Elastic energy storage in seahorses leads to a unique suction flow dynamics compared with other actinopterygians.

Corrine Avidan,Roi Holzman

doi:10.1242/jeb.236430

Abstract

ABSTRACTSuction 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 those of 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, or how differences 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 those of similar-sized fish, and that the temporal patterns of cranial kinematics and suction flows in seahorses differ 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.

Highlights

Suction feeding is a highly stereotypic feeding behavior employed by the majority of aquatic vertebrates, including fishes, amphibians, reptiles, birds and mammals (Bardet et al, 2013; Cundall et al, 1987; Enstipp et al, 2018; Jacobs and Holzman, 2018; Marshall et al, 2008; Muller and Osse, 1984; Werth, 2005)
Do suction flows differ between seahorses and non-latchmediated spring actuated (LaMSA) fishes? Flow visualization experiments (Fig. 2) revealed that peak flow speed in seahorses was 8 times faster than that in non-LaMSA fishes with a comparable gape diameter (Figs 2–5), as indicated by the significant effect of LaMSA on the slope of peak flow speed as a Statistical analyses We used new data collected for seahorses, as well as those previously published in Jacobs and Holzman (2018) for nonLaMSA fishes
To compare the magnitude of suction flows in seahorses with non-LaMSA fishes we ran a mixed-effect linear model, with peak flow speed at half-gape as the dependent variable, peak gape size and the presence of a LaMSA system as fixed factors along with their interaction, and species as a random factor

Summary

Introduction

Suction feeding is a highly stereotypic feeding behavior employed by the majority of aquatic vertebrates, including fishes, amphibians, reptiles, birds and mammals (Bardet et al, 2013; Cundall et al, 1987; Enstipp et al, 2018; Jacobs and Holzman, 2018; Marshall et al, 2008; Muller and Osse, 1984; Werth, 2005). This feeding behavior involves the predator closing the distance to the prey, rapidly opening its mouth and expanding the buccal cavity in order to draw water and the prey into their mouth. The mechanisms that drive suction feeding are phylogenetically conserved (i.e. reflecting the tendency of fish species to retain their ancestral traits; Kraft et al, 2007)

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