Maja Mielke

Dexterous manipulation of objects relies on precise coordination between anatomical elements. In seed-eating birds, seeds are manipulated and dehusked using both the beak and tongue, but the functional roles and coordination of these structures remain unresolved. Here, we quantified the 3D movements of the upper beak, lower beak, tongue, and seed in a hard-biting and a weak-biting songbird species using X-ray Reconstruction of Moving Morphology (XROMM) and measured contractile properties of their primary jaw muscles. We show that the tongue serves as the main tool for seed rotation, transport, and stabilization. Multi-dimensional, high-frequency movements of the upper and lower beaks reveal that efficient seed processing depends on high mobility of the kinetic avian skull. Strong and weak biters differ in feeding kinematics and jaw muscle speeds, suggesting ecological specialization of cranial mechanics. The complexity, precision, and tight coordination of beak and tongue motions show that the avian cranium rivals the dexterity of the primate hand despite limited degrees of freedom.

Dexterous manipulation of objects relies on precise coordination between anatomical elements. In seed-eating birds, seeds are manipulated and dehusked using both the beak and tongue, but the functional roles and coordination of these structures remain unresolved. Here, we quantified the 3D movements of the upper beak, lower beak, tongue, and seed in a hard-biting and a weak-biting songbird species using X-ray Reconstruction of Moving Morphology (XROMM) and measured contractile properties of their primary jaw muscles. We show that the tongue serves as the main tool for seed rotation, transport, and stabilization. Multi-dimensional, high-frequency movements of the upper and lower beaks reveal that efficient seed processing depends on high mobility of the kinetic avian skull. Strong and weak biters differ in feeding kinematics and jaw muscle speeds, suggesting ecological specialization of cranial mechanics. The complexity, precision, and tight coordination of beak and tongue motions show that the avian cranium rivals the dexterity of the primate hand despite limited degrees of freedom.

Oropharyngeal food processing exhibits a remarkable diversity among vertebrates, reflecting the evolution of specialised ‘processing centres’ associated with the mandibular, hyoid, and branchial arches. Although studies have detailed various food‐processing strategies and mechanisms across vertebrates, a coherent and comprehensive terminology is lacking. Here, we provide a synthesis, including a unified terminology for the intricate complexity of vertebrate oropharyngeal processing. Among gnathostomes, mandibular food processing predominates, ranging from discrete bites to rhythmic, cyclic chewing facilitated by precise tongue mechanics in aquatic and terrestrial environments alike. By contrast, some taxa have abandoned oropharyngeal processing entirely, relying instead on post‐oesophageal strategies such as gastric milling and chemical digestion. Interestingly, teleost (bony) fishes illustrate the evolutionary trade‐off between increased jaw protrusion for prey capture and reduced mandibular processing capacity. They compensated for this trade‐off by developing derived processing behaviours early in their evolutionary development. Through the re‐evolution of mandibular chewing, they succeeded in utilising all three known processing centres. Mastication is a specialised, dimensionally complex form of unignathic mandibular chewing (i.e. chewing restricted to the lower jaw) exclusive to mammals. However, our findings demonstrate that dimensionally complex forms of mandibular chewing have arisen independently multiple times and are widespread among gnathostomes. Notably, diverse taxa, including elasmobranch stingrays, Australian lungfish, sirenid salamanders, various songbirds, herbivorous turtles, and the tuatara, exhibit complex jaw movements combining arcuate, longitudinal, and sometimes transverse components enabled by specialised jaw joints, suspensions, and intracranial motions (‘cranial kinesis’). From a comparative, functional–morphological perspective, mammalian mastication may best be characterised as dimensionally complex chewing mediated by the secondary or temporomandibular joint. By contrast, analogous dimensionally complex non‐mammalian chewing involving motions confined to the primary or quadrate–articular jaw joint qualifies as pseudomastication. Both mastication and pseudomastication resemble functional masticatory behaviours, while those incorporating intracranial motions and movements of the jaw suspension belong to distinct categories. Our anatomical analysis highlights the convergent evolution of dimensionally complex chewing among gnathostomes and emphasises the importance of comprehensive studies on jaw development and function to deepen our understanding of the evolution of oropharyngeal processing.

Many songbird species rely on seeds as a primary food source and the process of picking up, positioning, cracking, dehusking and swallowing seeds is one of the most sophisticated tasks of the beak. Still, we lack understanding about how granivorous songbirds move their beak during the different phases of seed processing. In this study, we used multi-view high-speed imaging to analyze the 3D movement of the beak in feeding domestic canaries. Our analysis focused on the correlation of the upper and lower beak, the frequency of mandibulation and the direction of mandible movement in 3D space. We show that the correlation of maxilla and mandible movement differs among the phases of seed processing. Furthermore, we found that the beak moves at extremely high frequencies, up to 25 Hz, which resembles previously reported maximal syllable rates in singing canaries. Finally, we report that canaries use specific 3D mandible movements during the different phases of seed processing. Kinematic parameters do not differ between male and female canaries. Our findings provide an important biomechanical basis for better understanding the beak as a functional tool.

Digitization of video recordings often requires the laborious procedure of manually clicking points of interest on individual video frames. Here, we present progressive tracking, a procedure that facilitates manual digitization of markerless videos. In contrast to existing software, it allows the user to follow points of interest with a cursor in the progressing video, without the need to click. To compare the performance of progressive tracking with the conventional frame-wise tracking, we quantified speed and accuracy of both methods, testing two different input devices (mouse and stylus pen). We show that progressive tracking can be twice as fast as frame-wise tracking while maintaining accuracy, given that playback speed is controlled. Using a stylus pen can increase frame-wise tracking speed. The complementary application of the progressive and frame-wise mode is exemplified on a realistic video recording. This study reveals that progressive tracking can vastly facilitate video analysis in experimental research.

Sciuromorpha (squirrels and close relatives) are diverse in terms of body size and locomotor behavior. Individual species are specialized to perform climbing, gliding or digging behavior, the latter being the result of multiple independent evolutionary acquisitions. Each lifestyle involves characteristic loading patterns acting on the bones of sciuromorphs. Trabecular bone, as part of the bone inner structure, adapts to such loading patterns. This network of thin bony struts is subject to bone modeling, and therefore reflects habitual loading throughout lifetime. The present study investigates the effect of body size and lifestyle on trabecular structure in Sciuromorpha. Based upon high-resolution computed tomography scans, the femoral head 3D inner microstructure of 69 sciuromorph species was analyzed. Species were assigned to one of the following lifestyle categories: arboreal, aerial, fossorial and semifossorial. A cubic volume of interest was selected in the center of each femoral head and analyzed by extraction of various parameters that characterize trabecular architecture (degree of anisotropy, bone volume fraction, connectivity density, trabecular thickness, trabecular separation, bone surface density and main trabecular orientation). Our analysis included evaluation of the allometric signals and lifestyle-related adaptation in the trabecular parameters. We show that bone surface density, bone volume fraction, and connectivity density are subject to positive allometry, and degree of anisotropy, trabecular thickness, and trabecular separation to negative allometry. The parameters connectivity density, bone surface density, trabecular thickness, and trabecular separation show functional signals which are related to locomotor behavior. Aerial species are distinguished from fossorial ones by a higher trabecular thickness, lower connectivity density and lower bone surface density. Arboreal species are distinguished from semifossorial ones by a higher trabecular separation. This study on sciuromorph trabeculae supplements the few non-primate studies on lifestyle-related functional adaptation of trabecular bone. We show that the architecture of the femoral head trabeculae in Sciuromorpha correlates with body mass and locomotor habits. Our findings provide a new basis for experimental research focused on functional significance of bone inner microstructure.