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 () 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.

Beyond power amplification: latch-mediated spring actuation is an emerging framework for the study of diverse elastic systems

“…In the latched conformation during spring loading, the head cannot be raised. With a slight shift in geometric conformation, the torque reverses on the lower linkages, and enables the release of stored elastic energy to drive rapid head elevation (Longo et al, 2018). with high force, not with high power.…”

“…As with springs, initial hypotheses for latch mechanisms emerge from direct observations of moving structures in or on the organism. This is often coupled with morphological descriptions, ranging from dissections to micro-computed tomography (Evans, 1972;Patek et al, 2007;Larabee et al, 2017;Longo et al, 2018). While these descriptive approaches can be compelling, additional evidence is required to discriminate among hypothesized latch mechanisms.…”

“…Some fluidic latches can be detected as a pressure increase prior to movement followed by a rapid decrease once movement begins (Singh et al, 2011). Geometric latches can be inferred by demonstrating shifts in mechanical advantage or the direction of torques that occur during different phases of movement (Astley and Roberts, 2014;Kaji et al, 2018;Longo et al, 2018).…”

“…With a contact latch, the shape and removal speed of the latch strongly influence system output (Ilton et al, 2018;Bolmin et al, 2019); however, tribological analyses of contact latches are still needed. Parameters such as droplet surface separation or rupture force are relevant for fluidic latches (Noblin et al, 2009;Liu et al, 2017), whereas linkage lengths and mechanical advantage are important for geometric latches (Koh et al, 2013;Longo et al, 2018;Olberding et al, 2019). It is as yet unknown which geometries, materials or dynamic features characterize effective latches and their roles across different situations.…”

Rapid adaptive evolution of scale-eating kinematics to a novel ecological niche

“…Many changes accompany adaptation to a novel 55 niche, and previous studies have identified that shifts in behaviors (Bowman and Billeb 1965; Shifts in kinematic traits-particularly those which affect prey capture and feeding-are 61 especially promising, because they can provide biomechanical insights into the origins of novel 62 trophic niches. For example, some species of trap-jaw ants have evolved specialized latch, 63 spring, and trigger structures in their jaws which allow for rapid, power-amplified bites used to 64 capture prey items unavailable to other ant species (Patek et al 2006; Larabee and Suarez 2014); 65 power-amplified jaws in Syngnathiform fishes have evolved two different latch mechanisms for 66 specialization on evasive prey items (Longo et al 2018); and the Pacific leaping blenny (Alticus 67 arnoldorum) uniquely uses axial tail twisting to improve propulsion and stability for greater 68 jumping performance and terrestrial prey capture (Hsieh 2010). 69…”