Exceptional preservation and foot structure reveal ecological transitions and lifestyles of early theropod flyers

The ecology of early theropod flyers remains a topic of significant interest. Previous research has explored their anatomy, diet, locomotor abilities, and habitats, providing partial insights into their lifestyles. However, a comprehensive understanding requires a detailed analysis of their foot anatomy, a crucial indicator of ecological roles in modern birds. The diverse foot morphologies of extant birds reflect a wide range of ecological roles, including leg-based launch, perching, wading, swimming, prey capture, and dismemberment. This study aims to refine our understanding of early theropod flyer ecology by focusing on their foot anatomy, leveraging exceptionally preserved specimens and advanced imaging techniques. The specific objectives are to compare the toe pads, foot scales, claws, and joints of early theropod flyers with those of modern birds and to integrate this new data with existing ecological data to better understand the evolutionary trajectory of ecological roles in the context of flight development.

Existing literature on the ecology of early theropod flyers has focused on diverse aspects such as anatomy, diet, locomotor capabilities (including flight and terrestrial locomotion), and habitat analysis. While these studies have provided important insights into the lifestyles of these extinct creatures, they often lack a comprehensive analysis of foot morphology and its relationship with ecological roles. Studies on modern bird foot anatomy have demonstrated a strong correlation between foot morphology (toe pads, scales, claw shape, joint structure) and ecological preferences. For instance, the shape and arrangement of toe pads have been linked to perching, ground-dwelling, and predatory behaviors. Similarly, scale types and claw morphometrics provide information about locomotor styles and prey handling techniques. The existing body of work on fossil evidence provides a background against which this research will analyze the evolution of the bird foot and thus reveal the ecological behaviors of the extinct creatures.

This study examined over 1000 fossils of early theropod flyers from the Shandong Tianyu Museum of Nature, using laser-stimulated fluorescence (LSF) to reveal soft tissue details not visible under white light. Twelve specimens with preserved toe pads, foot scales, and claws were selected for detailed analysis, representing various early flyer taxa such as *Anchiornis*, *Confuciusornis*, *Sapeornis*, *Yanornis*, and *Microraptor*. Additional specimens of *Ambopteryx* and *Fortunguavis*, and *Archaeopteryx* (Berlin and Thermopolis specimens) were included using existing data. The study employed both qualitative and quantitative methods. Qualitatively, the arrangement and morphology of toe pads and scales were assessed. Quantitatively, traditional morphometrics was used to analyze claw shape and size, using measurements of toe length, relative digit size, and claw curvature. These morphometric data were analyzed using principal component analysis (PCA) and linear discriminant analysis (LDA) to separate taxa by ecological categories defined by the morphometrics of modern birds. The modern bird datasets for the comparative analyses used podothecae of 15 modern bird of prey species and 21 species of non-predatory birds, along with claw data from 61 crown bird families. The analyses involved creating separate datasets with and without digit I measurements to account for incomplete fossil preservation.

The study found a remarkable diversity in foot morphology among early theropod flyers. *Microraptor*, a non-avialan flyer, exhibited the most raptorial characteristics, suggesting a specialized aerial hunting lifestyle, unlike any modern bird analog within the Jehol Biota. Its protrusive toe pads and strongly ginglymoid joints indicate a high capacity for grasping and restraining prey, consistent with a restraining raptorial behavior inferred from previous studies. *Anchiornis* displayed adaptations suggestive of a primarily terrestrial lifestyle, with well-developed toe pads indicating raptorial capabilities but weaker flight capabilities and less specialized adaptations for capturing volant prey. *Archaeopteryx* specimens showed less recurved claws than most modern birds, hinting at a unique ecology with no clear modern analogue, with varying interpretations based on the specimens. *Confuciusornis* showed evidence of a generalist lifestyle, based on claw morphology and existing data on its jaws and habitat. *Sapeornis*, despite being herbivorous, showed traits usually associated with grasping, possibly reflecting an ecologically complex lifestyle involving supplementary meat consumption. *Fortunguavis* demonstrated characteristics consistent with a non-raptorial perching lifestyle. *Yanornis*, with its mesarthrally arranged toe pads, suggests less efficient grasping and a primarily ground-dwelling ecology supported by its straight claws and presumed fish-based diet from the existing literature. The study highlighted the ecological diversity among early theropod flyers, with early Jurassic forms showing primarily ground-dwelling lifestyles, followed by a diversification into more aerial roles in the Early Cretaceous. *Microraptor*'s specialized niche emphasized that non-avian flyers filled specialized predatory roles in ecosystems, roles now primarily occupied by birds.

The findings address the research question by revealing the diverse ecological strategies of early theropod flyers. The transition from primarily ground-dwelling lifestyles in the Jurassic to more diverse aerial and terrestrial roles in the Cretaceous is strongly supported. The remarkable specialization of *Microraptor* as a unique aerial predator during the Early Cretaceous is significant, suggesting that non-avian flyers played crucial roles in Mesozoic ecosystems that have since been taken over by avian predators. The different ecological profiles of *Archaeopteryx* and *Sapeornis* highlight the unusual complexity of some early bird ecologies. The generalist nature of *Confuciusornis* suggests adaptability to fluctuating environments. The study's implications extend to our understanding of avian evolution, suggesting a more complex interplay between flight evolution and ecological diversification than previously understood. The presence of both specialists and generalists among early flyers suggests that early specialist flyers might have been more vulnerable to extinction events compared to their generalist counterparts.

This study demonstrates that the foot morphology of early theropod flyers reveals a surprising diversity of ecological strategies, challenging previously held assumptions about their lifestyles. The results highlight the significance of integrated approaches combining advanced imaging techniques with comparative morphometrics to reconstruct the ecology of extinct organisms. Future research could focus on expanding the dataset to include additional taxa and refining the ecological categories used in the LDA and PCA to better explore the ecological niches of early theropod flyers. A more detailed analysis of the taphonomy of soft tissue preservation and how it influences measurements could also be beneficial.

The study's interpretations are based on preserved fossils, which may not fully represent the entire population's range of variation. The limited preservation of soft tissues in some specimens constrained the analyses. While the methodology attempted to mitigate potential biases from incomplete preservation, the possibility of some undetected biases exists. The ecological categories used in the comparative analyses relied on modern bird species, which may not perfectly reflect the ecological diversity of the Mesozoic. The study only used the claw curvature, toe pad arrangement, and joint ginglymoidy to infer ecological habits, while many other parameters could contribute to the ecological habit of early theropod flyers.