará State). The specimen arrived at the Palaeontology Museum Plácido Cidade Nuvens, Santana do museum having several parts put together by a plastic acrylic Cariri, CE, Brazil. resin, with a small misplacement at the manual digits area. At Locality and horizon the museum, the specimen was prepared mechanically by steel Crato Formation, Early Cretaceous (Aptian), Araripe needle and pneumatic micro tools under a microscope (PDV Basin, Santana do Cariri, Crato, Northeastern Brazil. TS-30Y). Comments MPSC R 1221 was measured, photographed and described The specimen is not complete enough to allow a classifica- for bone microstructure investigation before sectioned, tion at the generic or specific level. Wing element ratios are according to the methodology proposed by Lamm (2013). generally used in the classification of incomplete pterosaur Traditionally, osteohistological studies use the area of the materials (e.g., Vila Nova and Sayão 2012). Based on the bone diaphysis since this region preserves a comparatively comparison of the proportion between the first wing phalanx larger amount of cortical tissue and growth markers (e.g., and the wing metacarpal among several clades (Table 1), the Francillon-Vieillot et al. 1990; Andrade and Sayão 2014). ratio of MPSC R 1221 is consistent with the Anhangueridae, However, some samples were sectioned in the portion of the to which this specimen is referred. Although not exclusive of metaphysis (second wing phalanx) following original the Araripe deposits (e.g., Rodrigues and Kellner 2013), this breakages of the limestone plates. A sample (approximately clade is well represented in the Romualdo Formation (e.g., 1cm of thickness) from the first and second wing digits was Kellner and Tomida 2000). obtained for osteohistological sections. The sectioned samples were immersed in clear epoxy resin Resapol T-208 catalyzed Description and comparison with Butanox M50. They were cut with the aid of a micro rectify (Dremel 4000 with extender cable 225) coupled to a MPSC R 1221 was preserved in a pale-yellow limestone diamond disk and left to dry. The section was ground and slab and the bones were flattened, a typical feature of the polished in a metal polishing machine (AROPOL-E, fossils recovered from the Crato Formation (Figure 1). AROTEC LTDA) using AROTEC abrasive grit (grit size 60/ The specimen is composed of an incomplete right wing, P60, 120/P120, 320/P400, 1200/P2500) to remove scratches including proximal and distal carpals, wing metacarpal, from the block. After the blocks were polished, they were another metacarpal (probably metacarpal I), manual glued on glass slides and thinned again, in order to make the digits, and first and second wing phalanges. The metacar- blocks translucent enough to enable the observation of osteo- pals and wing phalanges are still articulated while the histological structures under a biological microscope (Zeiss carpals and manual digits are displaced not far from Axio Imager 2). As usually used for paleobiological interpre- their original anatomical position. tations, all slabs were oriented exclusively in transversal view The carpal region is exposed in dorsal view, with all elements (see Lamm 2013 for a review). of the proximal and distal carpal series fused (Figure 2A). The sections were examined and photographed under a light Although crushed during the preservation process, the general microscope (Zeiss Inc. Barcelona) equipped with an AxioCam outline of the carpals is similar to pteranodontoids (see Kellner camera with Axio Imager. The M2 imaging software was used 2003), particularly to Anhanguera (Wellnhofer 1985, 1991b; in the examination procedure. Kellner and Tomida 2000). The proximal carpal is shorter in The maximized wingspan (maxws) and the normal wing- width than the distal and one is pierced by a foramen (Figure 2A). span (nws) were estimated based on a previous study (Kellner The metacarpal IV is a robust element with a length of et al. 2013), where the maximized wingspan being the result 246 mm, larger than the specimen (MN 6527-V) described by of the sum of the length of all front limbs plus the shorter one Sayão (2003) where this bone reached a length of 200 mm. between scapula and coracoid, and the normal wingspan The proximal end of this bone in MPSC R 1221 is taphono- being the maximized wingspan reduced by a reducing factor, mically deformed and exposed in anterior view (Figure 1). which is 5%. Based on the reconstructions of anhanguerid The preserved width is 36 mm, which is comparably smaller specimens provided by Wellnhofer (1991b) and Frey and than AMNH 22552 and the holotype of Anhanguera piscator Martill (1994), the completely preserved elements of MPSC (Wellnhofer 1991b; Kellner and Tomida 2000). The distal end R 1221, the wing metacarpal and the first wing phalanx, are is still articulated with the first wing phalanx and exposed in used to estimate the length of other incomplete or not pre- ventral view, and it is not clear if this bone was pierced by served bones. foramina as that of other anhanguerids (Wellnhofer 1991b; Kellner and Tomida 2000). Results and discussion Besides the wing metacarpal, another one is preserved (Figure 1). It is likely the metacarpal I and reaches the carpus. Systematic paleontology The bones of manual digit I-III were slightly displaced, Pterosauria Kaup, 1834 with two unguals still articulated with the phalanges Pterodactyloidea Plieninger, 1901 (Figure 2B). The unguals are curved and laterally compressed, Pteranodontoidea Marsh, 1876 showing a developed lateral sulcus positioned close to the Anhangueridae Campos and Kellner, 1985 ventral margin. Compared to AMNH 22552, the unguals in Anhangueridae indet. MPSC R 1221 are shorter and wider, being in this respect HISTORICAL BIOLOGY 3

Table 1. Measurements and proportions of the first wing phalanx and wing metacarpal of MPSC R 1221 and related taxa (in mm), including all published specimens recovered from the Araripe Basin. Specimen mcIV ph1d4 ph1d4/mcIV Authors Anhangueridae indet. 246 581 2.36 this paper MPSC R1221 Anhangueridae indet. 261 618 2.37 Kellner et al. 2013; this paper MPSC R1395 Anhangueridae 172 372 2.16 Wellnhofer 1991b; Kellner and Tomida 2000 AMNH 22552 Brasileodactylus sp. 171 355 2.08 Veldmeijer 2003 AMNH 24444 Arthurdactylus conandoylei 227 445 1.96 Frey and Martill 1994 SMNK 1132 PAL Ornithocheiridae indet. 169 383 2.27 Elgin and Frey 2012 SMNK PAL 3854 Anhangueridae indet. 137 251 1.83 Vila Nova et al. 2011 MN 7060-V Azhdarchoidea indet. 170 296 1.74 Elgin 2014 SMNK PAL 3900 Nurhachius ignaciobritoi 131.7 233 1.77 Wang et al. 2005 IVPP V 13288 Longchengpterus zhaoi 101 188 1.86 Lü et al. 2008 LPM0003 Tapejara wellnhoferi 102* 154* 1.51 Eck et al. 2011; this paper SMNK PAL 1137 Azhdarchidae? 180 235 1.31 Martill and Frey 1999 SMNK 2342 PAL Tupuxuara longicristatus 359 505 1.41 Unwin et al. 2000; IMCF 1052 Sinopterus dongi 95 121 1.27 Wang and Zhou 2003b IVPP V 13363 “Huaxiapterus” benxiensis 133 176 1.32 Lü et al. 2007; Kellner and Campos, 2007 BXGM V0011 Chaoyangopterus zhangi 185 200 1.08 Wang and Zhou 2003a IVPP V 13397 Jidapterus edentus 145.3 185.4 1.28 Wu et al. 2017 RCPS-030366CY Pteranodon 294 348 1.18 Bennett 2001 AMNH 4908 Pteranodon 556 573 1.03 Bennett 2001 BMNH 2959[R] Pteranodon 361 418 1.16 Bennett 2001 BMNH 3299 Pteranodon 345 394 1.14 Bennett 2001 BMNH 4006[L] Pteranodon 373 432 1.16 Bennett 2001 BMNH 4542 Pteranodon 459 493 1.07 Bennett 2001 FHSM 2120 Pteranodon 349 427 1.22 Bennett 2001 FMNH PR 494 Pteranodon 370 420 1.14 Bennett 2001 KUVP 977 Pteranodon 578 639 1.11 Bennett 2001 KUVP 1952 Pteranodon 394 468 1.19 Bennett 2001 LACM 50926[L] Pteranodon 484 558 1.15 Bennett 2001 ROM 26105 Pteranodon 315 376 1.19 Bennett 2001 UALVP 24239 Pteranodon 408 471 1.15 Bennett 2001 UM 12404 ‘A’ Pteranodon 389 447 1.15 Bennett 2001 UM 12404 ‘B’ Pteranodon 366 422 1.15 Bennett 2001 UUPI R.197[L] Pteranodon 601 692 1.15 Bennett 2001 YPM 2833 Pteranodon 400 467 1.17 Bennett 2001 CU 45062[R] *, measured by figure. Abbreviations: mcIV, metacarpal IV; ph1d4, first phalanx of manual digit IV. 4 X. CHENG ET AL.

Figure 1. The specimen MPSC R 1221. (A) Photo and (B) line drawing with missing portions in dark grey. The displacement of part of the specimen was corrected during the preparation of (B). Dotted lines are indicating the positions where samples for osteohistological sections were taken. Scale bars: 100 mm. Abbreviations: dca, distal carpal series; mcI, the ﬁrst metacarpal; mcIV, wing metacarpal; pca, proximal carpal series; pfo, pneumatic foramen; ph1-2d4, ﬁrst to second phalanges of manual digit IV; r, right; S1 and 2, section sample 1 and 2.

Figure 2. Details of MPSC R 1221. (A) Close up of the carpals. (B) Close up of manual digits I to III. (C) Close up of the proximal end of the first phalanx of manual digit IV. Scale bars: 10 mm. Abbreviations: dca, distal carpal series; etp, extensor tendon process; fo, foramen; pca, proximal carpal series; pfo, pneumatic foramen; ph1d4, first phalanx of manual digit IV; sul, sulcus. similar to the holotype of Anhanguera piscator (Wellnhofer Bone histology 1991b; Kellner and Tomida 2000). No pneumatic foramen on When analysing the thin sections in transversal view of the the unguals can be observed, differing from the condition first and second wing phalanx, micro-fragmentation of bone reported for Pteranodon and likely present in related taxa was observed due to the relatively flattened and two-dimen- (see Bennett 2001; Kellner 2010; Martin-Silverstone et al. sional preservation of the specimen. Despite the alteration of 2017; Kellner 2017; for controversy regarding the taxonomy the original conformation of the bone cortex, it is possible to of the Pteranodon complex). It is interesting to note that all observe several structures that characterize MPSC R 1221 as a unguals present a much lighter colour than other bones, sub-adult individual. suggesting the presence of the remains of a horny covering. The first wing phalanx is complete with a length of First phalanx of manual digit IV (S1) 581 mm, while the second lacks the distal half (Figure 1). Cortex of the first wing phalanx is low vascularized and The extensor tendon process is fused with the first wing predominantly constituted by lamellar bone, with a max- phalanx and no suture is visible (Figure 2C). At the ventral imum thickness of 460 μm(Figure 3A). Compared to the side of the proximal end, the first wing phalanx presents a proximal region of the second phalanx of manual digit IV, well-developed ridge surrounding the articulation that S1 presents a smaller quantity of reticular (Figure 3B, 3D) received the wing metacarpal (Figure 2C). Nearby the and longitudinal (Figure 3C) vascular canals, the same ridge, there is a large, longitudinally directed pneumatic feature observed in MN 6594-V (Kellner et al. 2013). The foramen (Figure 2C), which is also seen in AMNH 22552 endosteal region does not show endosteal lamellae and the holotype of Anhanguera piscator (Wellnhofer (Figure 3B), but in some places it is possible to observe 1991b; Kellner and Tomida 2000). the formation of trabeculae (Figure 3C). The cortex of the HISTORICAL BIOLOGY 5

first phalanx of manual digit IV is separated into two parts (Figure 3B), the inner (or endosteal) region with the gaps of osteocyte lacunae being horizontally arranged, and the outer region (in the periosteum) with disorganized and unstandardized osteocytes. This condition represents a secondary bone tissue, defined by deposition of a new bone layer over a previously resorbed layer (Steel 2008). In the endosteal portion, some small areas of bone resorption can be observed (Figure 3D). Since the bone remodelling was active before this individual death, it indicates this animal has reached an advanced ontogenetic stage (De Ricqlès et al. 2000; Sayão 2003;Steel2008). Two LAGs (Lines of arrested growth) can be seen in S1 (Figure 3B)thatindi- cates at least two pauses during the growth of this individual. LAGs have been reported in different bones of several pterosaur taxa (Steel 2008; Kellner et al. 2013), indicating that bone growth rate was not always constant in these flying reptiles (Sayão 2003). In the periosteal region, the EFS (External Fundamental System) is absent, which means that this animal had not yet reached its total asymptotic growth before being fossilized. EFS has been found in some skeletally mature tetrapods and is characterized by a periosteal layer without vascular channels and highly laminated (Andrade et al. 2015). In pterosaurs, this bone deposition was found so far only in Tropeognathus cf. T. mesembrinus (Kellner et al. 2013), a potential anhanguerid (MN 4809-V, Sayão 2003) and an unnamed ornithocheirid (UP 2000.2, Steel 2008). Osteohistological samples of large pterosaurs (wingspans more than 5 m) have not been often performed, with the exception of Tropeognathus cf. T. mesembrinus (Kellner et al. 2013)andQuetzalcoatlus sp. (De Ricqlès et al. 2000). In the general osteohistological features, MPSC R 1221 is very similar to Tropeognathus cf. T. mesembrinus with some particularities, most concerning the developmental stages of each studied individual. Despite presenting LAGs, MPSC R 1221 does not show any endosteal or periosteal lamellae, both features present in Tropeognathus cf. T. mesembrinus (Kellner et al. 2013). The absence of these layers indicates that MPSC R 1221 could still grow more, exceeding its current size despite its subadult stage. These features also indicate that MPSC R 1221 was a younger individual than Tropeognathus cf. T. mesembrinus. As described above, the extensor tendon process and the first wing phalanx are fused and no suture is observable. According to Kellner (2015), the fusion of these elements is one feature of the ontogeny stage 5 (OS5), which is the last stage before ontogenetic maturity (OS6). The author also pointed out that the ossification did not stop at OS5 consistent with the osteohistological analysis performed here. Proximal portion of the second phalanx of manual digit Figure 3. Osteohistological sections of the first phalanx of manual digit IV from IV (S2) MPSC R 1221 (S1). (A) Cross section of the cortex sample of the first phalanx of manual digit IV is dominated by lamellar bone with red frames indicating the The cortex of the second wing phalanx has a maximum position of B, C and D. (B) Total cortex with 2 LAGs and reticular canals. (C) thickness of 410 μm, is highly vascularized and formed basically Endosteal portion of the bone, showing the presence of erosion rooms. (D) by parallel-fibered bone tissue, including a well-developed Small cortex showing one LAG, and one trabecula. Scale bars: 10mm in A, 200 μm in B, C and D. The symbols + and – represents respectively periosteum and Haversian bone complex (Figure 4A-E). The Haversian bone endosteum. Abbreviations: er, erosion room; lag, line of arrested growth; t, complex was recovered in only a few pterosaurs (e.g., Sayão trabeculae; vc, vascular canal. 2003) and its function has already been related to endothermy 6 X. CHENG ET AL.

Figure 4. Osteohistological sections of the proximal portion of the second phalanx of manual digit IV from MPSC R 1221 (S2). (A) Cross section of the cortex sample of the second phalanx of manual digit IV is dominated by parallel-ﬁbered bone with red frames indicating the position of B, C, D and E. (B) Total cortex with 2 LAGs and many secondary osteons, forming a Haversian bone complex. (C) Inner region containing a high number of secondary osteons and vascular canals. (D) Endosteal portion of the bone, containing 2 erosion rooms in initial formation. (E) Endosteal portion of the bone, containing many erosion rooms and trabeculae. Scale bars: 10mm in A, 200 μm in B, C, D and E. The symbols + and – represents respectively periosteum and endosteum. Abbreviations: er, erosion room; lag, line of arrested growth; so, secondary osteon; vc, vascular canal.

(De Ricqlès et al. 2000;Steel2008;Chinsamyetal.2009). piscator, AMNH 22552, and the holotype of Arthurdactylus However,thepresenceofthisbonetissueindicatesonlyahigh conandoylei. First, we calculated the sum of the length of wing growth rate (Sayão 2003). In S2, secondary resorption occurred metacarpal and ﬁrst wing phalanx in these specimens (mcIV on most of the endosteal surface that modify the pneumatic space +ph1d4). Then calculated the ratios between ‘mcIV+ph1d4’ in the centre of the bone and forms several trabeculae composed and other elements (Table 2). These ratios were used to of parallel axial lamellae, with some showing signs of reabsorption estimate the length of missing bones and wingspan of and redeposition (Figure 4B). A few vascular canals are present in MPSC R 1221 (Table 3). The maximized wingspan of MPSC the cortex, being mostly anastomosed and reticular. Because of R 1221 is 5.5 m, with a normal wingspan of 5.2 m, following the high rate of remodelling in this bone, most of the cortex is the reducing factor introduced by Kellner et al. (2013). ﬁlled with areas of bone resorption and secondary osteons. In the The holotype of Arthurdactylus conandoylei and the holo- periosteum, two LAGs have been observed, with one in the type of the tapejarine Sinopterus dongi were used to estimate uppermost layer of the cortex and the other one in the deep maximized wingspans of other pterosaur material recovered cortex, which is remarkably reabsorbed in the endosteal region from the Crato Formation (Table 4). MPSC R 1221 presents a (Figure 4B). These characters also point to a more advanced maximized wingspan that is at least 23% larger than any other ontogenetic stage, possibly in a sub-adult stage, as that have toothed or toothless species recovered from the Crato been observed in S1. Formation. Based on the bone histology, this new specimen represents It should be noted that another specimen referable to a sub-adult individual by the presence of a secondary bone, Anhangueridae (MPSC R 1395) from the Romualdo with growth marks, secondary osteons and resorption zones. Formation consisting of a partial wing, has a similarly estimated wingspan (maxws=5.5 m, nws=5.2 m; Kellner et al. 2013). MPSC R 1395 was regarded to represent a young Maximized wingspan animal, what was based on the unfused extensor tendon The calculation of the wingspan of MPSC R 1221 was made process (Kellner et al. 2013). In the same paper, another based on comparisons with the holotype of Anhanguera anhanguerid specimen, MN 6594-V (Tropeognathus cf. T. HISTORICAL BIOLOGY 7

Table 2. Anhanguera piscator (NSM-PV 19892), AMNH 22552 and Arthurdactylus conandoylei (SMNK 1132 PAL) ratios. Ratios Anhanguera piscator AMNH 22552 Arthurdactylus conandoylei (mcIV+ph1d4)/sca 7.268 7.282 8.400 (mcIV+ph1d4)/hu 3.192 3.200 2.922 (mcIV+ph1d4)/ul(or ra) 2.807 2.243 2.154 (mcIV+ph1d4)/ph2d4 1.675 1.679 1.672 (mcIV+ph1d4)/ph3d4 2.153 2.159 2.154 (mcIV+ph1d4)/ph4d4 3.392 3.400 2.444 (mcIV+ph1d4)/fe 3.479 3.487 3.537 (mcIV+ph1d4)/ti 2.907 2.914 2.872 Authors Kellner and Tomida 2000 Wellnhofer 1991b Frey and Martill 1994 Abbreviations: fe, femur; hu, humerus; mcIV, wing metacarpal; ph1-4d4, ﬁrst to fourth phalanx of manual digit IV; ra, radius; sca, scapula; ti, tibia; ul, ulna.

Table 3. Estimated lengths (in mm) of the forelimb and hind limb elements of MPSC R 1221 based on the bone ratios of Anhanguera piscator (NSM-PV 19892), AMNH 22552 and Arthurdactylus conandoylei (SMNK 1132 PAL) (Table 2). The length of the wing metacarpal, the ﬁrst wing phalanx and the carpals were kept constant since they were measured directly on the specimen. The maxws and nws were obtained based on Kellner et al. (2013). sca hu ul mcIV ph1d4 ph2d4 ph3d4 ph4d4 car fe ti maxws nws Based on Anhanguera piscator 114 259 295 246 581 494 384 244 30 238 284 5294 5029 Based on AMNH 22552 114 258 369 246 581 493 383 243 30 237 284 5434 5162 Based on Arthurdactylus conandoylei 98 283 384 246 581 495 384 338 30 234 288 5678 5394 mean values 109 267 349 246 581 494 384 275 30 236 285 5470 5197 Abbreviations: car, carpals; fe, femur; hu, humerus; maxws, maximized wingspan; mcIV, wing metacarpal; nws, normal wingspan; ph1–4d4, ﬁrst to fourth phalanx of manual digit IV; sca, scapula; ti, tibia; ul, ulna.

Table 4. Measurements and maximized wingspan (in mm) of specimens with postcranial elements recovered from the Crato Formation based on Arthurdactylus conandoylei (SMNK 1132 PAL) and Sinopterus dongi (IVPP V 13363). Taxa sca hu ul mcIV ph1d4 ph2d4 ph3d4 ph4d4 car fe ti maxws Author MPSC R1221 - - - 246 581 - - - 30 - - 5678** This paper Arthurdactylus conandoylei 80 230 312 227 445 402 312 275 20* 190 234 4606 Frey and Martill 1994 SMNK 1132 PAL Ornithocheiridae indet. 73.5 157 252 169 383 - - - - 161 202 3682** Elgin and Frey 2012 SMNK PAL 3854 MN 6527-V - 148.7 206.0 201.2 ------2761*** This paper Azhdarchoidea indet. - - - - 294 209 127 45 - 183 262 2669*** Elgin 2014 SMNK PAL 6409 Azhdarchoidea indet. - 139 177 170 296 185 121 - - 157.5 234 2544*** Elgin 2014 SMNK PAL 3900 Azhdarchid - - - 180 235 165 78 - - - - 2155*** Martill and Frey 1999 SMNK 2342 PAL *estimated based on MPSC R 1221; ** calculated based on the holotype of Arthurdactylus conandoylei (SMNK 1132 PAL); ***calculated based on the holotype of Sinopterus dongi (IVPP V 13363). Abbreviations: car, carpals; fe, femur; hu, humerus; maxws, maximized wingspan; mcIV, wing metacarpal; ph1–4d4, first to fourth phalanx of manual digit IV; sca, scapula; ti, tibia; ul, ulna. mesembrinus) was considered an adult individual and is the wing phalanx and bone histology, MPSC R 1221 presents a sub- largest pterosaur ever recorded in the Araripe Basin. This adult individual of a late ontogeny stage (OS5) at time of death, individual had a maximized wingspan of 8.7 m and a normal which means that the final maximized wingspan might have been wingspan of 8.3 m (Kellner et al. 2013), which is about 59% larger. This is corroborated by the osteohistological sections since larger than MPSC R 1221. this individual did not present an external fundamental system. This specimen also shortens the size-gap between the pterosaur fauna from the Crato and Romualdo Formations. We advocate Conclusion that the comparatively small sizes of the Crato pterosaurs might be a taphonomic artefact and that large flying reptiles might have The discovery of MPSC R 1221 provides new information for the presented in the region of the Araripe basin since the deposition of pterosaur materials from the Crato Formation (Aptian, the Crato layers. Cretaceous), including size and ontogeny. MPSC R 1221 is the largest pterosaur material discovered from the Crato Formation so far, with a maximized wingspan of about 5.5 m. It represents an Acknowledgments Anhangueridae, based on the portion of the metacarpal IV and the first wing phalanx, with the genus and species still uncertain. We thank Esau Victor Araújo (CAV-UFPE) for preparing the osteohistolo- Based on the fusion of the extensor tendon process and the first gical sections. 8 X. CHENG ET AL.

Funding Kellner AWA. 1989. A new edentate pterosaur of the Lower Cretaceous from the Araripe Basin, Northeast Brazil. Anais da Academia This study was supported by the Fundacão Cearense de Apoio ao Brasileira de Ciências. 61:439–445. fi Desenvolvimento Cientí co e Tecnológico (FUNCAP) under Grant to Kellner AWA. 1996. Reinterpretation of a remarkably well preserved XC DCR-0024-02039.01.00/ and to RAMB BMD-0124-00302.01.01/19; pterosaur soft tissue from the Early Cretaceous of Brazil. Journal of fi the Conselho Nacional de Desenvolvimento Cientí co e Tecnológico Vertebrate Paleontology. 16(4):718–722. (CNPq) under Grant to AAFS 458164/2014-3, to AWAK 304780/2013- Kellner AWA. 2003. Pterosaur phylogeny and comments on the 8 and 420687/2016-5 and to JMS 311715/2017-6; the Fundação Carlos evolutionary history of the group. In: BuffetautE,MazinJM,eds. Chagas Filho de Amparo a Pesquisa do Estado do Rio de Janeiro Evolution and paleobiology of pterosaurs. 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