Come on baby, let's do the twist: the kinematics of killing in loggerhead shrikes

1. Introduction

Shrikes (Passeriformes: Laniidae) are medium-sized (approximately 50 g) predatory songbirds, best known for their tendency to impale their prey [1]. Although the dietary composition of arthropods and vertebrates varies among species [1], most shrikes possess features adapted for carnivory [2]. Vertebrate prey of shrikes range 13–206% of their body mass [3] and probably are more difficult than arthropods to subdue, given their greater strength and potential to inflict harm [4–6]. Their falcon-like upper bills house a sharply hooked tip and tomial projections of the rhamphotheca [2], which are thought to penetrate between cervical vertebrae of their prey and cause partial paralysis [2,4].

Previous workers have described prey-capture and killing behaviour in shrikes, emphasizing the importance of the beak and jaw strength for delivering mortal bites to the neck of their prey [4,5,7,8]. Few, however, have described other aspects of prey processing, such as the vigorous shaking or pounding of prey against the substrate that ensues immediately upon prehension [9–11]. We captured and quantified this underappreciated aspect of shrike predatory behaviour through high-speed videography of captive San Clemente loggerhead shrikes (Lanius ludovicianus mearnsi) attacking vertebrate prey. We measured the frequencies and angular accelerations of these prey-handling movements to address our ultimate objective of understanding the relative roles of beak shape, bite force and prey-handling kinematics in processing vertebrate prey.

3. Results

Shrikes immobilized and killed vertebrate prey by repeatedly biting the head or neck, or by latching onto the nape with their beaks and vigorously shaking them with rapid, long-axis head rolls (figure 1; electronic supplementary material, videos S1–S3). Although this behaviour was not captured by video for all shrikes, 13/14 that were filmed completing their kills performed it at some point during the sequence. The mean ± s.d. cycle frequencies (11.02 ± 3.07 Hz, n = 28 attack sequences by 13 shrikes) and ω_avg (57.3 ± 9.5 rad s⁻¹, n = 4 attack sequences by four shrikes) were within ranges reported for non-predatory shaking behaviours of other birds [16] and mammals [17].

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Figure 1.

Approximately four cycles from a representative sequence of an adult male shrike shaking an adult mouse immediately upon capture. Dots are mean-centred angles (± s.d. from five repeated measurements) of the shrike's head (black) and mouse's head (blue) and body (red), computed from landmark coordinates (curves represent low-pass filtered data).

Our kinematic analysis of one approximately 58 g adult male shrike shaking an approximately 17 g adult mouse yielded approximately four cycles of axial head rotations (figure 1). The shrike's head rotations reached mean ± s.d. (n = 5 repeated measures) |peaks| of 68.9 ± 2.5° in amplitude and ω = 71.2 ± 8.7 rad s⁻¹. The mouse's body rotation reached peaks of ω = 39.4 ± 1.4 rad s⁻¹, α = 2696.1 ± 125.2 rad s⁻² and 6.0 ± 0.3 g (assuming r = 0.0217 m; electronic supplementary material, figure S2). The peak cross-correlation (r = 0.46 ± 0.03 at a lag of −2 frames for all repeated measures) between the mouse's body and head indicated that the angular movements of the mouse's body lagged those of its head by approximately 0.016 s. Based on the rotational inertia for the average-sized mouse (I_CM = 7.99 × 10⁻⁶ kg m²), we obtained a peak τ of 0.022 ± 0.001 N m (n = 5 repeated measures) exerted by the body of the mouse about its own neck.

4. Discussion

Adult shrikes rely almost exclusively on their beaks for capturing, processing and ingesting prey. However, an underappreciated component of their prey-processing behaviour is the rapid axial head-rolling movements performed by many of the shrikes we observed upon seizing vertebrate prey. We suggest that the angular accelerations shrikes impart on their prey may be sufficient to cause pathological damage to the spinal column. Furthermore, the motions of the mouse's head and body progressively become shifted out of phase (figure 1), potentially inducing greater compressive forces on the vertebrae from simultaneous flexion and extension of the cervical spine [18].

We estimated a peak instantaneous acceleration corresponding to 6 g for a mouse's body about its neck while being shaken by a shrike. By analogy, victims of low-speed rear-end car crashes experience head accelerations of 2–12 g [19]. These accelerations can result in cervical spine extensions that exceed physiological ranges [20], and damage the cervical facet capsular ligaments that stabilize the zygapophyseal joints between successive vertebrae [21]. In rats, these ligaments rupture at stresses of 2–4 MPa and a mean tensile force of 2.45 N [22]. Assuming that a moment arm equal to the dorsoventral depth (approximately 2.1 mm, estimated from [22]) of the rats' vertebral centrum can place the capsular ligaments into tension upon sufficient acceleration of the body relative to the head, then approximately 0.0051 N m would be required to cause failure (electronic supplementary material, figure S2). Thus, our estimate of torque on the cervical spine of the mouse during the shrike's head-rolling behaviour is approximately four times greater than that required to fail the capsular ligaments of rats approximately 20 times larger than the mice in this study. Cade [4] showed that of the 94 ‘major’ wounds inflicted on prey by Northern Shrikes, 55 were along the middle cervical vertebrae, which coincides with the region of tension and buckling of whiplash-related injuries to human car collision victims [20].

Similar prey-shaking behaviour has been reported for other birds [23–25], crocodilians [26], mammals [27], snakes [28], lizards [29] and has even been inferred in Tyrannosaurus rex [30]. However, save for ‘spinning’ in crocodiles [26], many of these differ substantively from our observations of axial head-rolling in shrikes, in that the prey are beaten against the substrate [23,25], or the action emanates primarily from side-to-side (yaw) movements [28,31]. When combined with the effects of beak shape and bite force [32], this behaviour may help explain how shrikes dispatch relatively larger vertebrate prey than would be expected for their body sizes [2], and provides another example of the importance of prey inertial forces for feeding in predators [26,30].

Ethics

Live prey were not used solely for the purpose of this study; captive shrikes were routinely fed live prey for ensuring predatory proficiency upon their release into the wild [12], and no additional mice were killed than would have occurred without the videos. We filmed under University of Connecticut IACUC #E08-003 and #E11-014.

Data accessibility

Data and videos accompanying this article have been uploaded as electronic supplementary material.

Authors' contributions

D.S. and M.A.R. conceived the study; S.M.F. facilitated the project, supervised the fieldwork and edited manuscript drafts; D.S. gathered and analysed data; D.S. and M.A.R. wrote the paper. All authors approved the final version of the manuscript and agree to be held accountable for its content.

Competing interests

The authors declare no competing interests.

Funding

This project was funded by NSF DDIG IOS-1110716.