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The Evolution of Pneumatic Foramina in Pterosaur Vertebrae Anais da Academia Brasileira de Ciências (2019) 91(Suppl. 2): e20180782 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201920180782 www.scielo.br/aabc | www.fb.com/aabcjournal The Evolution of Pneumatic Foramina in Pterosaur Vertebrae RICHARD BUCHMANN and TAISSA RODRIGUES Laboratório de Paleontologia, Departamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, Avenida Fernando Ferrari, 514, Goiabeiras, 29075-910 Vitória, ES, Brazil Manuscript received on September 24, 2018; accepted for publication on January 18, 2019 How to cite: BUCHMANN R AND RODRIGUES T. 2019. The Evolution of Pneumatic Foramina in Pterosaur Vertebrae. An Acad Bras Cienc 91: e20180782. DOI 10.1590/0001-3765201920180782. Abstract: Pterosaurs possess skeletal pneumatization, which can be assessed externally through the observation of pneumatic foramina. These foramina vary in position, shape, and number among taxa. Here we propose new characters referring to the position and number of pneumatic foramina present in cervical and dorsal vertebrae of pterosaurs. A cladistic analysis was performed after first-hand study of material in collections and using data from the literature in order to test these new characters for homology, and they were subsequently mapped in a strict consensus tree. The analysis resulted in nine equally parsimonious trees with 215 steps each. The strict consensus tree obtained does not present significant differences in relation to trees obtained in previous studies. The mapping performed identified that most pneumatic foramina evolved independently in several lineages, and only two of the eight added characters appeared once in the evolution of pterosaurs. In general, pneumatic foramina were more common in the Dsungaripteroidea, however, the flattened preservation of non-pterodactyloids and in the Archaeopterodactyloidea often precludes their visualization, and therefore the presence of vertebral pneumatization may be broaden with the discovery of new, better preserved specimens. Key words: Pterosauria, phylogeny, axial skeleton, skeletal pneumatization. INTRODUCTION can be inferred by the observation of external structures, such as the pneumatic foramina, which Pterosaurs are known as the first vertebrates are connected to internal cavities. to develop the ability to fly actively. This is Besides pterosaurs and extant birds, possible due to the presence of an extremely postcranial pneumatization is also observed in specialized skeleton with unique features, such as the Sauropodomorpha and non-avian Theropoda the presence of wings and of pneumatic bones, a (O’Connor 2006, Butler et al. 2012), raising condition analogous to birds (Nesbitt 2011) which questions about the evolution of this system considerably decreases bone mass, reducing the in archosaurs (Butler et al. 2012). As some weight of the animal. Internal bone pneumatization archosauriforms, such as Erythrosuchus, have limited evidence of pneumatization such as Correspondence to: Richard Buchmann foramina and fossae that do not contact pneumatic E-mail: [email protected] chambers, Butler et al. (2012) did not exclude ORCid: http://orcid.org/0000-0003-4428-9224 * Contribution to the centenary of the Brazilian Academy of the possibility of skeletal pneumatization being Sciences. plesiomorphic for Archosauria. BIOLOGICAL SCIENCES An Acad Bras Cienc (2019) 91(Suppl. 2) RICHARD BUCHMANN and TAISSA RODRIGUES THE PNEUMATIC FORAMINA IN PTEROSAUR VERTEBRAE In birds, postcranial pneumatization is The present study aims to better understand associated with the presence of air sacs, which allow possible homologies and convergences in the the invasion of air inside the bone. Considering evolution of pneumaticity in Pterosauria. the role of pneumatic structures in avian lung INSTITUTIONAL ABBREVIATIONS ventilation, its presence in pterosaurs suggests the existence of a respiratory system analogous to that MN, Departamento de Geologia e Paleontologia, present in birds (Claessens et al. 2009). Museu Nacional, Universidade Federal do Rio de Postcranial pneumatization in pterosaurs is Janeiro, Rio de Janeiro, Brazil; NSM-PV, Division mostly inferred for the vertebral column, although of Vertebrate Paleontology, National Science specimens with a wingspan greater than 2.5 m Museum, Tokyo, Japan; YPM, Yale Peabody also tend to present evidences for pneumatization Museum of Natural History, New Haven, USA. in the appendicular skeleton (Butler et al. 2009, Claessens et al. 2009). In birds, pneumatic MATERIALS AND METHODS foramina are observed in vertebral regions that do We used as a base the data matrix from Wang et not compromise the bone’s integrity, thus varying al. (2008), a dataset which has been updated and between taxa (Müller 1908). Possibly the same corrected several times since its first proposal happened in pterosaurs. (Kellner 2003) and therefore likely has fewer, if In all phylogenetic proposals so far raised for any, character states incorrectly scored. This data the Pterosauria, characters referring to the vertebrae matrix also focused on the Pterodactyloidea, which are limited mainly to the morphology of mid- besides including the largest known pterosaurs cervicals or the ontogenetic fusion of structures, (and therefore the ones more prone to possess such as between the atlas and axis and the formation pneumatization), are generally better preserved, of the notarium (Kellner 2003, Unwin 2003, Wang facilitating the visualization of pneumatic foramina et al. 2008, Andres et al. 2014) and thus could be and therefore of skeletal pneumatization. In further explored. In this aspect, Andres et al. (2014) addition, this matrix presented few pterodactyloid incorporate new characters referring to the size and terminal taxa in which data regarding the vertebral proportion of different types of vertebrae, including column data was not preserved and thus would be dorsals and caudals (characters 17 to 21). However, missing data. generally, characters on vertebral pneumatization As in the original analysis by Wang et al. refer only to the presence of pneumatic foramina (2008), the outgroup was composed by three on the lateral sides of the centrum in the mid- successive outgroups: Ornithosuchus longidens cervical vertebrae, such as characters 44 in Kellner (Huxley 1877) (the one outgroup defined as such (2003), 47 in Wang et al. (2008) and 159 in Andres in TNT), Herrerasaurus ischigualastensis Reig, et al. (2014). Andres et al. (2014) proposed a new 1963, and Scleromochlus taylori Woodward, 1907. character on the presence of pneumatic foramina In this analysis, we used the 79 characters and the laterally to the neural canal (character 160); 46 species analyzed in the original matrix. Here, however, the occurrence of the pneumatic foramina we considered Anhanguera santanae (Wellnhofer dorsally to the neural canal, commonly observed 1985) a nomen dubium, after Pinheiro and in dsungaripteroids, was not discussed. Pneumatic Rodrigues (2017) and substituted this species for foramina present in dorsal vertebrae were also not the specimen AMNH 22555 (Anhanguera sp.), included in their analysis. which was previously referred to this taxon. An Acad Bras Cienc (2019) 91(Suppl. 2) e20180782 2 | 13 RICHARD BUCHMANN and TAISSA RODRIGUES THE PNEUMATIC FORAMINA IN PTEROSAUR VERTEBRAE Eight characters were incorporated into this Forey and Kitching (2000). Therefore, as character matrix; three of them were proposed by Andres et 85 depends on the presence of characters 81 and/or al. (2014) (their characters 158, 159 and 160) and 84, it is possible to have an inapplicable condition five of them are new (Figure 1). Four of these five for some terminal taxa. Inapplicable codings were were proposed based on codification of nominal scored as “?”, as in the original matrix (Wang et al. variables (Hawkins 2000), referring to either the 2008). However, in the figures missing data and absence or the presence of pneumatic foramina inapplicable characters related to the characters in cervical and dorsal vertebrae, establishing that being investigated are differentiated. Individual characters are attributes that can be proposed each variations in which, for instance, a foramen is as transformations, being independent of each other observed only in one side of the vertebra, were (De Pinna 1991). scored as present. Character 80: Mid-cervical vertebra, neural arch, Character 47 of the original matrix, “Pneumatic lateral surface, pneumatic foramen: absent (0); foramina on the side of centrum in cervical present (1) (from Andres et al. 2014). vertebrae”, was divided in two characters to Character 81: Mid-cervical vertebra, centrum, consider variations in the pneumatization between lateral surface, pneumatic foramen: absent (0); mid-cervical and posterior cervical vertebrae present (1) (from Andres et al. 2014). (present characters 81 and 84). Character 82: Mid-cervical vertebra, lateral to The data matrix was edited with Mesquite, neural canal, pneumatic foramen: absent (0); version 3.03 (Maddison and Maddison 2015) present (1) (from Andres et al. 2014). and the phylogenetic analysis was performed Character 83: Mid-cervical vertebra, dorsal to in TNT, version 1.1 (Goloboff et al. 2008). All neural canal, pneumatic foramen: absent (0); characters were considered with equal weights present (1) (new). and non-addictive. The analysis was performed Character 84: Posterior
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