Suction feeding biomechanics of Polypterus bichir: investigating linkage mechanisms and the contributions of cranial kinesis to oral cavity volume change

Many fishes use substantial cranial kinesis to rapidly increase buccal cavity volume, pulling prey into the mouth via suction feeding. Living polypterids are a key lineage for understanding the evolution and biomechanics of suction feeding due to their phylogenetic position and unique morphology. Polypterus bichir have fewer mobile cranial elements compared to teleosts (e.g., immobile [pre]maxillae) but successfully generate suction through dorsal, ventral, and lateral oral cavity expansion. However, the relative contributions of these motions to suction feeding success have not been quantified. Additionally, extensive body musculature and lack of opercular jaw opening linkages make P. bichir of interest for examining the role of cranial vs. axial muscles in driving mandibular depression. Here we analyze the kinematics of buccal expansion during suction feeding in P. bichir using X-Ray Reconstruction of Moving Morphology (XROMM) and quantify the contributions of skeletal elements to oral cavity volume expansion and prey capture. Mouth gape peaks early in the strike, followed by maximum cleithral and ceratohyal rotations, and finally by opercular and suspensorial abductions, maintaining the anterior-to-posterior movement of water. Using a new method of quantifying bones’ relative contributions to volume change (RCVC) we demonstrate that ceratohyal kinematics are the most significant drivers of oral cavity volume change. All measured cranial bone motions, except abduction of the suspensorium, are correlated with prey motion. Lastly, cleithral retraction is largely concurrent with ceratohyal retraction and jaw depression while the sternohyoideus maintains constant length, suggesting a central role of the axial muscles, cleithrum, and ceratohyal in ventral expansion.

The feeding system of Tiktaalik roseae: an intermediate between suction feeding and biting

Changes to feeding structures are a fundamental component of the vertebrate transition from water to land. Classically, this event has been characterized as a shift from an aquatic, suction-based mode of prey capture involving cranial kinesis to a biting-based feeding system utilizing a rigid skull capable of capturing prey on land. Here we show that a key intermediate, Tiktaalik roseae, was capable of cranial kinesis despite significant restructuring of the skull to facilitate biting and snapping. Lateral sliding joints between the cheek and dermal skull roof, as well as independent mobility between the hyomandibula and palatoquadrate, enable the suspensorium of T. roseae to expand laterally in a manner similar to modern alligator gars and polypterids. This movement can expand the spiracular and opercular cavities during feeding and respiration, which would direct fluid through the feeding apparatus. Detailed analysis of the sutural morphology of T. roseae suggests that the ability to laterally expand the cheek and palate was maintained during the fish-to-tetrapod transition, implying that limited cranial kinesis was plesiomorphic to the earliest limbed vertebrates. Furthermore, recent kinematic studies of feeding in gars demonstrate that prey capture with lateral snapping can synergistically combine both biting and suction, rather than trading off one for the other. A “gar-like” stage in early tetrapod evolution might have been an important intermediate step in the evolution of terrestrial feeding systems by maintaining suction-generation capabilities while simultaneously elaborating a mechanism for biting-based prey capture.

Anatomy and morphometry of the skull of Amazona aestiva (Linnaeus, 1758; Psittaciformes, Aves)

Obtaining craniometric data is key to establishing parameters that can help in the anatomic identification and understanding of species. The aim of the present study was to establish the craniometric data and describe the main skull bones and structures of Amazona aestiva, which has become common in veterinary clinics, originated from the legalized purchase or trafficking of animals. A total of 20 adult specimens were used, donated for studies by the Paraíba Wild Animal Screening Center (Centro de Triagem de Animais Silvestres da Paraíba (CETAS-PB)/IBAMA-PB, Brazil. The skulls were dissected and macerated with water. First were identified the frontal, maxilla, mandible, nasal, jugal and quadrate bones that served as a base to identify other bone structures that were then compared with the skull of other bird species already described in the literature, especially psitacids. Values were obtained by measuring with a digital pachymeter, and the maximum skull length was 63.0 mm, the maximum width 33.0 mm and the rhamphotheca was 33.8 mm long. No significant differences were observed between males and females and well developed cranial kinesis was a remarkable characteristic of the species. The data obtained serve as a base to identify and characterize the species. These data can also aid in the clinic, imaging and veterinary surgery.

The impact of allometry on vomer shape and its implications for the taxonomy and cranial kinesis of crown-group birds

Crown birds are subdivided into two main groups, Palaeognathae and Neognathae, that can be distinguished, among others, by the organization of the bones in their pterygoid-palatine complex (PPC). Shape variation to the vomer, which is the most anterior part of the PPC, was recently analysed by Hu et al. (2019) with help of geometric morphometrics to discover morphological differences between palaeognath and neognath birds. Based on this study, the vomer was identified as sufficient to distinguish the two main groups (and even more inclusive neognath groups) and their cranial kinetic system. As there are notable size differences between the skulls of palaeognaths and neognaths, we here investigate the impact of allometry on vomeral shape and its implication for taxonomic classification by re-analysing the data of the previous study. Different types of multivariate statistical analyses reveal that taxonomic identification based on vomeral shape is strongly impaired by allometry, as the error of correct identification is high when shape data is corrected for size. This finding is evident by a great overlap between palaeognath and neognath subclades in morphospace. The correct identification is further influenced by the convergent presence of a flattened vomeral morphotype in multiple neognath subclades. As the evolution of cranial kinesis has been linked to vomeral shape in the original study, the existing correlation between shape and size of the vomer across different bird groups found in the present study questions this conclusion. In fact, cranial kinesis in crown birds results from the loss of the jugal-postorbital bar in the temporal region and ectopterygoid in the PPC and the combination of a mobilized quadrate-zygomatic arch complex and a flexible PPC. Therefore, we can conclude that the vomer itself is not a suitable proxy for exploring the evolution of cranial kinesis in crown birds and their ancestors.

Origin of the avian predentary and evidence of a unique form of cranial kinesis in Cretaceous ornithuromorphs

The avian predentary is a small skeletal structure located rostral to the paired dentaries found only in Mesozoic ornithuromorphs. The evolution and function of this enigmatic element is unknown. Skeletal tissues forming the predentary and the lower jaws in the basal ornithuromorph Yanornis martini are identified using computed-tomography, scanning electron microscopy, and histology. On the basis of these data, we propose hypotheses for the development, structure, and function of this element. The predentary is composed of trabecular bone. The convex caudal surface articulates with rostromedial concavities on the dentaries. These articular surfaces are covered by cartilage, which on the dentaries is divided into 3 discrete patches: 1 rostral articular cartilage and 2 symphyseal cartilages. The mechanobiology of avian cartilage suggests both compression and kinesis were present at the predentary–dentary joint, therefore suggesting a yet unknown form of avian cranial kinesis. Ontogenetic processes of skeletal formation occurring within extant taxa do not suggest the predentary originates within the dentaries, nor Meckel’s cartilage. We hypothesize that the predentary is a biomechanically induced sesamoid that arose within the soft connective tissues located rostral to the dentaries. The mandibular canal hosting the alveolar nerve suggests that the dentary teeth and predentary of Yanornis were proprioceptive. This whole system may have increased foraging efficiency. The Mesozoic avian predentary apparently coevolved with an edentulous portion of the premaxilla, representing a unique kinetic morphotype that combined teeth with a small functional beak and persisted successfully for ∼60 million years.

Compared Cranial Osteology of Species of Leptoptilus (Lesson, 1831) (Aves, Ciconiidae)

The species of the Ciconiidae family (Ciconiiformes), commonly known as storks, exhibit a cosmopolite distribution, being represented by swamp birds of medium and large size. The present work aimed to describe minutely and comparatively the cranial osteology of Leptoptilus species. The study was performed based on the description of cranial bones of the species Leptoptilus dubius, L. crumeniferus, and L. javanicus. The studied specimens were previously prepared (dry crania and mandibles). Among the studied characteristics, it was possible to observe some structures of systematic importance, such as the zygomatic process, the temporal fossa, the ectethmoid, the superior maxilla, the quadrate bone that interconnects the palate, the neurocranium, and the mandible, performing a key role in the work of cranial kinesis. Leptoptilus javanicus possesses, in the lateral portion of the cranium, an emargination of the rostrodorsal edge of the postorbital process, not observed in either Leptoptilus dubius or Leptoptilus crumeniferus. The fossa ventralis possesses a projection in the caudal extremities in L. dubius and L. crumeniferus, which is absent in L. javanicus. The transpalatine process is present in both L. dubius and L. crumeniferus and is absent in L. javanicus. The pterygoid process of the palatine is short in both L. dubius and L. crumeniferus, and long in L. javanicus. The ectethmoid is reduced in both L. dubius and L. javanicus, whereas in L. crumeniferus, besides being more developed, it presents a “U” shape. Based on the present study, L. dubius and L. crumeniferus are phylogenetically closer to each other than L. javanicus.

Evolution of the vomer and its implications for cranial kinesis in Paraves

Most living birds exhibit cranial kinesis—movement between the rostrum and braincase—in which force is transferred through the palatal and jugal bars. The palate alone distinguishes the Paleognathae from the Neognathae, with cranial kinesis more developed in neognaths. Most previous palatal studies were based on 2D data and rarely incorporated data from stem birds despite great interest in their kinetic abilities. Here we reconstruct the vomer of the Early Cretaceous stem bird Sapeornis and the troodontid Sinovenator, taxa spanning the dinosaur–bird transition. A 3D shape analysis including these paravians and an extensive sampling of neornithines reveals their strong similarity to paleognaths and indicates that morphological differences in the vomer between paleognaths and neognaths are intimately related to their different kinetic abilities. These results suggest the skull of Mesozoic paravians lacked the kinetic abilities observed in neognaths, a conclusion also supported by our identification of an ectopterygoid in Sapeornis here. We conclude that cranial kinesis evolved relatively late, likely an innovation of the Neognathae, and is linked to the transformation of the vomer. This transformation increased palatal mobility, enabling the evolution of a diversity of kinetic mechanisms and ultimately contributing to the extraordinary evolutionary success of this clade.