Suction feeding is a dominant prey-capture strategy across actinopterygians, consisting of a rapid expansion of the mouth cavity that drives a flow of water containing the prey into the mouth. Suction feeding is a power-hungry behavior, involving the actuation of cranial muscles as well as the anterior third of the fish's swimming muscles. Seahorses, which have reduced swimming muscles, evolved a unique mechanism for elastic energy storage that powers their suction flows. This mechanism allows seahorses to achieve head rotation speeds that are 50 times faster than fish lacking such a mechanism. However, it is unclear how the dynamics of suction flows in seahorses differ from the conserved pattern observed across other actinopterygians, nor how differenced in snout length across seahorses affect these flows. Using flow visualization experiments, we show that seahorses generate suction flows that are 8 times faster than similar-sized fish, and that the temporal patterns of cranial kinematics and suction flows in seahorses differs from the conserved pattern observed across other actinopterygians. However, the spatial patterns retain the conserved actinopterygian characteristics, where suction flows impact a radially symmetric region of ∼1 gape diameter outside the mouth. Within seahorses, increases in snout length were associated with slower suction flows and faster head rotation speeds, resulting in a trade-off between pivot feeding and suction feeding. Overall, this study shows how the unique cranial kinematics in seahorses are manifested in their suction feeding performance, and highlights the trade-offs associated with their unique morphology and mechanics.

Ubiquitous constraints derived from the muscle's structure limit the power capacity of fast contracting muscles. Correspondingly, organisms evolved elastic elements that store energy which, when released, can be used to rapidly accelerate appendages. Such latch-mediated spring actuation (LaMSA) systems comprise of a single elastic element and are used to actuate a single mass. Here we reveal a dual LaMSA system in seahorses, in which two elastic elements actuate two masses: the head as they rapidly swing it towards the prey, and the water mass sucked into the mouth to prevent the prey from escaping. This power-amplified system enhances the speeds of both head rotation and suction flows by x10 compared to similarly-sized fish. Furthermore, the dual system provides temporal coordination between head rotation and suction flows, a novel function for LaMSA. These findings extend the known function, capacity and design of LaMSA systems.

Throughout evolution, organisms repeatedly developed elastic elements to power explosive body motions, overcoming ubiquitous limits on the power capacity of fast-contracting muscles. Seahorses evolved such a latch-mediated spring-actuated (LaMSA) mechanism; however, it is unclear how this mechanism powers the two complementary functions necessary for feeding: rapidly swinging the head towards the prey, and sucking water into the mouth to entrain it. Here, we combine flow visualization and hydrodynamic modelling to estimate the net power required for accelerating the suction feeding flows in 13 fish species. We show that the mass-specific power of suction feeding in seahorses is approximately three times higher than the maximum recorded from any vertebrate muscle, resulting in suction flows that are approximately eight times faster than similar-sized fishes. Using material testing, we reveal that the rapid contraction of the sternohyoideus tendons can release approximately 72% of the power needed to accelerate the water into the mouth. We conclude that the LaMSA system in seahorses is powered by two elastic elements, the sternohyoideus and epaxial tendons. These elements jointly actuate the coordinated acceleration of the head and the fluid in front of the mouth. These findings extend the known function, capacity and design of LaMSA systems.