Extremely fast feeding strikes are powered by elastic recoil in a seahorse relative, the snipefish, Macroramphosus scolopax

Abstract

Among over 30 000 species of ray-finned fishes, seahorses and pipefishes have a unique feeding mechanism whereby the elastic recoil of tendons allows them to rotate their long snouts extremely rapidly in order to capture small elusive prey. To understand the evolutionary origins of this feeding mechanism, its phylogenetic distribution among closely related lineages must be assessed. We present evidence for elastic recoil-powered feeding in snipefish (Macroramphosus scolopax) from kinematics, dynamics and morphology. High-speed videos of strikes show they achieve extremely fast head and hyoid rotational velocities, resulting in rapid prey capture in as short a duration as 2 ms. The maximum instantaneous muscle-mass-specific power requirement for head rotation in snipefish was above the known vertebrate maximum, which is evidence that strikes are not the result of direct muscle power. Finally, we show that the over-centre conformation of the four-bar linkage mechanism coupling head elevation to hyoid rotation in snipefish can function as a torque reversal latch, preventing the head from rotating and providing the opportunity for elastic energy storage. The presence of elastic recoil feeding in snipefish means that this high-performance mechanism is not restricted to the Syngnathidae (seahorses and pipefish) and may have evolved in parallel.

Keywords: Syngnathiformes; over-centre latch; suction feeding; torque reversal; trigger mechanism.

Figure 1.

A representative snipefish strike. (a–f) Select frames from a feeding strike, beginning one frame before hyoid onset (time h in g) and ending at prey capture. Frame (f) illustrates total head rotation (pink angle) and hyoid rotation (green angle). Dots correspond to linkage joints similar to figure 3c. (g) Kinematic profile for a different strike, showing excursions relative to their maximum values (for magnitudes, see electronic supplementary material, figure S3). Dashed lines indicate onset times and the solid blue line is prey capture.

Figure 2.

Peak instantaneous muscle-mass-specific requirements for each strike in our dataset by individual (means in red). Most values are above the in vitro peak instantaneous muscle power output recorded for a vertebrate (middle grey-dashed line) [24] and well above that for fish (bottom black-dashed line) [25]. This is evidence for elastic recoil, because no vertebrate muscle is known to possess such high power output. For comparison, the top blue dashed line indicates the pipefish peak instantaneous power requirement [11].

Figure 3.

The snipefish elastic recoil mechanism. (a) Posterior view of the hyoid region from a cross section made just posterior to the hyoid–preopercular joint. Each hyoid (green) fits into a joint with the preoperculum (pink highlight) and is further bounded by the basihyal (purple) and urohyal (blue). Ventral armour is coloured tan for contrast. (b) Dorsal view of the hyoid region from a transverse section (the basihyal has been digitally removed for visibility). The hyoid is adducted in A and B. (c) Digital radiograph with the hyoid depressed in the orientation seen near the end of the strike. The four-bar linkage coupling head elevation and hyoid depression is overlaid. (d) Four-bar linkage when the hyoid is adducted. (e) Muller's hypothesis was that the hyoid and urohyal–sternohyoideus linkages are aligned and lock the system in place, compared with our finding (f) that the linkages are partially overlapped. Note how the circled torques for the hyoid and urohyal–sternohyoideus linkages change sign depending on their arrangement. (+) and (−) refer to the direction of torque on specific linkages. The trigger arrow in (f) is a schematic of the proposed hypaxial trigger. Pink, neurocranium–suspensorium linkage (n); yellow, pectoral linkage (p); blue, urohyal–sternohyoideus linkage (u); lime green, hyoid linkage (h); green, epaxial tendon (t); red, epaxial muscle (e); purple, basihyal. Scale bar, 1 mm.

Figure 4.

The two possible scenarios for the evolution of power-amplified head rotation by elastic recoil in Syngnathiformes. (a) This mechanism may have evolved multiple times (one possible scenario shown on the left), or it may have evolved once at the base of the clade (right). Pivot feeding, or rapid rotation of the long snout (*), seems to characterize syngnathiform feeding [17] and may have been an important preadaptation facilitating the origin of elastic recoil. The feeding functional morphology of (b) pipefish and (c) snipefish are similar, but also notably different. These differences could hint at parallel evolution of elastic recoil among lineages or simply be a consequence of evolutionary divergence.