Climate influences bill shape diversification in cavity-excavating birds

Abstract

The remarkable structural and functional diversity of the avian bill serves as an ideal system to understand how ecological and environmental factors influence morphological diversification under physically demanding tasks. For example, in cavity-excavating birds where the bill experiences tremendous physical stresses, climate and habitat affect the mechanical properties of available nesting substrates and therefore can potentially influence the shape and performance of bills. Few studies have focused on the entire avian bill, a complex structure consisting of the rhamphotheca and bony core of the upper and lower mandibles, which may evolve as independent modules or as a single integrated unit. Here, we examined patterns and drivers of bill shape diversification in barbets using micro-computed tomography of museum study skins. We employed landmark-based geometric morphometrics and phylogenetic comparative methods to study the influence of climatic conditions, integration and phylogenetic constraints on bill shape diversification. Asian and African barbets have explored distinct maxillary shape spaces without corresponding change in mandibular shape after correcting for phylogenetic non-independence. Additionally, maxillary shape for both rhamphotheca and bony components was significantly correlated with climate variables and exhibited signatures of allometric scaling. All four bill components, however, covaried with each other and have evolved in a gradual and integrated fashion, exhibiting late-stage shape disparity. Through these findings, our study offers crucial insights into how ecological behaviors impact morphological evolution of complex, multifunctional features.

Bill shape imposes biomechanical tradeoffs in cavity-excavating birds

“…A similar finding was reported in a study on the functional implications of edentulism in the therizinosaur Erlikosaurus andrewsi , where finite element analysis demonstrated that the presence of a keratinous rhamphotheca enhanced the stress dissipation ability of the skull for different biting scenarios (22). Thus, our study reveals a functional synergy underlying the integrated diversification of the rhamphotheca and bony modules in barbet bills (31).…”

“…Second, the geometry, excavation performance and behavior of barbet bills may be affected by the mechanical properties of available nesting substrates. African barbets, which occupy drier climatic regimes, exhibit deeper maxillae on average compared to the Asian barbets, which typically reside in more humid, forested regions (31, 32). Because climatic factors like temperature, precipitation and hydrological conditions affect wood decay rates and wood density, we surmise that they may also influence the availability of dead and decaying wood in the habitat (46, 47).…”

“…Study skins for these species were loaned from the Field Museum of Natural History in Chicago and the American Museum of Natural History in New York (see Table 1 for a list of specimens). For each species, we chose the micro-computed tomography (µCT) scan of one specimen from a dataset that we collected for another study (refer to Chhaya et al 2022 for a detailed description of scanning procedures) (31). Scans were selected on the basis of quality (intactness of the bill and absence of dirt or other extraneous material in the scans) for meshing, processing and simulation.…”

“…Scans were selected on the basis of quality (intactness of the bill and absence of dirt or other extraneous material in the scans) for meshing, processing and simulation. Because much of the bill shape diversification in Asian and African barbets has been driven by changes in maxillary shape (31), we focused on studying the effect of maxillary geometry on performance during cavity excavation. To obtain the three-dimensional and multilayered structures of barbet maxillae for finite element analysis, we imported micro-CT scans into Amira 6 (ThermoFisher Scientific, Waltham, Massachusetts, USA) as DICOM image stacks, where we manually segmented them.…”

“…During the initial stages of cavity excavation, barbets typically employ two excavation techniques -a pecking action which involves an impact along the dorsoventral axis, and a gouging action which involves torsional loading along the longitudinal axis (27)(28)(29)(30). The Asian and African barbets occupy different regions of bill shape morphospace, with African barbets generally possessing more convex maxillae with greater depth compared to the narrower and pointed maxillae of the Asian barbets (31). The diversity of bill shapes and excavation behaviors in these birds thus offers an excellent opportunity to comparatively explore the relationships between morphology, behavior and functional performance.…”