Biomechanics of predator–prey arms race in lion, zebra, cheetah and impala

Abstract

The fastest and most manoeuvrable terrestrial animals are found in savannah habitats, where predators chase and capture running prey. Hunt outcome and success rate are critical to survival, so both predator and prey should evolve to be faster and/or more manoeuvrable. Here we compare locomotor characteristics in two pursuit predator–prey pairs, lion–zebra and cheetah–impala, in their natural savannah habitat in Botswana. We show that although cheetahs and impalas were universally more athletic than lions and zebras in terms of speed, acceleration and turning, within each predator–prey pair, the predators had 20% higher muscle fibre power than prey, 37% greater acceleration and 72% greater deceleration capacity than their prey. We simulated hunt dynamics with these data and showed that hunts at lower speeds enable prey to use their maximum manoeuvring capacity and favour prey survival, and that the predator needs to be more athletic than its prey to sustain a viable success rate.

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Figure 1: Overview
Figure 2: Muscle contraction mechanics
Figure 3: Locomotor performance based on stride parameters.
Figure 4: Output of the model of predator–prey interaction.
Figure 5: Orientation of direction of acceleration for each stride grouped by species.

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Acknowledgements

We thank S. Amos for fabricating collars, N. Jordan and G. Gilfillan, M. Claase and N. Terry and BPCT research assistants for working with us in the study area and M. Flyman (DWNP) for his support and enthusiasm; J. Usherwood, R. Bomphrey and A. R. Wilson for comments on the manuscript; EPSRC (EP/H013016/1), BBSRC (BB/J018007/1) and ERC (323041) for funding. The Botswana Predator Conservation Trust was supported by private donors, Tusk Trust and the Cincinnati Zoo. Work was approved by RVC Ethics & Welfare Committee (RVC 2013 1233) and Botswana Department of Wildlife and National Parks Research Permits were held by J.W.M. and A.M.W. (EWT 8/36/4 plus additions) and a Botswana Veterinary Registration held by A.M.W. Tissue shipping was covered by CITES, Botswana export, Botswana National Veterinary Laboratory approval, South African transit and UK DEFRA import permits.

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Contributions

A.M.W., T.Y.H. N.A.C., R.C.W. and T.G.W. conceived, designed and led the study. K.A.G., J.W.M., H.L.A.B.-B. and E.B. organized field work, monitored animals and downloaded data. A.M.W. performed veterinary procedures, J.C.L. and A.M.W. designed and built collars. R.D., M.L., N.A.C. and T.W. carried out muscle experiments and interpreted the muscle data. T.Y.H., O.P.D., T.G.W. and A.M.W. analysed data. S.W. created the model and carried out statistical analysis. A.M.W. wrote the paper with input from all authors.

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Correspondence to Alan M. Wilson.

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The authors declare no competing financial interests.

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Reviewer Information Nature thanks A. Biewener and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Figure 1 GPS data summary.

a, Example manoeuvring sequence for a cheetah showing position based on fused GPS-IMU data (250 Hz) colour-coded according to speed and segmented for clarity (1–5, duplicated in be). b, Speed based on fused GPS-IMU data (250 Hz). ce, Stride-wise values for speed (averaged over stride), tangential (fore–aft) acceleration (change in stride speed/stride durations) and centripetal (lateral) acceleration ((change in heading/stride duration) × stride speed). f, Details on the animals used and datasets collected. Reduced dataset of non-steady state stride used for analysis of maximum performance. Note, the number of strides and distance per run was based on all strides (steady-state included).

Extended Data Figure 2 Muscle data summary.

ac, Time course of stress (force) development in a single skinned impala fibre, showing transition of the fibre through pre-activation, activation and relaxation solutions, and stress development after temperature jump (T-jump) from 1 to 25 °C. The sample rate was 5 kHz. The grey noisy parts of the stress trace denote periods of solution change. The four downward ‘spikes’ in the stress record (at 9, 10, 11 and 12 s) are distinct periods of force control, where the fibre length was first rapidly reduced from Lo and then reduced at an appropriate rate to maintain force at pre-defined sub-maximal levels. The broken-line box in a surrounds the first episode of force control and is presented in b and c on an expanded time scale. b Relative force (F/Fisom) was reduced to 40% of the maximum for 20 ms, where F indicates force during shortening, Fisom indicates isometric force. Isometric force (Fisom) and the force during force clamp (F) were recorded as average values for the central 10-ms intervals (vertical lines). A force measurement, Fisom, was recorded just before each of the four force-control events and used in the calculation of F/Fisom. c, Shortening speed (in Lo s−1) was derived from the rate of change in fibre length during each force clamp. At the end of the force clamp, fibre length was ‘quick-released’ to a slack length (70% of Lo), where force was reduced to the zero baseline. After 10 ms at slack length, the motor lengthened the fibre back to the starting length (Lo), isometric stress was re-established (as shown in a) and another force control event was initiated. d, Twelve points on a power–force relationship could be obtained from three temperature jump activations of a single fibre. The curves were fitted (see Methods) to give relative power (power/FisomLo (in s−1)) as a function of relative force (F/Fisom). Expressing both variables in relative units is important for the curve-fitting process, mainly because the measurements of Fisom often vary between and within activations; in the example shown in a there was a small reduction in Fisom through the activation at 25°C. e, Peak isometric force relative to fibre cross-sectional area (CSA) for fibres from the four species. f, Power output relative to fibre volume. There was a distinct subpopulation of low-performance fibres (mostly from lion and zebra) that displayed lower power at a given fibre volume. Fibres with a shortening velocity at peak power of <1.35 Lo s−1 (see also Fig. 2c) were classified as low performance. g, Peak power relative to stress at peak power. The low performing fibres also had stress at peak power values that were relatively low—the data points below the thin dashed black line have velocities of shortening <1.35 Lo s−1. h, The variability in stress at peak power was similar across the species tested. i, Details about the muscle fibres. Mean (±s.e.m.) mechanical features for single skinned skeletal muscle fibres from biceps femoris of cheetah, lion, impala and zebra. Mean values are also categorized for the predator and prey groups, and further as the high-performing sub-groups of fibres (high-performing fibres had optimal shortening speeds >1.35 Lo s−1, see main text and Extended Data Fig. 2f, g, i).

Extended Data Figure 3 Predator–prey run comparisons.

a, b, Histograms of all strides (a) and extracted non-steady state strides (b), for which the cut-off was species-specific based on their kurtosis. The x axis is the normalized and squared horizontal acceleration in arbitrary units (that is, combined tangential and centripetal). In b, on the x axis, the cut-off is zero and the 98th percentile is one. Cheetah, blue; impala, red; lion, purple; zebra, yellow. Removing steady-state strides delivers a similar distribution tail for all four species. This is critical for deriving an appropriate 98th percentile, as this should be equally representative in all four species. c, Histogram of maximum stride parameters recorded in each run (speed, centripetal and tangential acceleration) for each species. Colour-coded by individuals, n is the number of runs used for data extraction. One concern of the comparison between predator and prey species is the potential lack of high-performance runs in prey species due to the low number of actual one-on-one chases. However, the distribution of the performance data shows that the cheetah and impala data include a considerably higher proportion of high-performance runs, whereas the lion and zebra dataset includes a large percentage of slower runs. Recognizing that the species differ in run characteristics (motivation, proportion of steady-state versus non-steady-state strides), we removed steady-state strides, based on the species-specific kurtosis, resulting in a comparable distribution in all four species (see Methods).

Extended Data Figure 4 Performance metrics separated by individual and species plotted against run distance and against run tortuosity.

Maximum accelerations and speeds were extracted from each run and displayed versus distance covered during the run and versus tortuosity of the run. Tortuosity is the ratio of distance covered in a run to net displacement (distance between start and end of the run). Markers are colour-coded per individual, dashed black line maximum values are based on 98th percentile. Number of runs (data points) are given in Extended Data Fig. 1f. Cheetah, 520 runs; impala, 515 runs; lion, 2,726 runs; zebra, 1,801 runs.

Extended Data Figure 5 Work and power analysed for each species.

a, Cheetah. b, Impala. d, Lion. e, Zebra. a, b, d, e, Dots indicate the data points and the line marks the 98th percentile for data in speed bins as shown in Fig. 3a, b, d, e. Markers are colour-coded by individual, the solid black line is the 98th percentile. c, f, Comparison of the predator–prey pairs. c, Cheetah–impala. f, Lion–zebra. g, Comparison of the predator species (lion–cheetah). h, Comparison of the herbivore species (impala–zebra). i, The 98th percentile for all four species. c, fi, Data are colour-coded by species (key is shown in i). In all four species maximum negative power was similar to maximum positive power. Muscle stress can be considerably higher when performing negative work than positive work70,71 and a 60% higher fascicle power in lengthening (rather than shortening) has been reported71, so mass-specific muscle power can be much higher in deceleration72. Body geometry relative to the ground reaction force vector or grip may limit the attainable horizontal ground reaction force15 and the muscles need to be arranged to lengthen while experiencing the large horizontal forces. Many of the propulsive muscles are hip retractors (Extended Data Table 1), which are not configured to resist forward motion.

Extended Data Figure 6 Tangential and centripetal acceleration analysed for each species.

a, Cheetah. b, Impala. d, Lion. e, Zebra. Dots indicate the data points and the line marks the 98th percentile for data in speed bins as shown in Fig. 3a, b, d, e. Markers are colour-coded by individual, the solid black line is the 98th percentile. c, f, Comparison of the predator–prey pairs. c, Cheetah–impala. f, Lion–zebra. g, Comparison of the predator species (lion–cheetah). h, Comparison of the herbivore species (impala–zebra). i, The 98th percentile for all four species. c, fi, Data are colour-coded by species (key is shown in i).

Extended Data Figure 7 Locomotor performance based on stride parameters.

This is the same as Fig. 3, but the ratios compare the two predators and the two prey species. All values are averaged per stride or represent the change over a stride. ae, Acceleration. a, Positive net work performed in each stride. b, Stride frequency. c, Stride power. d, Increase in speed per stride. e, Forward acceleration with the curved lines representing a mean power of 30, 60, 90, 120 and 150 W. f–j, Deceleration. fj, As ae but for decelerating strides. kn, Turning. k, Centripetal acceleration. l, The relationship between speed and turn radius with limit lines for a coefficient of friction (μ) of 0.6 and 1.3. m, Change in heading versus speed. n, Lateral versus tangential acceleration with limits as for μ. In n, F represents pure forward acceleration; B, deceleration; and C, acceleration to the side. In each panel, there is one line per species that represents the 98th percentile for data in speed bins (bins always include 400 data points, therefore bin width varies). Cheetah, blue; impala, red; lion, purple; zebra, yellow. Bottom, the ratio of that parameter for cheetah to lion (green circle) and impala to zebra (magenta circle) is given for each speed bin.

Extended Data Figure 8 Output of model of predator–prey interaction and impact of performance differential on hunt outcome.

See also Fig. 4. a, b, Plot showing output of simulation. a and b are equivalent to Fig. 4d with more subplots for cheetah–impala and lion–zebra, respectively. At the start of simulation, both have initial velocity towards the top of the page and initial separation. After one stride the prey can move to anywhere in the red or yellow ellipse by acceleration in the appropriate direction. Predator velocity remains unchanged, as there is no prey acceleration in the previous stride to react to. Initial positions are shown. Larger red or yellow ellipse perimeter is the area prey can reach after two strides of the chosen maximum acceleration. The blue or purple filled ellipse represents the locations the predator can occupy after its second stride (responding to the prey acceleration observed in first stride). The area of the prey ellipse that is covered by the predator ellipse line is defined as probability of capture. Predator is given a starting speed for each combination of prey speed and initial spacing that maximizes the capture probability. Rows are different initial prey speeds, values in red to the left of each row. Columns are different initial predator–prey separations at the start of the simulation with values given in red below each column. Scale for all instances is given in the bottom left plot in metres (in black). The inset black numbers in each sub-panel are the initial (optimized for maximum success) predator speeds in m s−1. c, The optimum lion speed to maximize overlap (hotter colours indicate faster speed, key on the right) as a function of zebra speed (x axis) and starting separation (y axis). The histogram above the main plot shows the distribution of actual zebra speed at first turn of 10 degrees or more for each run (same x axis as the main plot) and the vertical histogram shows distribution of actual lion speed at first turn (scale as for heat bar). d, The proportional overlap (capture probability), as a function of zebra initial speed and starting separation. e, Modelled capacity for forward acceleration (speed increase per stride) as a function of speed (Extended Data Table 2b). Cheetah, blue; impala, red; lion, purple; zebra, yellow.

Extended Data Table 1 Proportion of animal that is locomotor muscle
Extended Data Table 2 Performance parameters

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Wilson, A., Hubel, T., Wilshin, S. et al. Biomechanics of predator–prey arms race in lion, zebra, cheetah and impala. Nature 554, 183–188 (2018). https://doi.org/10.1038/nature25479

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