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ABSTRACT Understanding how organismal traits determine performance and, ultimately, fitness is a fundamental goal of evolutionary eco-morphology. However, multiple traits can interact in non-linear and context-dependent ways to affect performance, hindering efforts to place natural populations with respect to performance peaks or valleys. Here, we used an established mechanistic model of suction-feeding performance (SIFF) derived from hydrodynamic principles to estimate a theoretical performance landscape for zooplankton prey capture. This performance space can be used to predict prey capture performance for any combination of six morphological and kinematic trait values. We then mapped in situ high-speed video observations of suction feeding in a natural population of a coral reef zooplanktivore, Chromis viridis, onto the performance space to estimate the population's location with respect to the topography of the performance landscape. Although the kinematics of the natural population closely matched regions of high performance in the landscape, the population was not located on a performance peak. Individuals were furthest from performance peaks on the peak gape, ram speed and mouth opening speed trait axes. Moreover, we found that the trait combinations in the observed population were associated with higher performance than expected by chance, suggesting that these combinations are under selection. Our results provide a framework for assessing whether natural populations occupy performance optima. 

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. 

Abstract Suction feeding has evolved independently in two highly disparate animal and plant systems, aquatic vertebrates and carnivorous bladderworts. We review the suction performance of animal and plant suction feeders to explore biomechanical performance limits for aquatic feeders based on morphology and kinematics, in the context of current knowledge of suction feeding. While vertebrates have the greatest diversity and size range of suction feeders, bladderworts are the smallest and fastest known suction feeders. Body size has profound effects on aquatic organismal function, including suction feeding, particularly in the intermediate flow regime that tiny organisms can experience. A minority of tiny organisms suction feed, consistent with model predictions that generating effective suction flow is less energetically efficient and also requires more flow-rate specific power at small size. Although the speed of suction flows generally increases with body and gape size, some specialized tiny plant and animal predators generate suction flows greater than those of suction feeders 100 times larger. Bladderworts generate rapid flow via high-energy and high-power elastic recoil and suction feed for nutrients (relying on photosynthesis for energy). Small animals may be limited by available muscle energy and power, although mouth protrusion can offset the performance cost of not generating high suction pressure. We hypothesize that both the high energetic costs and high power requirements of generating rapid suction flow shape the biomechanics of small suction feeders, and that plants and animals have arrived at different solutions due in part to their different energy budgets.