Biomechanics of biting in loggerhead shrikes: jaw-closing force, velocity and an argument for power Free

Birds are often touted for their evolutionary lock-and-key fits between their beaks and diets, thanks in large part to insights gleaned from Darwin's finches (e.g. Bowman, 1961). However, over the past few decades an awareness of the selective forces acting on beak form and function beyond the context of feeding (e.g. vocalization, preening, nest-building, climbing, etc.) has surged (Rico-Guevara et al., 2019; Krishnan, 2023; Young et al., 2023). Even within the context of feeding, many birds face conflicting demands on their form and function: hummingbirds honed for nectarivory have flexible jaws that facilitate insectivory (Yanega and Rubega, 2004); ducks with specialized filter-feeding morphologies employ different feeding mechanics for grazing on grass (Van der Leeuw et al., 2003); and scrub jays in mixed pine–oak woodland have bill shapes that are intermediate between those of pine versus oak woodland specialists (Bardwell et al., 2001). Different prey types clearly impose different physical demands. For example, several studies have demonstrated clear and direct positive relationships between bite force and food hardness (e.g. Wainwright, 1991; Herrel et al., 2001; Aguirre et al., 2002; and several others cited herein). Intuitively, with more evasive prey, such as insects, the opposite should also be true, i.e. increased speed and dexterity. Bock (1964) and Herrel et al. (2000) suggested that speed and kinesis are important for predators of active prey. However, characteristics favoring mobility and speed may trade-off against those favoring force and robustness, based on fundamental biomechanical principles of lever mechanics and muscle structure and function (Hildebrand and Goslow, 2001; Schenk and Wainwright, 2001; Vogel, 2001; Kardong, 2002; Herrel and Aerts, 2004). Such biomechanical trade-offs may translate into a trade-off between the ability to generate forces required to consume certain types of prey, and the speed required to procure them (Herrel et al., 2002, 2004; Corbin et al., 2015). Nevertheless, very little is known regarding how predators biomechanically and/or behaviorally navigate these disparate demands of their prey.

The loggerhead shrike (Passeriformes: Laniidae: Lanius ludovicianus) is a medium-sized (∼50 g) passerine that feeds on arthropods and vertebrates (Yosef, 2008), most noted for its characteristic prey impaling behavior (Yosef and Pinshow, 2005). Shrikes hunt primarily by waiting on high perches to attack their prey on ground-level substrates. Shrikes are also known to catch insect prey in the air, either by hawking them or by hovering (Yosef, 2008; Pavnov, 2011; D.S., personal observation). Scott and Morrison (1990, 1995) showed that shrikes are generalists with no explicit preferences for insect or vertebrate prey, whose diet seems to be influenced mostly by the relative abundance of prey items (Craig, 1978). Further support comes from conflicting studies such those of Slack (1975), who suggested that loggerhead shrikes prefer mice of smaller weight classes, and Miller (1931), who argued that shrikes prefer prey of larger mass. Scott and Morrison (1995) later argued on the basis of the metabolizable energy obtained from their primarily insect and vertebrate prey, that San Clemente loggerhead shrikes could not fully subsist on one type of prey or the other. Thus, shrikes must be flexible to accommodate all types (and sizes) of arthropod and vertebrate prey they might encounter.

Shrikes primarily use their beaks for procuring and dispatching their arthropod and vertebrate prey (Cade, 1967; Smith, 1973; Busbee, 1976; Craig, 1978; Olsson, 1984; Sustaita and Rubega, 2014; Sustaita et al., 2018). Insects, especially volant ones, are relatively small and evasive and their predators require greater jaw-closing speed (e.g. Lederer, 1975) and mandibular dexterity (e.g. Hull, 1991). Vertebrates might be comparatively less evasive, but because of their greater relative size, robustness and ability to fight back, their predators require greater strength (Cade, 1967; Sustaita and Rubega, 2014; Sustaita et al., 2018). Thus, differences in the physical and behavioral attributes of these prey types are likely to impose disparate demands of force and speed on shrikes (Sustaita and Rubega, 2014), rendering both bite force and jaw-closing velocity ecologically important for their feeding performance. However, biomechanical systems that are geared for force are often compromised for speed (and vice versa), because of the force–velocity trade-off inherent to musculoskeletal systems (Hildebrand and Goslow, 2001; Lieber and Ward, 2011).

The force–velocity trade-off exists at all levels of structural organization, from individual muscle fibers (Hill, 1938) to bone–muscle systems (Arnold et al., 2011), and naturally trickles up to performance (Herrel et al., 2009; Corbin et al., 2015; Irschick and Higham, 2016). Previous studies on granivorous birds have demonstrated trade-offs between bite force (e.g. for crushing seeds) and upper and lower jaw-closing velocities (e.g. for song production) (Herrel et al., 2009; Corbin et al., 2015; Irschick and Higham, 2016). These functional trade-offs are strongly determined by morphology. Wider and deeper jaws favor larger muscle attachments resulting in forceful bites, whereas gracile, longer jaws favor greater displacement resulting in faster jaw-closing speeds (Irschick and Higham, 2016). Furthermore, the perpendicular distances between lines of muscle action and upper and lower jaw joints (i.e. in-lever moment arms) also enforce these trade-offs, because for the same amount of muscle shortening, longer muscle moment arms result in a greater mechanical advantage, whereas shorter ones result in a greater distance advantage (Vogel, 2001). Potential trade-offs between the ability to generate bite forces required to consume and speeds required to apprehend more evasive prey might be mitigated by structural modifications in other elements of the feeding apparatus (e.g. Herrel et al., 2004). For example, Goyens et al. (2016) found that in stag beetles, the disproportionate increase in jaw length adaptive for winning intrasexual battles comes at the cost of decreased mechanical advantage, which, in turn, is met with a disproportionate increase in the jaw muscle in-lever moment arm. How predatory birds deal with prey that ostensibly require both jaw-closing force and speed remains an open question.

Shrikes have beak morphologies that are not particularly suited for generating especially high bite forces or high jaw-closing velocities in comparison to other passeriforms (e.g. Herrel et al., 2005a,b, 2009; Corbin et al., 2015; Irschick and Higham, 2016; Deeming et al., 2022), raptors (e.g. Sustaita, 2008; Sustaita and Hertel, 2010) and parrots (e.g. Carril et al., 2015; Dickinson et al., 2022). Their ‘raptorial’ features for carnivory have been well described (Schön, 1994; Cade, 1995), yet they are not so specialized as to impair their ability to process insects (Safriel, 1995). However, like other birds, shrikes have prokinetic skulls that allow elevation and depression of the upper bill about the craniofacial hinge (Movie 1), independent of the lower bill (Bramble and Wake, 1985; Hull, 1991; Zusi, 1993; Hoese and Westneat, 1996; Bout and Zweers, 2001; Bout, 2003; Gussekloo and Bout, 2005a,b; Meekangvan et al., 2006). Rotation/flexion of the upper beak has been shown to exhibit a range of 5–15 deg of angular displacement (Bout and Zweers, 2001; Van den Heuvel, 1992; Hoese and Westneat, 1996; Olsen and Westneat, 2016; Van Gennip and Berkhoudt, 1992; Zusi, 1967). A recent study measuring prokinesis in rosy-faced lovebirds observed an upper bill displacement of up to ∼40 deg (Young et al., 2023). Several plausible adaptive explanations have been advanced for avian prokinesis, many of which lack empirical support (Bock, 1964; Zusi, 1967; Bramble and Wake, 1985). Some have suggested that prokinesis enhances jaw speed (Klein et al., 1985; Herrel et al., 2000) or bite force (Zweers et al., 1997), or both (Bock, 1964; Herrel et al., 2000; Bout and Zweers, 2001). Others have commented on the role of prokinesis for enhancing coordinated movement of the jaws, facilitating bill dexterity (e.g. Bramble and Wake, 1985; Hull, 1991; Zusi, 1993; Bout and Zweers, 2001; Meekangvan et al., 2006), serving as a shock absorber to buffer external (e.g. woodpecker drilling) and internal (rapid jaw-closure) impacts (Bock, 1964; Lyons et al., 2023), facilitating retraction from substrates (Van Wassenbergh et al., 2022) and propelling the body during locomotion (Young et al., 2023). With regard to predatory feeding behavior, Bock (1964) suggested that the speed-enhancing qualities of prokinesis are important for insectivorous birds and, by extension, for killing small vertebrates, because of the kinetic energy imparted by fast-moving jaws. Hull (1991) also found qualitative differences in the degree of mobility of cranial and jaw elements between falcons that specialize on vertebrate (Falco peregrinus) and insect (Falco berigora) prey, and inferred that the increased robustness of the former, and greater mobility in the latter, might be associated with demands for increased strength and dexterity imposed by vertebrate and insect prey, respectively.

Whereas other studies have examined force–velocity relationships between behavioral contexts (e.g. feeding versus singing; Herrel et al., 2009; Corbin et al., 2015), we approached this by examining the relationship between jaw-closing force and velocity in the singular context of biting a force transducer to address three objectives: (1) to examine the relative roles of upper and lower bill movements (after Hoese and Westneat, 1996; Bout and Zweers, 2001; Gussekloo and Bout, 2005a,b) for generating jaw-closing forces and velocities; (2) to understand the relationship (i.e. trade-off) between bite force and jaw-closing velocity during biting (after Herrel et al., 2009; Corbin et al., 2015); and (3) to understand how biting power (bite force×jaw-closing velocity) relates to bite force and jaw-closing velocity among individual shrikes. Although power is a ubiquitous metric in studies of locomotion and muscle physiology (e.g. Irschick and Higham, 2016), it seems to enjoy comparatively less attention in the feeding literature. However, in some taxa, power is the most ecologically important variable for feeding success [e.g. chameleon lingual projection (Anderson, 2016), fish suction feeding (Camp et al., 2015), and mantis shrimp raptorial prey strikes (Patek, 2019)], and a similar argument might be made for predators of fast and formidable arthropod and vertebrate prey, such as shrikes.

We captured loggerhead shrikes (Lanius ludovicianus Linnaeus 1766) in two bouts of fieldwork between December 2010 and November 2011 in six general locations in California, USA (Sustaita and Rubega, 2014; Sustaita et al., 2014). Trapping and handling procedures are detailed in Sustaita and Rubega (2014), but to summarize, we systematically searched for shrikes by vehicle, and used the walk-in trap described by Craig (1997) baited with a live domestic mouse (Mus musculus) to capture them, one individual at a time. Upon capture, the shrikes were sexed, aged and weighed (to ±0.5 g using a 100 g-capacity Pesola spring scale), and a series of linear morphological measurements were taken with digital calipers (Absolute Digimatic, Mitutoyo) as detailed by Sustaita and Rubega (2014). Among these measurements, body mass and nalospi (the distance between the rostral end of the naris and the tip of the upper bill) were incorporated to account for potential differences in beak, head and body size. Nalospi was significantly correlated with total head length (from the rostral surface of the upper bill to the occipital protuberance of the caudal end of the head), based on a subset of individuals (n=29) for which total head length was also taken (r=0.77, P<0.0001). All procedures were conducted under state (California Department of Fish and Wildlife SCP, SC-11001) and federal (United States Geological Survey Bird Banding Laboratory Banding Subpermit, 22664-N; United States Fish and Wildlife Service Scientific Collecting Permit, MB232078-1) permits, and in accordance with University of Connecticut IACUC (#A09-040) regulations, as well as the Guidelines for the Use of Wild Birds in Research (http://www.nmnh.si.edu/BIRDNET/guide). We obtained bite force and corresponding kinematic measurements (see below) for n=51 shrikes [20 females, 31 males; 37 adults (‘after hatch year’, i.e. >1 year old), 14 juveniles (‘hatch year’, i.e. <1 year old)].

We used a custom-made force transducer (Sustaita and Rubega, 2014) based on a deformable strain gauge-type load cell (LCL-020 Omega Engineering, Inc.), connected to a data acquisition system (DAQ; OMB-DAQ 54 Omega Engineering). The default sampling rate of the DAQ was 4.6–4.7 Hz, and this was used for 21 of the subjects. For the remaining 30 subjects, the rate was increased to between 8.2 and 13.2 Hz to improve the resolution. A stainless-steel (upper) beam was mounted directly onto the load cell (Fig. 1), and another (lower) beam was affixed to the moveable end of a crescent wrench to accommodate different gape sizes, which was set to approximately half the maximal gape estimated for each individual bird, and so as to not allow the bite beams to come into contact with one another (Sustaita and Rubega, 2014). We calibrated the device to units of Newtons (N) before and after use by suspending weights at the bite point. This transducer design (Sustaita and Rubega, 2014) allows a greater range of displacement of the upper beam relative to the lower beam (and hence, the upper and lower bill tips) during jaw-closure (and force recording), which in turn allows for the measurement of velocity (see below). Shrikes were held by the body with one hand while the other hand stabilized the head and compelled the bird to bite the self-supported force transducer several times in succession, and force was continuously recorded over time, resulting in a ‘biting sequence’ (Movies 1 and 2) composed of individual ‘bites’ (i.e. individual acts of jaw-closure; ranging from 1 to 13, with a mean of 3.8 bites per sequence). An important methodological note is that the head was not fixed in space, but rather birds were able to orient their heads about the transverse axis in the parasagittal plane to some degree during jaw-closure. The outcome of this design limitation is that the upper and lower bill forces could not be isolated, as both the upper and lower jaws contributed to the bite forces measured.

Shrikes were filmed biting the force transducer (clamped to a support) in lateral view at 120 frames s⁻¹ with a Fujifilm Finepix HS10 digital camera, for the purpose of integrating kinetic and kinematic aspects of bite performance (after Reilly and Biknevicius, 2003; Anderson et al., 2008). The long axis of the bite beams was positioned orthogonal to the camera lens to ensure a lateral planar view for downstream 2-dimensional (2D) landmark tracking. Every effort was made to ensure that the shrikes bit the transducer with their heads in alignment with the long axis of the bite beams. Naturally, this was not perfectly controlled, and there is some degree of error in the measurements described below attributable to random variation in head orientation. Some degree of rotation of the head about the transverse axis (explained above) would not substantively affect the measurements. Head roll (i.e. rotation about the long axis of the head) was mostly restricted by the width of the lower bite beam (wider than the bill) when the tomial surface of the mandible was squared up and applied to it. Head yaw (i.e. rotation about the dorsoventral axis) could have the greatest effect on the measurements, so we performed a sensitivity analysis (after Lyons et al., 2023) to examine the potential effects of non-planar distance and angular measurements (Supplementary Materials and Methods and Fig. S1).

The landmarks tracked using ImageJ (Rasband, 2011) included: rictal commissure, rostral eye margin at the lore, vertex of the lore (to approximate the position of the craniofacial hinge), vertex of the tomial tooth, upper bill hook tip, and distal tip of mandible (Fig. 1A). Among these, the vertex of the lore position was the most subjective and variable (as evidenced by the comparatively low repeatability of the upper bill angle measurement derived from this point, see below). Furthermore, it was impossible to perfectly align this landmark with the underlying position of the osteological craniofacial hinge from the light camera images alone. However, based on our estimates of osteological craniofacial hinge positions of the birds we measured, landmark 3 of Fig. 1A fell within a radius of <2 mm (Supplementary Materials and Methods and Fig. S2). Two additional landmarks were tracked along the upper bite beam in each frame (Fig. 1A) to obtain measurements of tracking and measurement precision, as the s.d. of the marker-to-marker distances between two fixed points (after Brainerd et al., 2010). We used the length of the upper margin of the steel load cell mounting block (12.75 mm) as a reference to calibrate the image sequences in ImageJ.

The videos were tracked by two separate people after a focused training session to ensure consistency between them, with no apparent bias regarding which person tracked which videos. A landmark tracking repeatability analysis was performed (Supplementary Materials and Methods), although no explicit attempt was made to test for discrepancies between personnel. For each frame, we computed the bill tip-to-tip distance (BTD), gape angle, lower bill angle (LBA) and upper bill angle (UBA) from the 2D coordinates using Microsoft Excel trigonometric formulas. We then relativized the values to the position of the bills at initial contact with the bite beams, by subtracting each value (frame) from the value (frame) at which the bills first contacted the bite beams (Fig. 1; Movie 2). We note that these are inter-segmental angles computed relative to the position of the head. The kinematic profiles were smoothed with a low-pass 4th-order Butterworth filter (written by S. Van Wassenberg: https://www.uantwerpen.be/en/staff/sam-vanwassenbergh/my-website/excel-vba-tools/) prior to computing instantaneous jaw-closing velocities (dBTD/dT, where T is time) (Supplementary Materials and Methods). Finally, we measured the average angular velocities of the lower and upper bills independently, as the UBA and LBA angular excursions observed during each bite divided by the time to peak force (i.e. from bill contact to peak force), then we averaged these over the first three bites of a biting sequence for each bird.

We calculated power (W) as force (N)×instantaneous velocity (m s⁻¹). Because the DAQ and camera systems were not integrated and the sampling rates differed between them, kinematic and force profiles were first synchronized by aligning the times of peak forces to those of the minimum bill tip distance (i.e. complete jaw closure) values within each biting sequence. For every force datum registered (not interpolated) by the DAQ during jaw closure (i.e. only for the ascending arms of the individual bite force-over-time traces), the corresponding (i.e. nearest in time, within a mean±s.d. of 0.003±0.020 s, n=305) kinematic value was obtained. Thus, power values were calculated from each set of corresponding force and velocity data points within a biting sequence for each shrike, and the individual-level maxima were used in subsequent analyses.

To address objective 1, the contribution of prokinesis to bite force and jaw-closing velocity, we used linear mixed-effects (LME) models to test for relationships between the UBA and LBA excursions (i.e. the maximum minus minimum bill angles observed during the bite) against the peak bite forces and peak jaw-closing instantaneous velocities (each dependent variable was tested separately), among repeated bites for all shrikes. Thus, each individual bite in a biting sequence constituted the unit of replication, and shrike identity was included as a random subject effect to account for variation among repeated bites (only the first three bites in a sequence were included). We used bill angle excursions, rather the values of the angles at peak bite forces, because different shrikes performed peak bite forces at different bill angles. We initially included nalospi and body mass as covariates to account for potential differences in body, head and beak size. Furthermore, because previous work on shrikes (Sustaita and Rubega, 2014) and other taxa (Dumont and Herrel, 2003; Dickinson et al., 2022) has shown negative relationships between bite force and gape angle, we included gape angle at peak bite force as an additional covariate for the bite force analysis. Although we could not measure the independent contributions of the upper and lower bills to bite force (above), we could assess their independent contributions to jaw-closing velocity by comparing their angular average velocities using a paired t-test for differences between upper and lower bill angular velocities (deg s⁻¹) within shrikes.

We addressed objective 2, jaw-closing force–velocity trade-offs, within individual bite sequences of shrikes for which the force sampling rate was set to ≥8.2 Hz (n=30). Each force datum registered by the DAQ, and its corresponding instantaneous velocity (during jaw closure only), constituted the unit of replication for this analysis. Accordingly, we included shrike identity as a random subject effect in a LME model to assess the relationship between bite force and jaw-closing velocity within biting sequences across all shrikes collectively.

We addressed objective 3, how power relates to force and velocity across shrikes, based on the peak bite force, instantaneous jaw-closing velocity and biting power recorded for each shrike at any point during its biting sequence. Thus, each individual shrike constituted the unit of replication for this analysis, which sought to identify how the maximal jaw-closing forces and speeds relate to power output across individuals. We used linear models (LM) with maximum bite force and maximum power as the dependent variables (tested separately) and maximum velocity as the predictor. We included nalospi and body mass as covariates to account for potential differences in beak, head and body size across individual shrikes.

We used the ‘lmer’ function of the R package lme4 (Bates et al., 2015; https://cran.r-project.org/web/packages/lme4/index.html) to run the LME models and the ‘lm’ function of base R (http://www.R-project.org/) to run the linear models, followed by the ‘check_model’ function of the R package performance (Lüdecke et al., 2021) to assess model diagnostics and the ‘compare_performance’ function to compare model fits using different data transformations. When data violated assumptions of the analyses based on visual assessment of the diagnostic plots, they were transformed. Model diagnostics for analyses within biting sequences improved with square root transformation of force and velocity. For analyses among individual shrikes, no transformation was necessary for tests of force and velocity, but model diagnostics for tests of power substantially improved with square root transformation of power and velocity. We note that residuals were normally distributed, but there remained some degree of heteroscedasticity which may comprise the parameter estimates. Therefore, we re-ran the analysis using the ‘PermTest’ function of the R package pgirmess (https://CRAN.R-project.org/package=pgirmess), which provides a more conservative Monte Carlo permutation test of effects (based on 10,000 replicates). We used the R package ggeffects (Lüdecke, 2018) to estimate and plot predicted values of the dependent variables, adjusted for other covariates in the models. Data used for the statistical analyses are included in the Supplementary Materials and Methods, Dataset 1.

Mean±s.d. tracking precision was 0.18±0.12 mm and all of the kinematic measurements were significantly repeatable (r_i=0.82 for UBA; r_i=0.92 for LBA; r_i=0.99 for gape angle; r_i=0.99 for BTD; all P<0.0001; Fig. S3). We observed only minor deviations from 2D planarity, which we estimate were no more than ±20 deg about any given axis. The sensitivity analysis suggests potential errors in the key measurements of interest (UBA, LBA and BTD) of 0.13–16.3% resulting from roll, 0–1.1% resulting from pitch, and 0.02–7.5% resulting from yaw, across all three measurements collectively (Supplementary Materials and Methods and Fig. S1). We note that one extreme upper and lower bill angle case was removed (but see Fig. S4).

For the analysis of bite force with respect to bill angle, bite force significantly increased with UBA excursion (P=0.0010; Table 1, Fig. 2A) but was unrelated to LBA excursion (P=0.1996; Fig. 2B). Bite force significantly decreased with gape angle (estimate=−0.160, P=0.0020). The effects of body mass (P=0.0939) and nalospi (P=0.8706) were not significant (Table 1). Peak jaw-closing velocity was unrelated to UBA excursion (P=0.6200; Table 2, Fig. 2C), but significantly increased with LBA excursion (P<0.0001; Fig. 2D). Here again, the effects of body mass (P=0.0980) and nalospi (P=0.992) were not significant (Table 2). LBA excursion average velocity (40.4±17.7 deg s⁻¹, mean±s.d.) was significantly greater than UBA excursion average velocity (18.5±9.2 deg s⁻¹) (paired t-test, t=−8.64, d.f.=50, P<0.0001).

For the analysis of individual bites within biting sequences for each shrike, bite force was significantly negatively related to jaw-closing velocity (estimate=−4.391, P<0.0001; Fig. 3). For the bulk of the data, biting power peaked at values around 37.5% of the maximal bite force and values around 30% of the maximal jaw-closing velocity observed, but power generally increased with higher jaw-closing velocity (Fig. 3).

The analyses among individual shrikes were restricted to n=48 individuals for which corresponding maximal jaw-closing forces and velocities were obtained. Maximum bite force was independent of maximum jaw-closing velocity (P=0.8060; Fig. 4A), after accounting for the non-significant and significant effects of nalospi (P=0.6877) and body mass (P=0.0216; Fig. 4B, Table 3), respectively. Maximum biting power increased significantly with maximum jaw-closing velocity (estimate=1.508, P<0.0001; Fig. 4C), but was not significantly related to maximum bite force (P=0.0669; Fig. 4D), and the effects of nalospi (P=0.0769) and body mass (P=0.1764) were not significant in the Monte Carlo permutation test (Table 4). Inspection of Fig. 4C,D shows that maximum biting power is achieved by shrikes that exert various combinations of maximal jaw-closing velocity and bite force, but shrikes that produce more powerful bites are typically associated with mid-range jaw-closing velocities and higher bite forces.

Loggerhead shrikes are voracious predators of aerial and terrestrial arthropods and small vertebrates that may select for jaw-closing speed and strength, respectively. Our results show that, although shrikes experience a force–velocity trade-off during the act of biting, this trade-off is not manifested across individuals. As a corollary, bite force is more closely associated with upper bill depression, whereas jaw-closing speed is more closely associated with lower jaw elevation. We hypothesize that prokinesis (particularly upper bill depression) might facilitate decoupling of jaw-closing force and velocity, which in turn might allow shrikes to avoid the force–velocity trade-off constraint. By having unrestricted access to different combinations of jaw-closing forces and speeds, shrikes (and possibly other birds) could maximize biting power to deliver strong bites very rapidly, to accommodate a variety of arthropod and vertebrate prey.

The fact that the force–velocity trade-off was manifested within individual bites during biting sequences (i.e. during individual jaw-closing events) suggests that shrikes are operating within the ranges of bite force and jaw-closing velocity that limit one another. However, two methodological points could be raised here. First, the relationship between upper jaw depression with bite force, and lower jaw elevation with jaw-closing velocity, could be a simple artefact of the force transducer design, given that only the upper beam (directly) registered the force. We do not know what these patterns would look like were we to, for example, introduce the device upside down, or have the lower beam fitted to a load cell as well. However, as mentioned previously, the shrikes' heads were not fully immobilized during testing, so the upper jaw forces could not be isolated, and hence were not restricted to the upper beam. Thus, the forces registered by the upper beam resulted from adduction of both the upper and lower beams by the upper and lower jaws, combined. Without measuring the isolated, independent forces of the upper and lower jaws separately (which is practically impossible in a wild population of a protected species), the outcome is that even if the forces were entirely supplied by upper bill depression, we cannot discount the contributions of the lower jaw to bite force in resisting/counteracting these forces. Second, given the synthetic nature of the device and contrived circumstances, it is likely that the wild shrikes in our study bit the devices defensively, which may or may not have elicited their maximal capacities. By operating at relatively lower bite forces, they may not actually be forced into trade-offs with jaw-closing velocity, which might inadvertently maximize power. To properly assess the decoupling of upper and lower jaw forces, and determine their maximal outputs, would require more invasive in vivo methods involving cranial restraint and/or electrical stimulation of jaw adductor muscles. Alternatively, detailed biomechanical models may accurately quantify the independent contributions of the upper and lower jaws to maximal bite force and jaw-closing velocity.

We observed an angular excursion of prokinesis of approximately 0.04–15.8 deg across all shrikes, with a mean±s.d. of 3.5±2.5 deg (n=196 bites), which is a range that incorporates values reported for both neognathous (∼12 deg; Bout and Zweers, 2001) and paleognathous birds (∼10 deg; Gussekloo and Bout, 2005a). For example, in white-throated sparrows (Zonotrichia albicollis), Hoese and Westneat (1996) observed upper jaw rotations of 1.2–9.5 deg, with an average of ∼4.6 deg, during song production. A study by Van Wassenbergh et al. (2022) on cranial prokinesis during beak retraction from wood substrates showed that the black woodpecker produced clockwise upper bill rotations with respect to the cranium of 4±3 deg during the first phase of beak removal, followed by rotations of 8±5 deg. Lyons et al. (2023) quantified cranial kinesis kinematics in a diversity of birds, finding that both woodpeckers and non-woodpecker insectivores display upper beak rotations of up to 8 deg.

Cade (1995) speculated that the large, heavy head of shrikes accommodates large muscles for producing ‘powerful’ bites, although this has yet to be comprehensively studied. High bite forces could result from hypertrophied jaw musculature, increased mechanical advantage, or both (Herrel and Aerts, 2004; Sustaita, 2008). Clearly there are many ways in which this could be achieved, and a truly ‘powerful’ bite, by definition, requires a fast jaw-closing speed. Prokinesis allows the jaws to close more rapidly, simply because both jaws can move toward one another (Bock, 1964; Bout and Zweers, 2001). At the same time, changes in the mechanical advantage of the adductors resulting from the movement of the quadrate could enhance force production (Herrel et al., 2000, 2004; Bout and Zweers, 2001). Thus, our current and future efforts to quantify the relative development of muscles involved in prokinesis should help to reveal how the purportedly powerful bites of shrikes are produced. Nuijens and Bout (1998) reported observations of zebra finches using upper bill depression during seed crushing, suggesting its particular importance for crushing hard seeds. Contrary to their expectations, Lyons et al. (2023) observed upper bill depression more in woodpeckers than in other insectivorous birds (which primarily showed upper bill elevation) during a variety of behaviors, including drilling.

Our observations of upper bill depression during biting in shrikes suggest a force-enhancing role of prokinesis (e.g. Herrel et al., 2000), but warrant more explicit testing of the precise contributions of the upper and lower jaws to bite force. The biomechanical hypothesis for this is derived from the interspecific static 2D modeling study of finch skulls by van der Meij and Bout (2008), who found that a caudal shift of the quadrate, a downward inclination (i.e. angle of depression) of the beak, and a caudal shift of the rictus resulted in larger bite forces. These are the same conformational changes that are observed (e.g. downward shift of the upper bill and caudal shift of the rictus), and presumed to occur (e.g. caudal shift of the quadrate), in our videos during biting (Movies 1, 2 and 3). van der Meij and Bout (2008) attributed the increase in bite force with greater upper beak downward inclination (analogous to the depression observed here) to the decrease in the distance between the jaw-closing muscles and the prey item. The caudal shift of the rictus is thought to be associated with a shortening of the out-lever of the jaw-closing muscles (van der Meij and Bout, 2008), rotation of the upper bill about the craniofacial hinge would act to increase the moment arms of the upper jaw-closing muscles (van der Meij and Bout, 2008). Nevertheless, this may not be entirely universal among birds. Young et al. (2023) found that lower bill elevation, rather than upper bill depression, was the primary driver of jaw adduction force in lovebirds. This, however, may derive from the comparatively unique mode of feeding in parrots, whereby the maxilla is used to manipulate and support food items, against which the mandible acts to break them (Young et al., 2023).

During jaw adduction (i.e. the act of biting), jaw-closing force and velocity trade off, as tenets of muscle physiology and lever mechanisms dictate. However, the peak bite forces that individual shrikes generate are independent of the peak jaw-closing velocities they produce during a bite (i.e. there is no trade-off). Similarly, Corbin et al. (2015) found no direct functional trade-off between bite force and jaw-closing speed (during vocalizations) across a range of species after adjusting for body size. They suggested the possibility that velocity and force might be biomechanically decoupled, citing morphological evidence that bite force is influenced more by jaw muscle size, whereas jaw-closing speed is explained more by jaw lever lengths and mechanics (Corbin et al., 2015). Gomes et al. (2020) also described a potential division of labor underlying the bite forces and bite durations in the wall lizards they studied, between the muscles dictating bite force (musculus adductor mandibulae externus superficialis, composed of fast fibers) versus bite duration (m. pterygoideus, composed of slow fibers). Similar decoupled jaw mechanisms have also been described in the intramandibular joints of angelfishes (Konow and Bellwood, 2005). Copus and Gibb (2013) also described the advantage of independent upper and lower jaw rotation for decreasing jaw-closing duration in butterflyfishes, and how the relatively greater mechanical advantage of the upper jaw (versus the lower jaw) mechanism increased bite force by 33%. Our performance data suggest a similar kind of biomechanical decoupling, in that greater bite forces were associated with greater angular excursions of upper bill depression, whereas greater jaw-closing speeds were associated with greater angular excursions of lower jaw elevation. Moreover, lower jaw angular average velocities were greater than those of the upper jaw, providing partial support for a division of labor between the upper and lower jaws.

The analysis of individual bites (within shrikes) demonstrated that the force–velocity trade-off exists and presents a physical constraint during the act of biting. However, the lack of a trade-off across peak forces and velocities of individuals suggests that perhaps birds fine tune their biting behavior primarily through alterations to jaw-closing speed. This is reflected by the greater coefficient of variation of maximal jaw-closing velocities (65%) over those of peak forces (20%) of bites across individual shrikes. Evolutionary adaptation for high bite force need not come at the expense of a fast-closing velocity (Corbin et al., 2015). In fact, other animals have found other physiological and biomechanical ways of ‘getting around’ the force–velocity constraint. For example, dynamic actuators, such as spring (e.g. McHenry, 2011) and latch (e.g. Longo et al., 2019) mechanisms, can alter the speed of movement by storing and releasing energy. But if the ‘goal’ is to operate outside the range of bite forces and jaw-closing velocities that limit one another, the question remains as to what specifically the advantage of a division of force–velocity labor between the upper and lower jaws is. Hypothetically, simply by not biting too hard, animals should bite faster, and by not biting too fast, they should bite harder. Perhaps the division of labor between the upper and lower jaws provides greater flexibility for achieving more optimal combinations of bite force and jaw-closing velocity to increase biting power (below).

Naturally there are other factors underlying feeding performance. Andries et al. (2023) found no significant positive effects of beak kinematics (e.g. closing velocity) on feeding performance (e.g. seed handling duration) in canaries, for which they postulated an underlying ‘speed–accuracy’ trade-off: greater beak movement speeds limit control over the seeds, and thereby reduce the success of husking attempts. Andries et al. (2023) instead found that ‘skilled’ positioning of seeds via coordination of beak and tongue movements was the primary explanator of variation in feeding performance among individuals. This highlights the importance of understanding the role of trade-offs for mediating functional performance, and the importance of factors other than shear bite force for determining feeding performance.

We found that shrikes apply jaw-closing forces and velocities that maximize biting power. Our data are consistent with Westneat's (2003) modeling of fish jaws, which illustrated how total jaw-closing power peaked in the center of the contraction cycle when force and velocity were both at intermediate levels. Sargeant (2007) suggested that to achieve a mid-range power, only 50% of the muscle power-generating capability is needed at optimum velocity, but 100% is required at the slower speed. Thus, there are clear benefits to operating at faster speeds at the expense of force, which supports our contention that across individuals, shrikes might modulate jaw-closing velocity more so than force.

There is a substantial gap in the literature regarding the advantages of biting power in vertebrates. Studies that address power in the context of feeding behavior deal with extremely fast ballistic or projectile movements, such as mantis shrimp appendages (e.g. Patek et al., 2004), trap-jaw ant jaws (Patek et al., 2006; Larabee et al., 2017), and the tongue projection of salamanders (e.g. Deban et al., 2007) and chameleons (e.g. Anderson and Deban, 2012). These are often underlain by complex power-amplifying elastic latch or spring mechanisms, thought to have evolved to overcome the limits of muscle power production (e.g. Patek et al., 2007; Ilton et al., 2018; Longo et al., 2019; Deban et al., 2020). Other studies have focused on power in terms of, for example, suction-feeding in fishes to better understand the sources of the suction expansion power they produce (e.g. Westneat, 2003; Camp et al., 2015; Camp and Brainerd, 2022). This study offers an opportunity to understand the role of power in the context of jaw-closing (biting) mechanics in birds. For comparative context, we estimated the mass-specific power requirements of the jaw-closing musculature. We currently do not have detailed measurements of jaw musculature in shrikes, but based on the allometric equation for jaw-closing muscle mass versus body mass for a diversity of passerine species from Deeming et al. (2022), along with a mean body mass of 48.6 g and a maximum biting power of 0.466 W for the shrikes in our study, we estimated jaw muscle power requirements of ∼63.2 W kg⁻¹. This is relatively low compared with other taxa and feeding contexts: Westneat (2003) estimated power requirements for subdivisions of the adductor mandibulae muscle of labrid fishes of 160.2–169.4 W kg⁻¹ during suction feeding, and Camp et al. (2015) reported epaxial and hypaxial mass-specific peak power of 14–438 W kg⁻¹ during suction feeding in bluegill sunfish. The maximum peak muscle requirements for generating observed tongue projection accelerations in chameleons range from 1410 to 14,040 W kg⁻¹ (Anderson, 2016). Impressively, mantis shrimp have a minimum muscle power requirement of 4.7×10⁵ W kg⁻¹ for a typical strike (Patek et al., 2004). Naturally, the accuracy of our estimate will benefit from our forthcoming micro-computed tomography-based musculoskeletal analyses of jaw structure and function.

We suggest that power enhancement is a consequence of the force–velocity characteristics of shrike bite performance. Hull (1991) concluded that ‘power and kinesis are not compatible within the jaw system’ of insect- and vertebrate-eating falcons. Conversely, we hypothesize that prokinesis may allow shrikes (and possibly other birds) to decouple jaw force and speed to operate more effectively in the region of the force–velocity trade-off that maximizes biting power. Increased biting power should be selectively advantageous for taking relatively large and strong vertebrate prey and small and fast arthropod prey alike. Previous work has suggested that shrikes with different beak shapes can generate similar levels of biting pressure (force per unit area) by modulating bite force (Sustaita and Rubega, 2014). Our work here extends this demonstration of many-to-one mapping of form to function (Wainwright et al., 2005) to performance, in that different combinations of jaw-closing force and velocity can result in similar levels of biting power. Nevertheless, further work is required to understand specifically whether, and how, biting power enhances prey capture performance in the wild, and the extent to which it is under direct or indirect selection.

Shrikes regularly encounter demands for both jaw-closing force and speed by their relatively large vertebrate and small arthropod prey, suggesting a potential role for jaw-closing power. The components of power, jaw-closing force and velocity trade off while biting, and biting power is optimized at mid-to-high levels of jaw-closing velocity and low-to-mid levels of bite force. However, the maximum bite force a shrike produces is independent of its maximum jaw-closing velocity, and as a result maximal biting power tends to occur along a broad range of maximal bite forces and maximal jaw-closing speeds across individuals. Furthermore, maximum biting power among shrikes is associated more with their maximal jaw-closing velocities than their maximal bite forces, suggesting that jaw-closing speed is at least as ecologically important as bite force in these birds. Upper and lower bill kinematics suggest that lower jaw elevation contributes more to jaw-closing speed than does upper bill depression. Conversely, given the latter's comparatively higher correlation with bite force, we hypothesize that upper jaw depression contributes more to bite force production, although this remains to be tested more explicitly. If so, such decoupling may provide alternative means for modulating bite force and velocity to effect greater power. Our analysis contributes to a small, but growing, literature on in vivo cranial kinesis in birds (e.g. Hoese and Westneat, 1996; Gussekloo et al., 2001; Gussekloo and Bout, 2005a,b; Dawson et al., 2011; Van Wassenbergh et al., 2022; Lyons et al., 2023), showing how the versatility of avian jaws often transcends beak dimensions to generate the great functional and ecological diversity observed among species. Studies like this will help to expand our understanding of the prevalence, and functional contexts, of decoupling mechanisms and power production in vertebrate jaws.

Very special thanks to N. Broccoli for assistance with video tracking, and to M. Rubega, A. Rico-Guevara, B. Ryerson, K. Schwenk and the UConn Ornithology Research group for helpful discussions on this topic. Felipe Garzón Agudelo provided additional technical assistance. We are also greatly indebted to two anonymous reviewers, whose suggestions substantially improved the manuscript.