Biomechanics illuminates form–function relationships in bird bills

At its core, comparative biomechanics is a conceptually broad discipline, examining biological systems through the lens of physics. The form of any organism dictates both its response to stressors or external forces, and its interactions with the fluid environment (Vogel, 2011). For example, the muscles of various organisms perform critical movements, and the relative lengths of the input and output lever arms determine whether they perform better at generating forces or at rapid movements (Ritchie, 1954). The simple task of obtaining food presents a staggering diversity of mechanical solutions to the same problem, each with its own associated constraints on other functions. Form–function trade-offs enable examination of evolution in a mechanistic context, particularly for structures with great morphological variety and functional diversity (Arnold, 1983; Higham et al., 2021). In addition to biomimetic inspiration, the simple concepts of comparative biomechanics have transformed our inquiry and examination of the natural world.

The advent of high-speed videography for kinematics (Hedrick, 2008) and micro-computed tomography (micro-CT; James, 2017), together with computational techniques such as finite element analysis (Anderson et al., 2012; Brassey et al., 2013; Bright, 2014; Maas et al., 2012; Polly et al., 2016; Rayfield, 2007; Richmond et al., 2005; Ross, 2005), has proved transformative in comparative biomechanics. Here, I illustrate how this burgeoning field has revolutionized our understanding of the natural world, using the avian bill as a case study. The bill is a morphologically diverse multifunctional appendage (Rico-Guevara et al., 2019a) whose study spans material and fluid biomechanics, ecology, evolutionary biology and neuroscience. Biomechanics is critical to the function of diverse bill shapes in the over 10,000 species of birds (Fig. 1), from those that must withstand the stresses of cracking hard seeds (Olson, 2014; Schluter et al., 1985; Smith, 1987) and head-on impacts (Chhaya et al., 2022a preprint; Lee et al., 2014), to those whose shape reduces drag on movement through fluids (Crandell et al., 2019; Martin and Bhushan, 2016). Bill shape also influences how fluid moves through them, as exemplified by their role in vocalization (Podos et al., 2004; Riede et al., 2016; Trevisan and Mindlin, 2009). Recent studies suggest that trade-offs and constraints have exerted a potent influence on bill evolution (Navalón et al., 2019, 2020), and others suggest that certain key bill traits may be tightly linked to function, such that certain unrelated taxa converge on a similar bill morphology (Pigot et al., 2020). Here, I illustrate, using examples from the above topics, how bill mechanics influence diverse functions, emphasizing general principles to be gleaned from comparative study. Bird bills serve other functions (including preening and visual signalling); here, I primarily illustrate how a biomechanical perspective informs form–function studies on bird bills, and thus biological structures in general.

Birds have long played an important role in the art and customs of human civilization, with illustrations dating back to the Paleolithic. Illustrators of birds, from those behind cave paintings and Egyptian tombs to the Mughal courts of India and Western scientists such as Linnaeus (Linnaeus, 1758), have used bird bills as a defining anatomical trait. The sexes of the extinct huia (Heteralocha acutirostris) of New Zealand were originally described as separate species because of dramatically different bill shapes and foraging niches (Buller, 1870). Studying bill shape has proved highly consequential in our understanding of evolution and speciation. Darwin's initial examinations of Galapagos finches (Darwin, 1839) led to the influential later studies of David Lack, Robert Bowman and Peter and Rosemary Grant (Lack, 1947; Bowman, 1961; Grant and Grant, 2006). These studies drew an important mechanistic link between bill morphology and diet, and thus to the probability of survival in harsh environmental conditions. Birds with bills that could crack tougher seeds were more likely to survive food scarcity, shifting the morphology of the population. In parallel, the spectacular adaptive radiation of the Hawaiian honeycreepers was scientifically described in the late 19th century. In spite of their extraordinary divergence in bill morphology, careful examination revealed that they shared a common ancestor (Amadon, 1950; Perkins, 1901).

The twentieth century saw a movement from museum-based natural history toward observations of animals and their behaviour in the wild. This led to an interest in functional morphology, beginning with D'Arcy Thompson's landmark On Growth and Form, which integrated mathematical analyses into morphology (Thompson, 1917). In the latter half of the twentieth century, the functional and mechanical consequences of different forms and feeding strategies received much interest. By then, experiments on human bone identified mechanical response properties to a range of stresses (Evans, 1957; Koch, 1917). Further, comparative anatomy was increasingly blended with mechanical and engineering considerations in the study of biomechanics (Beecher, 1962). Dempster used free-body diagrams to examine forces acting on the human body (Dempster, 1961). Free-body diagrams proved useful as a static (or quasi-static) depiction of the mechanical function of the bill (Bowman, 1961). Although nowadays replaced by finite element models (which enable us to study the distribution of stresses on the bill), the free-body diagram still enables comparison of diverse bill shapes and feeding techniques (Korzun et al., 2003, 2008; Pêgas et al., 2021) (Fig. 2). Walter Bock provided an excellent example of applying this approach to a wide range of bill shapes (Bock, 1966). He treated the jaws of birds as rigid bodies rotating about a pivot, in this case the quadrate bone articulation, whose rotation propels the jaw open. Bock simplified the problem of jaw closing to include the force required and the length of the lever arm. This sets the stage for much of our discussion in upcoming segments, where most mechanical actions performed by the bill can be understood in this simple physical context. The limitations of assuming symmetric loading on the bill and the need to characterize all moving parts of the lever before using free-body diagrams must be acknowledged here, and Bock's work highlighted how a careful analysis of anatomy and natural history must precede any biomechanical analysis. The advance of his model over previous studies was in considering the movement or kinesis of the bill, as well as material inhomogeneity in the bony structures (Bock, 1966). Whereas Hofer examined loads only at the bill tip (Hofer, 1945), Bock examined static loads at various points along the tomium and added an analysis of torques and stress trajectories, introducing the concept of mechanical trade-offs in bill function. In nature, being very good at one function often comes at the expense of another. Sensitivity and resolution trade off against each other in sensory organs, and speed and manoeuvrability typically trade off against each other in flying animals. Bills are no exception to this, and specializations for a certain function result in deficits in others. This has ecological consequences, driving increasing specialization from a ‘generic’ bill morphology, and potentially restricting species to certain niches.

Rapid technological progress tremendously impacted comparative studies of the bill. Modern high-speed videography enables us to quantify how birds move their bills when interacting with solids or fluids (Riede et al., 2006; Van Der Meij and Bout, 2006). The ease and precision of 3D kinematic analysis, coupled with experimental measures of bite force (Herrel et al., 2005, 2009), enables us to verify the static measurements of earlier anatomical models. Further, we can now quantify material properties at small spatial scales using nano-indentation (Bonser and Witter, 1993; Seki et al., 2005, 2010). Using 3D printing, biological samples can now be replicated and mechanically tested. Thus, we may examine both microscale toughness and fracture properties in biological materials (Fig. 2). Energy-dispersive X-ray spectroscopy provides the mineral composition of materials, which influences their mechanical properties. Where bill materials are available, bending experiments and the use of digital speckle pattern interferometry and digital image correlation enable us to perform in vitro compressive testing (Soons et al., 2012a), thus integrating laboratory research with field-based natural history.

These advances in biomechanics have been accompanied by major advances in computation, with its attendant analytical power and processing speeds to handle large volumes of data. This has led to renewed interest in macroevolutionary morphological studies on bird bills, particularly based on museum specimens (Cooney et al., 2017; Navalón et al., 2019; Pigot et al., 2020). In addition, CT provides 3D morphological data, and we may virtually dissect and study relevant structures of both extant and extinct species (James, 2017; Lautenschlager et al., 2013). Finite element analysis helps us examine stresses and their transmission patterns across 3D geometries, incorporating information on material properties as well (Fig. 2) (Soons et al., 2010, 2012b, 2015). Finally, computational fluid dynamics, coupled with kinematic data, enables analysis of complex interactions of solid objects such as bills with surrounding fluid media (Crandell et al., 2019). This fusion of older and newer tools perhaps well deserves the name ‘integrative biology’, and informs my subsequent examination of bill form and function.

The avian bill consists of a bony maxilla and mandible with an outer keratinous rhamphotheca. The dorsal surface of the maxilla is called the culmen, whereas the ventral surface of the mandible is called the gonys. The meeting point of the maxilla and mandible, where most food handling and processing occurs, possesses a ridged biting surface called the tomium. In the absence of teeth, force application by the bill occurs at the tomium, and the rhamphotheca enables stress dissipation synergistically with bone (Lautenschlager et al., 2013; Seki et al., 2005). The keratin of the rhamphotheca is a structurally rigid, glycine-rich 15.5 kDa monomer with a high indentation hardness, representing an impact- and abrasion-resistant material (Bonser, 1996; Frenkel and Gillespie, 1976; Homberger and Brush, 1986; Wang et al., 2016). In many species, keratin forms overlapping scales that are attached to each other and layered over the bone, which may help enhance strength (Hieronymus and Witmer, 2010; Lee et al., 2014; Piro, 2022; Seki et al., 2005).

The discovery of feathered theropod dinosaurs demonstrated that birds evolved by edentulism (loss of teeth) from a toothed theropod ancestor, a feature retained by early avialans together with a rhamphotheca (Miller et al., 2020; Zheng et al., 2020). Genetic switches which reduced the development of dentition may have simultaneously keratinized the outer epidermis of the jaws to form the rhamphotheca (Louchart and Viriot, 2011), a trend seen in turtles and pterosaurs (Beccari et al., 2021; Bestwick et al., 2018; Osi et al., 2011). In non-avian theropods, edentulism coupled with a keratinous rhamphotheca has evolved independently in multiple groups, concomitant with a widespread trend toward herbivory (Lautenschlager et al., 2013; Ma et al., 2017; Meade and Ma, 2022; Norell et al., 2001; Wang et al., 2017; Zanno and Makovicky, 2011). Composite bill structures resist fracturing better than homogeneous materials, and a finite element analysis of the therizinosaur Erlikosaurus andrewsi demonstrated that the rhamphotheca considerably lowered stresses on the jaw during biting (Lautenschlager et al., 2013). Altogether, herbivory may have been a key driver in the evolution of keratinized bills.

However, in early birds, the process of edentulism and the evolution of a lightweight bill was accompanied by a spectacular diversification of shapes and functions (Cooney et al., 2017; Louchart and Viriot, 2011). These massive shape changes are driven by the Bmp4 and calmodulin gene pathways (Abzhanov et al., 2004, 2006), among others (Bhullar et al., 2015). The diversity of functions and specializations in the bill represent adaptations to distinct ecological niches, each shape exerting its own biomechanical constraints. Below, I discuss these trade-offs from the biologist's perspective, focusing on the link between form and function to examine the insights we now have from decades of research on the bill.

Solid biomechanics seeks to understand the resistance of materials to stresses (tensile, compressive or shear) that might cause deformation or fracture. Materials resist or dissipate stress in diverse ways, influenced by their ultrastructure or their geometry (Wainwright, 1992). The jaws of vertebrates experience both compressive and shear stresses during feeding (Therrien et al., 2005). Bills are subject to an additional constraint: being lightweight to support flight. A series of jaw muscles control cranial kinesis of both upper and lower jaws (the upper jaw bends at the nasofrontal hinge). The relative sizes of these muscles and the bones that they attach to determine the force generated by the bill, and the resultant stresses that the bill must withstand. Forces generated by jaw muscles are transmitted via flexibly articulated bones (the quadrate, jugal and pterygoid), which move the jaws (Bock, 1966; Hoese and Westneat, 1996). This facilitates cranial kinesis during diverse tasks such as feeding, singing, etc. In paleognathous birds (ratites), the upper bill is rhynchokinetic, i.e. can bend only at more distal positions (Gussekloo and Bout, 2005). Using the knowledge that bone performs well under compression or tension but relatively poorly under shear, Bock (1966) estimated that the nasofrontal hinge of a crow skull could resist ∼110–175 N forces in compression, but only ∼65–90 N in shear forces.

Bock (1966) also conducted a detailed examination of the structure of bone within the bill in relation to the stress trajectories experienced during loading. He found that areas of higher compressive stress (crowding of stress trajectories) coincided with the presence of compact bone, whereas areas with lower stress possessed spongy, lightweight trabecular bone. Trabecular bone importantly provides resistance to bending stresses (Seki et al., 2005). Again, the trade-off is evident; strength to perform one function may result in structural weakness in others, and also trade off against weight (critical for a flying bird). The combination of bony materials renders the avian bill robust yet lightweight, even without considering the keratinous rhamphotheca (Bock, 1966).

Bird bills also serve as a probing tool where loads emerge from moving the bill against dense mud or into crevices in tree trunks, as a head-butting implement where compressive stresses result from contact between two birds, as a seed-cracker where massive forces must be exerted in order to crush tough seeds, and as a chisel used to excavate holes in wood, just to name a few of their diverse functions. Many functions impose great physical demands on the bill, and hypertrophied jaw and neck muscles perform the work of actuating the bill against a substrate (Deeming et al., 2022; Heckeberg et al., 2021; Van Der Meij and Bout, 2008). These forces could easily fracture the bill if the resultant stresses are not dissipated. If the bill is approximated to a simple cylindrical beam loaded either axially (as during pecking) or transversely (as during biting), one might consider the stress trajectories as radiating dorsoventrally and posteriorly from the point of contact, eventually approaching the base of the skull and braincase, and it is thus critical for some dissipation to occur (Brassey et al., 2013). In their simplest form, these forces may be represented as buckling stress (predicted under Euler's Law) and shear stress (Chhaya et al., 2022a preprint), each of which could result in material failure when they cross a critical threshold.

The bill could theoretically, therefore, be highly susceptible to fracture or buckling during physically demanding tasks. How do bird bills support these demanding functions, and yet remain lightweight enough for flight? The keratinized rhamphotheca over the trabecular ‘spongy’ bone appears to represent a key step in the evolution of lightweight, fracture-resistant bills. This ‘sandwich’ composite structure lowers stresses experienced by the bill during compressive or shear loading, and stops fracture propagation before it reaches the bony layers of the bill. Fracture of the keratin occurs by scale displacement when strains are lower, and the scales themselves fail at higher strains (Genbrugge et al., 2012; Seki, 2009; Seki et al., 2005, 2010; Soons et al., 2012b). Wear and tear of the rhamphotheca thus protects the bony portions of the bill from injury (Hieronymus and Witmer, 2010; Lee et al., 2014). In addition to strength arising from the synergistic effects of a composite structure, bills may further be reinforced by the incorporation of minerals and pigments into the rhamphotheca. Melanin increases the hardness of keratin, thereby improving its resistance to fracture and particularly abrasion (Bonser and Witter, 1993). By increasing the abrasion resistance of bills, birds may compensate to some degree for damage over time, eventually replacing the keratin to provide a new surface. This presents advantages over teeth, which cannot be replaced. Further, the bill of the Toco toucan (Ramphastos toco) contains mineral deposits which increase the Young's modulus (Seki et al., 2005). Bird bill keratin normally contains calcium phosphate (hydroxyapatite) (Pautard, 1963). Mineralization increases material hardness, as in insect mandibles and ovipositors where zinc enrichment improves resistance to material stresses (Gundiah and Jaddivada, 2020). However, this field still largely operates outside of the ecological context of bill use, and eco-mechanical studies relating behaviour and morphology to the biochemical structure of bills represent an important frontier for future research.

Of course, the individual components of the bill ultimately give rise to distinct bill geometries (Al-Mosleh et al., 2021), which strongly influence stresses experienced during feeding or other functions (Rayfield, 2011), and thus bill shape evolution (Olsen, 2017; Reddy et al., 2012). Simply put, a thin, slender bill will not be very efficient at cracking hard seeds. This requires both musculature and a bill surface (tomium) that can generate high pressures, and a wide, deep bill that can withstand the resultant compressive and shear stresses (Field, 2019; Herrel et al., 2005; Soons et al., 2010). For example, the massive bill of the extinct Hawaiian honeycreeper Chloridops kona could crack seeds of the naio Myoporum sandwicense, which required forces in excess of 400 N (Olson, 2014; Perkins, 1893), and the finches Pyrenestes ostrinus (146 N force) and Coccothraustes coccothraustes (>400 N force) similarly feed on extremely tough materials (Sims, 1955; Smith, 1987, 1990). Such forces no doubt result in significant compressive and shear stress, particularly at the tomium, and may have driven repeated evolution of massive bills in finches, exemplified by Crithagra concolor of São Tomé (Melo et al., 2017). In contrast, the bills of the Hawaiian honeycreepers Rhodacanthis palmeri (now extinct) and Loxioides bailleui serve(d) to cut bean pods of Acacia koa and Sophora chrysophylla, respectively, rather than crush seeds (Perkins, 1893).

In seed-crushing bills, high bite force risks fracturing the bone. Bite forces are often higher toward the rear of the bill, but the fracture point owing to increased shear stress sets a constraint on the maximum force the bill can exert, and muscles, head and jaw-closing apparatus appear arranged to accommodate these constraints (Carril et al., 2015; Genbrugge et al., 2011; Rao et al., 2018; Soons et al., 2010, 2015). Bowman concluded that either a heavily curved bill or one with a thickened base could potentially support fracture resistance during seed cracking (Bowman, 1961). In the decurved bill of a cardinal (Cardinalis cardinalis), increased bill depth increases the moment arm of the force generated by the muscles, and hence torque, leading to increased bite force. Simultaneously, the bill withstands shear stresses at the base. The deep bill of the evening grosbeak (Coccothraustes vespertinus) exerts high compression with low shear (Bock, 1966). Bowman's (1961) and Bock's (1966) studies served as a prelude to Grant and Grant's (2006) study of the ecological consequences of bill shape, which informed our understanding of evolution. Recent studies using finite element analysis have found that the deep and wide bills of several species of Darwin's finches exhibit enhanced stress dissipation (Genbrugge et al., 2012; Herrel et al., 2005; Soons et al., 2010, 2015). Bill morphology in seed-eating birds supports resource partitioning, seed selection and surviving scarcity of food, further demonstrating how comparative biomechanics informs evolutionary biology (Abbott et al., 1975; Benkman and Pulliam, 1988; Foster et al., 2008; Grant and Grant, 2006; Hespenheide, 1966; Kear, 1962; Schluter et al., 1985; Smith, 1987, 1990; Willson, 1972).

In general, bills that are ‘buttressed’ or reinforced both dorsoventrally and mediolaterally perform well under compressive loads. These specializations impose trade-offs on other functions. For a given input arm length, a shorter output lever arm is important to increase mechanical advantage and thus generate greater force (Fig. 3). It thus stands to reason that a bill that cracks hard seeds, such as that of a parrot or finch, is also shorter in the dimension of length (Bock, 1966; Homberger, 2003). However, this geometric configuration potentially prioritizes force over jaw-closing velocity (Corbin et al., 2015; Herrel et al., 2009), which can impact a number of other behaviours. Birds with slender bills, such as insectivores that catch moving prey, prioritize closing velocity (or the velocity ratio), and thus possess longer output lever arms relative to input lever arms (Beecher, 1962; Lederer, 1975). Cracking of seeds in finches often also involves lateral movement of the bill, and the extent of this lateral movement differs between greenfinches (Chloris chloris) (with a lower husking time and a larger lateral movement) and Java sparrows (Padda oryzivora) (Van Der Meij and Bout, 2006; Van Der Meij et al., 2004). Crossbills (Loxia) use their unique bills in a lateral motion to open pine cones (Benkman, 1993), and specialization for mediolateral strength putatively reduces dorsoventral bite force. Analysis of kinematics and bite force coupled with finite element models and nanoindentation will help us better understand how bills withstand both compressive and shear stresses, and whether they trade off between dorsoventral and mediolateral strength (Fig. 2). Additionally, XROMM (X-ray reconstruction of moving morphology) technology provides a way to quantify the actions of the jaw musculature (Dawson et al., 2011), which in turn will help better understand the lever biomechanics employed to generate different kinds of forces.

Raptors, for example, use their thick hooked bills to tear into flesh, a process that requires both high pressure and resistance to torsional bending. The bills of raptors are evolutionarily integrated with the skull, putatively to withstand these stresses, and thus exhibit mainly allometric variation (Bright et al., 2016), also seen in other animal groups (Bright et al., 2019; Felice et al., 2019; Fritz et al., 2014; Goswami et al., 2014). Integration was probably crucial in the evolution of the diverse bill shapes (Tokita et al., 2007; Yamasaki et al., 2018) of lineages such as the Hawaiian honeycreepers (Navalón et al., 2020; Tokita et al., 2016). However, not all predatory bills operate in the same way as those of raptors. The extinct predatory Andalgalornis possessed a bill that was relatively weak mediolaterally, and may have instead delivered slashing bites to weaken larger prey (Degrange et al., 2010). Another extinct bird, Gastornis (Diatryma) was capable of high dorsoventral bite force, and could potentially crack bones or tough vegetable matter (Mustoe et al., 2012; Witmer and Rose, 1991). The latter was also suggested by the sharp-edged bill of the herbivorous New Zealand moa Anomalopteryx, which performed better for dorsoventral loads in finite element analysis (Attard et al., 2016). A similar ecological role on the Hawaiian islands may have been performed by the anatid Chelychelynechen, with a similar ‘turtle jaw’ (James and Burney, 1997). In contrast, the relatively broad, weak bill of the moa genus Euryapteryx may have handled softer food (Attard et al., 2016). Beam theory suggests similar functions in theropod jaws that are weak mediolaterally, with high dorsoventral strength putatively indicating cutting or slashing feeding mechanisms (Therrien et al., 2005). The success of these mechanisms in birds, along with the stress resistance provided by the rhamphotheca, may have been key morphological innovations leading to modern bird diversity.

Lastly, serrations or tomial ‘teeth’ occur in many taxa, and may enable birds to hold on to prey (locally increasing the pressure applied by the bill) (Sustaita and Rubega, 2014), to tear off fruit (Short and Horne, 2001) or leaves (Marshall, 1951), or in nectar feeding (Ornelas, 1994; Rico-Guevara and Rubega, 2017), but in general have received little study. Potential study taxa in this important frontier area include the pigeon Didunculus strigirostris of Samoa, the raptor Harpagus bidentatus, several African barbets (including Lybius bidentatus) and the bowerbird Scenopoeetes dentirostris. Hooked bills, by contrast, are widespread among birds with diverse diets such as the kingfisher Melidora macrorrhina, the vangid Vanga curvirostris, the bulbul Setornis criniger and the flowerpiercers, Diglossa. In loggerhead shrikes (Lanius ludovicianus), hooks and projections increase the bite pressure at the expense of overall bite force, which is probably important for a predatory feeder that handles diverse living prey (Sustaita and Rubega, 2014). These serrations or hooks are often outgrowths of the keratinous rhamphotheca, and may not always be reflected in the underlying bone; for example, the keratinous lamellae are comb-like outgrowths of the bill seen in filter-feeding anatids and flamingos, which help retain prey and expunge extraneous material (Jenkin, 1957; Kooloos et al., 1989; Li and Clarke, 2016). The bony pseudoteeth of the extinct Hawaiian anatids Thambetochen and Ptaiochen present the opposite scenario, and probably supported a herbivorous diet (James and Burney, 1997).

Bills serve many additional functions, such as thermoregulation (Friedman et al., 2019; Tattersall et al., 2009, 2017; Van De Ven et al., 2016), which imposes biomechanical constraints on feeding and other functions. Several non-dietary functions of the bill also involve significant physical stresses. The lightweight, yet hardened casques of hornbills serve many functions, including display, thermoregulation, and aerial jousting in species such as the helmeted hornbill Buceros vigil (Earl of Cranbrook and Kemp, 1995; Kinnaird et al., 2003; Seki et al., 2010). Some species of hummingbirds ‘duel’ with clashing bill tips, and their pointed bills may have evolved for combat purposes (Rico-Guevara and Araya-Salas, 2015).

One of the most physically demanding tasks performed by bird bills is excavating into wooden substrates. Birds such as woodpeckers and barbets may excavate hollows for nesting and roosting, or in search of food. On the island of Hawai'i, the ʻakiapōlāʻau (Hemignathus munroi), whose lower mandible is a broadened, chisel-like structure, can hammer away bark from tree limbs in search of insects or sap. The curved, slender maxilla is used as a probe to extract insect larvae from crevices in the wood (Pejchar and Jeffrey, 2004; Perkins, 1893; Ralph and Fancy, 1996). The prong-billed barbet (Semnornis frantzii) of Central America possesses a unique ‘forked’ mandible, that it apparently employs to bite out pieces of wood during cavity excavation (Skutch, 1944). However, relatively little biomechanical study has focused on the interaction of bills with wooden substrates. In woodpeckers, the most well-known cavity excavators, powerful neck muscles drive the head forward and into the substrate at high acceleration rates and with considerable force (Fig. 4A) (Bock, 1999; Spring, 1965). Although the absorption of impact shocks by the cranium (or potentially the lack thereof) has been examined in multiple studies (Ganpule et al., 2020; Jung et al., 2019; Liu et al., 2017; Schuppe et al., 2021; Wang et al., 2011; Van Wassenbergh et al., 2022; Yoon and Park, 2011; Zhu et al., 2012), the bill material itself has received little study. The composite arrangement of the bill, the presence of overlapping keratin scales and microscopic wavy sutures, and the low porosity of bill bone are all likely to help dissipate impact stresses without fracture (Lee et al., 2014).

In cavity excavation, as with other bill functions, geometry exerts an additional influence on stress dissipation. Barbets, which are closely related to woodpeckers, also excavate cavities for nesting and roosting (Fig. 4B), employing both pecking and gouging actions, which result in compressive and shear stresses (torsion), respectively. Preliminary analyses suggest that deeper bills resist impact forces better, whereas longer, narrower bills perform better (lower peak von Mises stress) under torsional loads, and composite bill structures typically exhibit lower stresses (Chhaya et al., 2022a preprint). Differences in material properties of the excavation substrate may be key to understanding bill evolution and function in cavity excavators (Chhaya et al., 2022b preprint). Examining the mechanical properties of excavation substrates will thus provide a holistic understanding of bill function in these contexts.

Finally, many bird groups (for example, kingfishers and jacamars) dig into soft soil in search of food or during the construction of nesting hollows (Morgan and Glue, 1977; Skutch, 1968). This behaviour is distinct from probe feeding, which I discuss in more detail below. In kingfishers, the broad bills of Clytoceyx rex and Melidora macrorrhina are apparently used for digging into dirt (Bell, 1981). The forces experienced by these bills remain to be modelled, and presumably involve resistance to abrasion experienced during digging. The unique wrybill (Anarhynchus frontalis), with its bill bent to one side (Conklin et al., 2019), could similarly provide interesting data on how a relatively slender bill resists potentially abrasive stresses when searching for food under rocks.

Thus far, I have treated bill geometry and material properties from the perspective of solid biomechanics. However, the shape of the bill simultaneously influences interactions with fluids. The bill is a potentially important source of drag when flying or underwater (Estrella and Masero, 2007), and lateral compression (being deeper than they are wide) suggests a reduction in profile drag during flight. Perhaps the best example of this is seen in kingfishers, wherein species that dive for food (plunge divers) possess distinctly narrowed, aerodynamically streamlined bill shapes. These bill shapes are distinct from those of terrestrial, ground-feeding kingfishers, and potentially trade-off mechanical advantage for reduced profile drag in water (Crandell et al., 2019; Eliason et al., 2020). Surface-feeding birds such as skimmers (Rynchops) experience significant drag, and the keratinized rhamphotheca of the lower jaw exhibits a series of ‘riblets’ or corrugations oriented at an angle to the flow experienced by the bill. These reduce pressure drag, thus enabling the mandible to be trailed along the surface of the water while the bird flies above it and catches food items at the surface (Martin and Bhushan, 2016).

The properties and structure of a bill also influences how fluids move through it, and this is particularly relevant during vocalization, where vibrations are transmitted through the fluid and emitted by the bill (Trevisan and Mindlin, 2009). As the most peripheral vocal structure, the bill is a critical coupling device to match the acoustic impedance of the vocal tract to that of the outside environment (Bradbury and Vehrencamp, 2011). However, the acoustic mechanics of the bill remain chronically understudied compared with other vocal structures (Riede and Goller, 2014), probably because of the difficulty in obtaining mechanistic data. Many studies measure correlations between bill morphology and parameters of emitted sound, with divergent results (Demery et al., 2021; Derryberry et al., 2012; Laiolo and Rolando, 2003; Langin et al., 2017; Podos, 2001; Porzio et al., 2019; Slabbekoorn and Smith, 2000). Mechanistic studies taking advantage of XROMM and acoustic finite element analysis, coupled with the use of CT scans and microphone arrays, are necessary to help address how peripheral vocal structures shape the emitted sound. The little we know suggests fascinating parallels to human speech, where lip and tongue movements influence the properties of emitted sound. Birds dynamically alter the resonant properties of the vocal tract by changing bill gape and moving the tongue, thereby emphasizing different frequencies (Hoese et al., 2000; Riede et al., 2006; Suthers et al., 2016). This is subject to the force–velocity trade-off discussed earlier. Because birds with thicker, seed-crushing bills cannot close and open them as fast, they often produce lower-frequency, slower songs (Podos et al., 2004). Alternatively, by closing the bill entirely, many birds can seal off the vocal tract, thereby forcing sound into a distinct amplification system that produces more resonant sounds (Riede et al., 2016). Finally, the aperture shape (bill shape and bill gape) of the sound-emitting structure influences the shape and directionality of the radiating sound wave. Although acoustic radiation patterns have received much study in bats and dolphins in the context of echolocation, there are very few studies on birds (Cornec et al., 2017; Dantzker et al., 1999; Patricelli et al., 2007, 2008; Yorzinski and Patricelli, 2010). The bill may also serve as a waveguide and resonator, creating interference patterns through casques (Alexander et al., 1994) or as sound leaks between gaps in a closed bill, which then shape the frequency properties and radiation patterns of emitted sound. In bats, gaps between teeth shape biosonar beam patterns (Lee et al., 2017). The diversity of emitter geometries in birds presents an incredibly fertile ground for future research, bringing together ecologists and engineers in interdisciplinary collaborations with potential biomimetic applications. This frontier area in comparative biomechanics will additionally provide mechanistic insight into acoustic form and function.

The bill also serves as a fluid-handling device, particularly for nectarivores such as hummingbirds (Rico-Guevara et al., 2019b). Serrations and keratinous prong-like structures on the bill, together with a narrowing near the distal tip, may help transfer nectar from the tongue to the bill (Rico-Guevara and Rubega, 2017). In addition, the bill performs various functions to help draw in fluids. Measures of wettability, viscosity and surface tension of fluids imbibed by the bill will help us better understand the mechanics of the bill during nectar feeding, and hummingbirds are an ideal system for such a study on account of their diverse bill shapes. Recent research shows that simple capillary action does not explain the nectar feeding of birds such as hummingbirds, and demonstrates the crucial role probably played by the bill in offloading nectar from the tongue and in generating suction forces to draw nectar to the back of the oral cavity (Cuban et al., 2022). Hummingbirds also use their bills in territorial combat, where rigid, pointed bills perform better. However, this trades off with feeding functions, as these bill morphologies may not perform as well at imbibing and offloading nectar. The same is true of keratinous serrations, which may improve nectar offloading if pointed forward, but may serve a combat function if oriented towards the rear (Rico-Guevara et al., 2019b). Hummingbirds possess flexible bills that support probing into flowers with complex shapes, and also enable insect capture to supplement their diet (Smith et al., 2011; Yanega and Rubega, 2004). The extraordinary bill of the sword-billed hummingbird, Ensifera ensifera, the result of coevolution with Passiflora flowers (Lindberg and Olesen, 2001), is so long that the bird has to use its feet to preen. However, great length and flexibility are liabilities during combat, as impact stresses are more likely to cause buckling. This is therefore an interesting case where the solid biomechanics and material rigidity of the bill trade off against its efficiency as a fluid-handling system. For most functions of bills, therefore, there exist apparent biomechanical trade-offs, as well as diverse bird taxa which could provide important insights in a comparative study.

A more nascent discipline in comparative biomechanics is examining the mechanical properties of sensory organs (Sane and McHenry, 2009). Many structures that interact with either fluids or solids contain sensors whose structure enables them to detect various forces. Load-bearing structures contain load sensors, whereas other sensors detect pressure differences in fluids. Here, too, the bill presents fascinating opportunities for study. Diverse bird groups use their bills to probe for invertebrates in soft mud or leaf litter, probably derived from an initial pecking mode of feeding (Gerritsen and Meiboom, 1986; Zweers and Gerritsen, 1997). Mechanosensors on the bill tip detect pressure changes near or at the bill surface (Fig. 5) (Du Toit et al., 2020; Piersma et al., 1998; Schneider et al., 2014). These mechanosensors are similar functionally to those found in many reptiles, either extant or inferred in fossils by the presence of neurovascular foramina, which may have helped them to probe in mud or capture fish in water (Barker et al., 2017; Carr et al., 2017; Foffa et al., 2014; Ibrahim et al., 2014; Martill et al., 2021; Soares, 2002). Mechanosensors may also help detect loads during seed cracking or pressure changes around the bill that support filter feeding (Avilova et al., 2018; Demery et al., 2011; Gottschaldt, 1974; Gottschaldt and Lausmann, 1974). The extinct anatid Talpanas lippa from Kaua'i possessed an enlarged trigeminal foramen, suggesting that its bill took on a somatosensory function at the expense of vision (Iwaniuk et al., 2009), similar to the platypus (Home, 1802). The most specialized bill tip organs, though, have evolved convergently in three groups of birds: Threskiornithidae (ibises and spoonbills), Scolopacidae (snipes, woodcocks, sandpipers, godwits and curlews) and the paleognathous Apterygidae (kiwis) (Cunningham et al., 2013). In these species, foramina at the tip of the bony portion of the bill contain sensors known as Herbst corpuscles organized into sensory pits (Cunningham et al., 2007, 2010a). These detect pressure differences and vibrations borne through substrates, and enable birds to locate wriggling worms or other prey without direct contact (‘remote touch’) or other cues (Cunningham et al., 2010b; Piersma et al., 1998). Ibises foraging in wetter substrates possess more pits with fewer Herbst corpuscles each, whereas species foraging in drier substrates possess fewer pits with more Herbst corpuscles each (du Toit et al., 2022). The structure and distribution of these sensors may support efficient directional localization as well as discrimination between different kinds of stimuli (Cunningham et al., 2007; Piersma et al., 1998), and these mechanosensory cues are necessary and sufficient for feeding (Cunningham et al., 2010b).

Mechanosensory systems within the bill close the loop between bill biomechanics and control via neural mechanisms, and are thus another important frontier area of future research into bills. Such research has the potential to inform remotely guided robotics, but also offers an evolutionary understanding of how different physical forces have shaped bill morphology. In particular, the Scolopacidae possess considerable diversity in bill shape and foraging mechanisms (Nebel et al., 2005). The probing Numenius curlews, Arenaria turnstones and the unique spoon-billed sandpiper, Calidris pygmaea, possibly convergent with the threskiornithid spoonbills (Platalea), all highlight the need for comparative study of Herbst corpuscle responses to distinct stimuli, generated by different feeding mechanisms.

The examples and concepts I have discussed above highlight both the diversity and multifunctionality of the avian bill, and the role biomechanics has played in understanding bill function. We now have a broad understanding of how geometry and material properties of the bill influence its strength and performance in diverse tasks. Other evolutionary pressures also act on bill structure (e.g. visual signalling, behaviour and thermoregulation), all of which merit further research. This Review instead uses examples where an integrative perspective transforms our understanding of bill function. As technology progresses, future areas of research include understanding the interplay between the material biomechanics of the bill and its interactions with moving fluids (air and water), the role of sensory control in dictating the kinematics of bill use, and its biomimetic potential in developing robust yet lightweight materials. In spite of recent progress, much remains to be understood about how geometry influences the use of the bill in tasks other than feeding, representing another fertile area for future study. These questions are general to almost any problem in biomechanics, and may help address a wide range of interdisciplinary research questions.

I thank Vaibhav Chhaya for discussions, Umesh Srinivasan, Seshadri KS, Abhijeet Rasal, Taksh Sangwan, Sutirtha Lahiri and Arpit Omprakash for photographs, and Prof. Monica Daley and two anonymous reviewers for their constructive feedback.