Cervical anatomy and its relation to foraging habits in aquatic birds (Aves: Neornithes: Neoaves).

Birds have extremely flexible necks, which help in their search for food. However, studies on the variation in bird cervical anatomy and its relationship with foraging are rare, despite the different habits presented between species. Here, we analyze the anatomy of the neck of aquatic birds and relate it to their foraging strategies. We dissected specimens representing four species of Charadriiformes, 11 species of Phaethoquornithes, and two specimens belonging to the outgroup Telluraves. We chose to emphasize Charadriiformes and Phaethoquornithes because they present several strategies that require cervical mobility and stability. We note that vertebral anatomy and dimensions vary, which affects the shape and size of the soft tissues attached throughout the neck. The synovial cartilage present in the articulatio intercorporalis represents an additional length in the neck, however, this is not longer than that observed in animals with intervertebral discs. Our analysis indicates that birds have a prevalence of dorsoventral movements in the middle of the neck and lateral and rotational movements near the base of the neck, while the region near the head presents a wide range of movement in all directions. Cervical ligaments and muscles throughout the neck provide stability in all segments, although the robustness of the soft tissues indicates that the most caudal portion of the neck is the most stable. The vertebral and soft tissue anatomy is consistent with the extensive mobility in pitching, yaw, and roll movements performed mainly by the head and first segment of the neck during the different foraging of the analyzed birds. Furthermore, the muscles closer to the skull are robust and allow the execution of a variety of habits to capture food in different species. The subsequent cervical segments present differences that explain their reduction in mobility, but they are equally stable.

Arthrological reconstructions of the pterosaur neck and their implications for the cervical position at rest.

The lack of any pterosaur living descendants creates gaps in the knowledge of the biology of this group, including its cervical biomechanics, which makes it difficult to understand their posture and life habits. To mitigate part of this issue, we reconstructed the cervical osteology and arthrology of three pterosaurs, allowing us to make inferences about the position of the neck of these animals at rest. We used scans of three-dimensionally preserved cervical series of Anhanguera piscator, Azhdarcho lancicollis and Rhamphorhynchus muensteri for the reconstructions, thus representing different lineages. For the recognition of ligaments, joint cartilages, and levels of overlapping of the zygapophyses, we applied the Extant Phylogenetic Bracket method, based on various extant birds and on Caiman latirostris. We inferred that pterosaur intervertebral joints were probably covered by a thin layer of synovial cartilage whose thickness varied along the neck, being thicker in the posterior region. Ignoring this cartilage can affect reconstructions. According to the vertebral angulation, their neck was slightly sinuous when in rest position. Our analyses also indicate that pterosaurs had segmented and supra-segmented articular cervical ligaments, which could confer stabilization, execute passive forces on the neck and store elastic energy.

A new toothless pterosaur from the Early Cretaceous Jehol Biota with comments on the Chaoyangopteridae.

The Chaoyangopteridae is a clade of azhdarchoid pterosaurs that stands out in China, particularly in the Jehol Biota, as a Cretaceous group of medium-sized and high-crested pterosaurs. Herein, we describe a new species, Meilifeilong youhao gen. et sp. nov., based on two specimens, one tentatively referred to this taxon. This new species represents the most complete and well-preserved chaoyangopterid recorded to date. Along with a set of characters (low premaxillary crest above the nasoantorbital fenestra extending posteriorly, posterior premaxillary process arched and curving posteriorly, a slightly convex sternal articulation surface of coracoid, and a fibular shaft close to proximal articulation strongly arched posteriorly), this species also provides new information both on the unknown palatal region of this clade, and on the rarely preserved (in place) ear portion with stapes. Moreover, M. youhao sheds light on paleoecological aspects, while also giving new information about the taxonomic diversity of this peculiar group of Jiufotang pterosaurs.

Quantitative assessment of the vertebral pneumaticity in an anhanguerid pterosaur using micro-CT scanning.

Research on the postcranial skeletal pneumaticity in pterosaurs is common in the literature, but most studies present only qualitative assessments. When quantitative, they are done on isolated bones. Here, we estimate the Air Space Proportion (ASP) obtained from micro-CT scans of the sequence from the sixth cervical to the fourth dorsal vertebra of an anhanguerine pterosaur to understand how pneumaticity is distributed in these bones. Pneumatisation of the vertebrae varied between 68 and 72% of their total volume. The neural arch showed higher ASP in all vertebrae. Anhanguerine vertebral ASP was generally higher than in sauropod vertebrae but lower than in most extant birds. The ASP observed here is lower than that calculated for the appendicular skeleton of other anhanguerian pterosaurs, indicating the potential existence of variation between axial and appendicular pneumatisation. The results point to a pattern in the distribution of the air space, which shows an increase in the area occupied by the trabecular bone in the craniocaudal direction of the vertebral series and, in each vertebra, an increase of the thickness of the trabeculae in the zygapophyses. This indicates that the distribution of pneumatic diverticula in anhanguerine vertebrae may not be associated with stochastic patterns.

Mass mortality events of autochthonous faunas in a Lower Cretaceous Gondwanan Lagerstätte.

Mass mortality events are unusual in the Crato Formation. Although mayflies' accumulations have been previously reported from that unit, they lacked crucial stratigraphic data. Here we provide the first taphonomic analysis of a mayfly mass mortality event, from a layer 285 cm from the top of the Formation, with 40 larvae, and an overview of the general biological community structure of a three meters deep excavated profile. The only other autochthonous taxon observed in the mayfly mortality layer was the gonorynchiform fish Dastilbe. The larvae and fishes were smaller than usual in the layer 285 cm, suggesting that they lived in a shallow water column. Their excellent preservation and a lack of preferential orientation in the samples suggest an absence of significant transport. All mayflies belong to the Hexagenitidae, whose larvae lived in quiet waters. We also recovered allochthonous taxa in that layer indicative of drier weather conditions. Adjacent layers presented crystals and pseudomorphs of halite, suggesting drought and high salinity. In other layers, Dastilbe juveniles were often found in mass mortality events, associated with a richer biota. Our findings support the hypothesis that the Crato Formation's palaeolake probably experienced seasonal high evaporation, caused by the hot climate tending to aridity, affecting the few autochthonous fauna that managed to live in this setting.

Unmasking a gap: A new oligoneuriid fossil (Ephemeroptera: Insecta) from the Crato Formation (upper Aptian), Araripe Basin, NE Brazil, with comments on Colocrus McCafferty.

The Crato Formation (Araripe Basin) preserves one of the most diverse entomofaunas of the Cretaceous. Among the groups of insects, mayflies stand out in abundance, but among them oligoneuriids are especially rare. A newly discovered adult oligoneuriid from this unit is here described as Incogemina nubila gen. et sp. nov. and new subfamily Incogemininae. A phylogenetic analysis recovered the new taxon as the sister group to the species-rich and cosmopolitan Oligoneuriinae. The paratype of Colocrus indivicum, described as an "oligoneuriid" from the same unit, is here reviewed and considered as belonging to the family Hexagenitidae. The biogeographical and taxonomic implications of this discovery and the phylogenetic position of Incogemina nubila are discussed. Incogemina bridge an important morphological gap between the Oligoneuriinae and the extant Chromarcys. Also, it demonstrates that the divergence between Oligoneuriinae and Incogemininae probably occurred in South America.

Author Correction: An Early Cretaceous pterosaur with an unusual mandibular crest from China and a potential novel feeding strategy.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Pterodactyloid pterosaur bones from Cretaceous deposits of the Antarctic Peninsula.

Fossil vertebrates from Antarctica are considerably rare, hampering our understanding of the evolutionary history of the biota from that continent. For several austral summers, the PALEOANTAR project has been carrying out fieldwork in the Antarctic Peninsula in search for fossils, particularly Cretaceous vertebrates. Among the specimens recovered so far are two bones referable to Pterosauria, more specifically to the Pterodacyloidea, the first volant reptiles from Antarctica to be fully described. MN 7800-V (part and counterpart) was recovered from a moraine at the Abernathy Flats (Santa Marta Formation, Lachman Crags Member, Santonian-Campanian) on James Ross Island. It is interpreted as the distal articulation of a first phalanx of the wing finger, representing an animal with an estimated wingspan between 3 and 4 m. The second specimen (MN 7801-V) comes from Vega Island (Snow Hill Island Formation, Maastrichtian) and is identified as a wing metacarpal IV of an animal with an estimated wingspan from 4 to 5 m. These occurrences show that pterodactyloids inhabited the Antarctic Peninsula at least during the Upper Cretaceous and demonstrate that large pterosaurs were widespread through all parts of the planet during that period.

Comparative analysis of the vertebral pneumatization in pterosaurs (Reptilia: Pterosauria) and extant birds (Avialae: Neornithes).

Birds and pterosaurs have pneumatic bones, a feature likely related to their flight capabilities but whose evolution and origin is still poorly understood. Pneumatic foramina are present on the external surface of the bone and are reliable indicators of post-cranial skeletal pneumatization present in Pterosauria, Eusauropoda, and Neotheropoda. Here, we carried out a qualitative analysis of the position, size and number of pneumatic foramina of the cervical and thoracic/dorsal vertebrae of pterosaurs and birds, as they have the potential to challenge hypotheses about the emergence and evolution of the respiratory trait in these groups. We also discussed differences between pneumatic and vascular foramina for identification purposes. Besides phylogenetic representativeness, the pterosaur taxonomic sampling considered the preservation of specimens and, for birds, their life habit, as this relates to the level of pneumatization. Pneumatic foramina on the lateral faces of the centrum of the mid-cervical vertebrae of pterosaurs and birds differ in position and size, and those adjacent to the neural canal additionally differ in number. The avian posterior cervical vertebrae show a higher number of pneumatic foramina in comparison to their mid-cervicals, while the opposite is true for pterosaurs, suggesting differences in the cervical air sac of these clades. Pneumatic foramina were found at the base of the transverse processes of the notarial vertebrae of birds, while they were absent from some of the pterosaurs analyzed here, revealing the presence of a pneumatic hiatus in the vertebral column that might be explained due to the distance of this structure to the cervical air sac. These findings indicate that, although the overall skeletal pneumatization of pterosaurs and birds present deep homologies, some pneumatic features occurred convergently because variation in the number of pneumatic foramina along the vertebral column is related to the position of the air sacs in pterosaurs and birds and/or the habit of each species. There is an evident reduction of the pneumatic foramina in birds that have aquatic foraging and an increase in the ones which perform static soaring. Although we did not find any external anatomical difference between pneumatic and vascular foramina, we observed that vascular foramina occur at specific sites and thus identification on the basis of location is reliable.

The Evolution of Pneumatic Foramina in Pterosaur Vertebrae.

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.

On a new crested pterodactyloid from the Early Cretaceous of the Iberian Peninsula and the radiation of the clade Anhangueria.

The pterosaur record from the Iberian Peninsula is mostly scarce and undefined, but in the last few years some new taxa have been described from different Lower Cretaceous sites of Spain. Here we describe a new genus and species of toothed pterodactyloid pterosaur from the Barremian of the Iberian Peninsula, Iberodactylus andreui gen. et sp. nov., that shows a close and rather unexpected relationship with Hamipterus tianshanensis from China. A review of the phylogenetic relationships of the Anhangueria reveals a new family of pterodactyloid pterosaurs, the Hamipteridae fam. nov. being recovered as sister-group of the Anhangueridae. This latter clade can be in turn divided into the new clades Anhanguerinae and Coloborhynchinae. The close relationships of Iberodactylus and Hamipterus shows an interesting palaeobiogeographical correlation between the Chinese and Iberian pterosaur faunas during the Barremian (Lower Cretaceous). The discovery of Iberodactylus strongly suggests that the clade Anhangueria has clear ancestral ties in eastern Laurasia.

Egg accumulation with 3D embryos provides insight into the life history of a pterosaur.

Fossil eggs and embryos that provide unique information about the reproduction and early growth of vertebrates are exceedingly rare, particularly for pterosaurs. Here we report on hundreds of three-dimensional (3D) eggs of the species Hamipterus tianshanensis from a Lower Cretaceous site in China, 16 of which contain embryonic remains. Computed tomography scanning, osteohistology, and micropreparation reveal that some bones lack extensive ossification in potentially late-term embryos, suggesting that hatchlings might have been flightless and less precocious than previously assumed. The geological context, including at least four levels with embryos and eggs, indicates that this deposit was formed by a rare combination of events, with storms acting on a nesting ground. This discovery supports colonial nesting behavior and potential nesting site fidelity in the Pterosauria.

Anhanguera taxonomy revisited: is our understanding of Santana Group pterosaur diversity biased by poor biological and stratigraphic control?

BACKGROUND: Anhanguerids comprise an important clade of pterosaurs, mostly known from dozens of three-dimensionally preserved specimens recovered from the Lower Cretaceous Romualdo Formation (northeastern Brazil). They are remarkably diverse in this sedimentary unit, with eight named species, six of them belonging to the genus Anhanguera. However, such diversity is likely overestimated, as these species have been historically diagnosed based on subtle differences, mainly based on the shape and position of the cranial crest. In spite of that, recently discovered pterosaur taxa represented by large numbers of individuals, including juveniles and adults, as well as presumed males and females, have crests of sizes and shapes that are either ontogenetically variable or sexually dimorphic. METHODS: We describe in detail the skull of one of the most complete specimens referred to Anhanguera, AMNH 22555, and use it as a case study to review the diversity of anhanguerids from the Romualdo Formation. In order to accomplish that, a geometric morphometric analysis was performed to assess size-dependent characters with respect to the premaxillary crest in the 12 most complete skulls bearing crests that are referred in, or related to, this clade, almost all of them analyzed first hand. RESULTS: Geometric morphometric regression of shape on centroid size was highly statistically significant (p = 0.0091) and showed that allometry accounts for 25.7% of total shape variation between skulls of different centroid sizes. Premaxillary crests are both taller and anteroposteriorly longer in larger skulls, a feature consistent with ontogenetic growth. A new diagnosis is proposed for Anhanguera, including traits that are nowadays known to be widespread within the genus, as well as ontogenetic changes. AMNH 22555 cannot be referred to "Anhanguera santanae" and, in fact, "Anhanguera santanae", "Anhanguera araripensis", and "Anhanguera robustus" are here considered nomina dubia. DISCUSSION: Historically, minor differences in crest morphology have been used in the definition of new anhanguerid species. Nowadays, this practice resulted in a considerable difficulty in referring well-preserved skulls into known taxa. When several specimens are analyzed, morphologies previously believed to be disparate are, in fact, separated by a continuum, and are thus better explained as individual or temporal variations. Stratigraphically controlled excavations on the Romualdo Formation have showed evidence for faunal turnover regarding fish communities. It is thus possible that some of the pterosaurs from this unit were not coeval, and might even represent anagenetic morphotypes. Unfortunately, amateur collecting of Romualdo Formation fossils, aimed especially at commerce, resulted in the lack of stratigraphic data of virtually all its pterosaurs and precludes testing of these further hypotheses.

Eggshell and Histology Provide Insight on the Life History of a Pterosaur with Two Functional Ovaries.

The counterpart of a previously described non-pterodactyloid pterosaur with an egg revealed the presence of a second egg inside the body cavity of this gravid female. It clearly shows that pterosaurs had two functional oviducts and demonstrates that the reduction of one oviduct was not a prerequisite for developing powered flight, at least in this group. Compositional analysis of one egg suggests the lack of a hard external layer of calcium carbonate. Histological sections of one femur lack medullary bone and further demonstrate that this pterosaur reached reproductive maturity before skeletal maturity. This study shows that pterosaurs laid eggs even smaller than previously thought and had a reproductive strategy more similar to basal reptiles than to birds. Whether pterosaurs were highly precocial or needed parental care is still open to debate.

An Early Cretaceous pterosaur with an unusual mandibular crest from China and a potential novel feeding strategy.

The Aptian Jiufotang Formation of northeast China is a Konservat Lagerstätte particularly rich in pterosaurs, notably azhdarchoids. Here we describe a new genus and species of toothed pteranodontoid pterosaur, Ikrandraco avatar gen. et sp. nov., based on two laterally flattened specimens. Ikrandraco avatar is diagnosed by a suite of features, including a very low and elongate skull, strongly inclined quadrate, and a deep, blade-like bony mandibular crest with a hook-like process on its posterior edge, an unusual structure so far unique to this taxon. The particular skull shape hints at a distinct feeding habit for pterosaurs that potentially includes temporary skimming and an extensible skin acting as a throat pouch that was more developed than in any other pterosaur known so far. The presence of two other taxa of purported piscivorous pterosaurs in the Jiufotang Formation suggests distinct resource exploitation in this part of China during the Early Cretaceous.

Sexually dimorphic tridimensionally preserved pterosaurs and their eggs from China.

BACKGROUND: The pterosaur record is generally poor, with little information about their populations, and pterosaur eggs are even rarer, with only four isolated and flattened eggs found to date. RESULTS: We report here a population of a new sexually dimorphic pterosaur species (Hamipterus tianshanensis gen. et sp. nov.), with five exceptionally well-preserved three-dimensional eggs, from the Early Cretaceous deposit in northwestern China. About 40 male and female individuals in total were recovered, but the actual number associated might be in the hundreds. All of the discovered skulls have crests, which exhibit two different morphologies in size, shape, and robustness. The eggs show pliable depressions with cracking and crazing on the outer surface. The eggshell, observed by scanning electron microscopy and energy-dispersive spectroscopy, comprises a thin calcareous external hard shell followed by a soft membrane. CONCLUSIONS: These fossils shed new light on the reproductive strategy, ontogeny, and behavior of pterosaurs. The cranial crests show sexually dimorphic morphologies, with presumed males and females differing in crest size, shape, and robustness. Ontogenetic variation is reflected mainly in the expansion of the rostrum. The eggs have some external rigidity of the general pliable eggshell, and the microstructure of the eggshell is similar to that of some modern "soft" snake eggs. We suggest that this new pterosaur nested in colonies and thus exhibited gregarious behavior, a possible general trend for at least derived pterodactyloid pterosaurs.

Taxonomic review of the Ornithocheirus complex (Pterosauria) from the Cretaceous of England.

Over a decade after the last major review of the Cambridge Greensand pterosaurs, their systematics remains one of the most disputed points in pterosaur taxonomy. Ornithocheiridae is still a wastebasket for fragmentary taxa, and some nomenclatural issues are still a problem. Here, the species from the Cretaceous of England that, at some point, were referred in Ornithocheirus, are reviewed. Investigation of the primary literature confirmed that Criorhynchus should be considered an objective junior synonym of Ornithocheirus. Taxonomic review of more than 30 species known from fragmentary remains showed that 16 of them are undiagnosable (nomina dubia): Palaeornis cliftii, Cimoliornis diomedeus, Pterodactylus compressirostris, Pterodactylus fittoni, Pterodactylus woodwardi, Ornithocheirus brachyrhinus, Ornithocheirus carteri, Ornithocheirus crassidens, Ornithocheirus dentatus, Ornithocheirus enchorhynchus, Ornithocheirus eurygnathus, Ornithocheirus oxyrhinus, Ornithocheirus scaphorhynchus, Ornithocheirus tenuirostris, Ornithocheirus xyphorhynchus, and Pterodactylus sagittirostris. Fourteen species are considered valid, and diagnoses are provided to all of them: Ornithocheirus simus, Lonchodraco giganteus comb. n., Lonchodraco machaerorhynchus comb. n., Lonchodraco(?) microdon comb. n., Coloborhynchus clavirostris, 'Ornithocheirus' capito, Camposipterus nasutus comb. n., Camposipterus(?) sedgwickii comb. n., Camposipterus(?) colorhinus comb. n., Cimoliopterus cuvieri comb. n., 'Ornithocheirus' polyodon, 'Ornithocheirus' platystomus, 'Pterodactylus' daviesii, and 'Ornithocheirus' denticulatus. These species are referred in the genera Ornithocheirus, Lonchodraco gen. n., Coloborhynchus, Cimoliopterus gen. n., and Camposipterus gen. n., but additional genera are probably present, as indicated by the use of single quotation marks throughout the text. A cladistic analysis demonstrates that Anhangueridae lies within a newly recognized clade, here named Anhangueria, which also includes the genera Cearadactylus, Brasileodactylus, Ludodactylus, and Camposipterus. The anhanguerian 'Cearadactylus' ligabuei belongs to a different genus than Cearadactylus atrox. Lonchodraconidaefam. n. (more or less equivalent to LonchodectidaesensuUnwin 2001) is a monophyletic entity, but its exact phylogenetic position remains uncertain, as is the case of Ornithocheirus simus. Therefore, it is proposed that Ornithocheiridae should be constricted to its type species and thus is redundant. Other taxa previously referred as "ornithocheirids" are discussed in light of the revised taxonomy.