Work that body: fin and body movements determine herbivore feeding performance within the natural reef environment

Abstract

Herbivorous fishes form a keystone component of reef ecosystems, yet the functional mechanisms underlying their feeding performance are poorly understood. In water, gravity is counter-balanced by buoyancy, hence fish are recoiled backwards after every bite they take from the substrate. To overcome this recoil and maintain contact with the algae covered substrate, fish need to generate thrust while feeding. However, the locomotory performance of reef herbivores in the context of feeding has hitherto been ignored. We used a three-dimensional high-speed video system to track mouth and body kinematics during in situ feeding strikes of fishes in the genus Zebrasoma, while synchronously recording the forces exerted on the substrate. These herbivores committed stereotypic and coordinated body and fin movements when feeding off the substrate and these movements determined algal biomass removed. Specifically, the speed of rapidly backing away from the substrate was associated with the magnitude of the pull force and the biomass of algae removed from the substrate per feeding bout. Our new framework for measuring biting performance in situ demonstrates that coordinated movements of the body and fins play a crucial role in herbivore foraging performance and may explain major axes of body and fin shape diversification across reef herbivore guilds.

Keywords: biting; body kinematics; fish feeding; herbivorous fish.

Figure 1.

Documenting in situ feeding kinematics of herbivorous reef fishes feeding in the Red Sea. (a) An aerial view of the fringing reef and algal turfs at the study site, the Interuniversity Institute for Marine Sciences (IUI) in Eilat, Israel. (b) The underwater video system, positioned on the algal turf, was comprised of two high speed cameras and a synchronized force transducer. The system allowed the three-dimensional tracking of the movements of the fish's body, fins and mouth during feeding, while simultaneously measuring the forces they exerted on a feeding plate naturally colonized by turf algae. (c) We focused on two species of Acanthuridae, Zebrasoma xanthurum (left) and Zebrasoma desjardinii (right), both characterized by a deep body shape, elongated dorsal and anal fins, protruding snout and a small mouth, as well as serrated teeth that allow them to tear algae. Photos by (a) Yoav Lindman and (c) François Libert. (Online version in colour.)

Figure 2.

Zebrasoma xanthurum, a browsing herbivorous fish, feeding from the substrate. Biting the substrate constitutes a mouth ‘opening phase’ that spans from the initiation of mouth opening until peak gape; a mouth ‘closing phase’ that spans from peak gape until the mouth is closed, and a ‘post mouth closer’ phase in which a rapid ‘head-flick’ is performed upon breaking contact with the substrate. Biting from the substrate is followed by transporting the detached algae into the mouth using rapid mouth opening to generate suction flows. See ‘video analysis’ subsection in the electronic supplementary material for complete description of the phases within a feeding event.

Figure 3.

Stereotypic mouth and body kinematics are reflected in the force exerted on the substrate. (a) An example from a single feeding event, depicting gape size, head angle with respect to the body, and the force exerted on the substrate throughout the event. A compression (push) force is assigned positive values and tension (pull) assigned negative ones. Grey shading represents the different phases of the feeding event (figure 2; see the electronic supplementary material, ‘video analysis’). GO, gape opening; PG, peak gape; GC, gape closing; HF, head-flick. The mouth is opened twice during the feeding event, once before biting the algae and once for prey transport. (b) The distribution of the timing of events during 40 bites, standardized to the time of contact with the feeding plate (i.e. contact defined as t = 0). Mouth opening occurs well before contact with the substrate, which coincides with mouth closing and peak push force. Peak pulling force is associated with the lateral movement of the head during ‘head flick’. Data is for 40 bites from 16 fishes. Boxes encompass first to third quartiles, horizontal line is the median, whiskers are 1.5 times the inter-quartile range. (Online version in colour.)

Figure 4.

Bites are characterized by fast body kinematics whereas transport events are characterized by fast mouth kinematics. A discriminant function analysis (error rate = 0.039; 73 of 76 events correctly assigned) revealed that bite and transport kinematics are significantly discriminated based on four mouth-related and two body-related variables: (a) time to peak gape was faster during transport while the post mouth-closure (PMC) angular speed of the head was faster following bites, (b) gape opening speed was faster during transports and the PMC angular speed of the pectoral fin was faster following bites, and (c) time to mouth closing (TTMC) was faster during transport, whereas peak gape was larger during bites. PMC head and pectoral fin angular speeds were measured starting when the fish broke contact with the feeding plate (for biting; also termed ‘flick phase’), or once the mouth was completely closed (for transport). The duration of the measurement was 0.04 s in both cases. (Online version in colour.)

Figure 5.

Body speed determines the pull force exerted on the substrate, and that force determines feeding success. (a) Fish body speed post mouth-closure was significantly correlated (p < 0.004) with the pulling force exerted on the substrate (linear mixed effect model, p < 0.05, marginal R² = 0.17). Depicted are the partial effects from the mixed-effect model. (b) The log of the total pulling force exerted on the plate was significantly correlated with the log of the total weight of algae removed during a feeding bout (permutation based linear model, p < 0.015, R² = 0.16). (c) The size of fish gape during contact with the algae did not have a significant effect on the pulling force exerted on the substrate. (d) A feeding plate, covered by natural algae, before and after a feeding bout. (Online version in colour.)