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Microscopic sessile suspension feeders live attached to surfaces and, by consuming bacteria-sized prey and by being consumed, they form an important part of aquatic ecosystems. Their environmental impact is mediated by their feeding rate, which depends on a self-generated feeding current. The feeding rate has been hypothesized to be limited by recirculating eddies that cause the organisms to feed from water that is depleted of food particles. However, those results considered organisms in still water, while ambient flow is often present in their natural habitats. We show, using a point-force model, that even very slow ambient flow, with speed several orders of magnitude less than that of the self-generated feeding current, is sufficient to disrupt the eddies around perpendicular suspension feeders, providing a constant supply of food-rich water. However, the feeding rate decreases in external flow at a range of non-perpendicular orientations due to the formation of recirculation structures not seen in still water. We quantify the feeding flow and observe such recirculation experimentally for the suspension feeder Vorticella convallaria in external flows typical of streams and rivers.

Unicellular flagellated protists are a key element in aquatic microbial food webs. They all use flagella to swim and to generate feeding currents to encounter prey and enhance nutrient uptake. At the same time, the beating flagella create flow disturbances that attract flow-sensing predators. Protists have highly diverse flagellar arrangements in terms of number of flagella and their position, beat pattern, and kinematics, but it is unclear how the various arrangements optimize the fundamental trade-off between resource acquisition and predation risk. Here we describe the near-cell flow fields produced by 15 species and demonstrate consistent relationships between flagellar arrangement and swimming speed and between flagellar arrangement and flow architecture, and a trade-off between resource acquisition and predation risk. The flow fields fall in categories that are qualitatively described by simple point force models that include the drag force of the moving cell body and the propulsive forces of the flagella. The trade-off between resource acquisition and predation risk varies characteristically between flow architectures: Flagellates with multiple flagella have higher predation risk relative to their clearance rate compared to species with only one active flagellum, with the exception of the highly successful dinoflagellates that have simultaneously achieved high clearance rates and stealth behavior due to a unique flagellar arrangement. Microbial communities are shaped by trade-offs and environmental constraints, and a mechanistic explanation of foraging trade-offs is a vital part of understanding the eukaryotic communities that form the basis of pelagic food webs., Competing Interests: The authors declare no competing interest.

Many planktonic suspension feeders are attached to particles or tethered by gravity when feeding. It is commonly accepted that the feeding flows of tethered suspension feeders are stronger than those of their freely swimming counterparts. However, recent flow simulations indicate the opposite, and the cause of the opposing conclusions is not clear. To explore the effect of tethering on suspension feeding, we use a low-Reynolds-number flow model. We find that it is favorable to be freely swimming instead of tethered since the resulting feeding flow past the cell body is stronger, leading to a higher clearance rate. Our result underscores the significance of the near-field flow in shaping planktonic feeding modes, and it suggests that organisms tether for reasons that are not directly fluid dynamical (e.g., to stay near surfaces where the concentration of bacterial prey is high)., Competing Interests: The authors declare no competing interest., (Copyright © 2020 the Author(s). Published by PNAS.)

Most marine plankton have a high energy (carbon) density, but some are gelatinous with approximately 100 times more watery bodies. How do those distinctly different body plans emerge, and what are the trade-offs? We address this question by modeling the energy budget of planktonic filter feeders across life-forms, from micron-sized unicellular microbes such as choanoflagellates to centimeter-sized gelatinous tunicates such as salps. We find two equally successful strategies, one being small with high energy density (dense dwarf) and the other being large with low energy density (gelatinous giant). The constraint that forces large-but not small-filter feeders to be gelatinous is identified as a lower limit to the size-specific filter area, below which the energy costs lead to starvation. A further limit is found from the maximum size-specific motor force that restricts the access to optimum strategies. The quantified constraints are discussed in the context of other resource-acquisition strategies. We argue that interception feeding strategies can be accessed by large organisms only if they are gelatinous. On the other hand, organisms that use remote prey sensing do not need to be gelatinous, even if they are large.

Microbial filter feeders are an important group of grazers, significant to the microbial loop, aquatic food webs, and biogeochemical cycling. Our understanding of microbial filter feeding is poor, and, importantly, it is unknown what force microbial filter feeders must generate to process adequate amounts of water. Also, the trade-off in the filter spacing remains unexplored, despite its simple formulation: A filter too coarse will allow suitably sized prey to pass unintercepted, whereas a filter too fine will cause strong flow resistance. We quantify the feeding flow of the filter-feeding choanoflagellate Diaphanoeca grandis using particle tracking, and demonstrate that the current understanding of microbial filter feeding is inconsistent with computational fluid dynamics (CFD) and analytical estimates. Both approaches underestimate observed filtration rates by more than an order of magnitude; the beating flagellum is simply unable to draw enough water through the fine filter. We find similar discrepancies for other choanoflagellate species, highlighting an apparent paradox. Our observations motivate us to suggest a radically different filtration mechanism that requires a flagellar vane (sheet), something notoriously difficult to visualize but sporadically observed in the related choanocytes (sponges). A CFD model with a flagellar vane correctly predicts the filtration rate of D. grandis , and using a simple model we can account for the filtration rates of other microbial filter feeders. We finally predict how optimum filter mesh size increases with cell size in microbial filter feeders, a prediction that accords very well with observations. We expect our results to be of significance for small-scale biophysics and trait-based ecological modeling., Competing Interests: The authors declare no conflict of interest.

Zooplankton feed on microscopic prey that they either entrain in a feeding current or encounter as they cruise through the water. They generate fluid disturbances as they feed and move, thus elevating their risk of being detected and encountered by predators. Different feeding modes generate different hydrodynamic signals to predators and different predator encounter speeds but may also differ in their efficiency; the optimal behaviour is that which maximizes the net energy gain over the predation risk. Here, we show by means of flow visualization and simple hydrodynamic and optimization models that copepods with a diversity of feeding behaviours converge on optimal, size-independent specific clearance rates that are consistent with observed clearance rates of zooplankton, irrespective of feeding mode, species and size. We also predict magnitudes and size-scaling of swimming speeds that are consistent with observations. The rationalization of the magnitude and scaling of the clearance rates of zooplankton makes it more suitable for development of models of marine ecosystems, and is particularly relevant in predicting the size structure and biomass of pelagic communities.

Copepod nauplii are either ambush feeders that feed on motile prey or they produce a feeding current that entrains prey cells. It is unclear how ambush and feeding-current feeding nauplii perceive and capture prey. Attack jumps in ambush feeding nauplii should not be feasible at low Reynolds numbers due to the thick viscous boundary layer surrounding the attacking nauplius. We use high-speed video to describe the detection and capture of phytoplankton prey by the nauplii of two ambush feeding species (Acartia tonsa and Oithona davisae) and by the nauplii of one feeding-current feeding species (Temora longicornis). We demonstrate that the ambush feeders both detect motile prey remotely. Prey detection elicits an attack jump, but the jump is not directly towards the prey, such as has been described for adult copepods. Rather, the nauplius jumps past the prey and sets up an intermittent feeding current that pulls in the prey from behind towards the mouth. The feeding-current feeding nauplius detects prey arriving in the feeding current but only when the prey is intercepted by the setae on the feeding appendages. This elicits an altered motion pattern of the feeding appendages that draws in the prey.

Zooplankton is a morphologically and taxonomically diverse group and includes organisms that vary in size by many orders of magnitude, but they are all faced with the common problem of collecting food from a very dilute suspension. In order to maintain a viable population in the face of mortality, zooplankton in the ocean have to clear daily a volume of ambient water for prey particles that is equivalent to about 10(6) times their own body volume. While most size-specific vital rates and mortality rates decline with size, the clearance requirement is largely size-independent because food availability also declines with size. There is a limited number of solutions to the problem of concentrating dilute prey from a sticky medium: passive and active ambush feeding; feeding-current feeding, where the prey is either intercepted directly, retained on a filter, or individually perceived and extracted from the feeding current; cruise feeding; and colonization of large particles and marine snow aggregates. The basic mechanics of these food-collection mechanisms are described, and it is shown that their efficiencies are inherently different and that each of these mechanisms becomes less efficient with increasing size. Mechanisms that compensate for this decline in efficiency are described, including inflation of feeding structures and development of vision. Each feeding mode has implications beyond feeding in terms of risk of encountering predators and chance of meeting mates, and they partly target different types of prey. The main dichotomy is between (inefficient) ambush feeding on motile prey and the more efficient active feeding modes; a secondary dichotomy is between (efficient) hovering and (less efficient) cruising feeding modes. The efficiencies of the various feeding modes are traded off against feeding-mode-dependent metabolic expenses, predation risks, and mating chances. The optimality of feeding strategies, evaluated as the ratio of gain over risk, varies with the environment, and may explain both size-dependent and spatio-temporal differences in distributions of various feeding types as well as other aspects of the biology of zooplankton (mating behaviour, predator defence strategies)., (© 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society.)

Zooplankton feed in any of three ways: they generate a feeding current while hovering, cruise through the water or are ambush feeders. Each mode generates different hydrodynamic disturbances and hence exposes the grazers differently to mechanosensory predators. Ambush feeders sink slowly and therefore perform occasional upward repositioning jumps. We quantified the fluid disturbance generated by repositioning jumps in a millimetre-sized copepod (Re ∼ 40). The kick of the swimming legs generates a viscous vortex ring in the wake; another ring of similar intensity but opposite rotation is formed around the decelerating copepod. A simple analytical model, that of an impulsive point force, properly describes the observed flow field as a function of the momentum of the copepod, including the translation of the vortex and its spatial extension and temporal decay. We show that the time-averaged fluid signal and the consequent predation risk is much less for an ambush-feeding than a cruising or hovering copepod for small individuals, while the reverse is true for individuals larger than about 1 mm. This makes inefficient ambush feeding feasible in small copepods, and is consistent with the observation that ambush-feeding copepods in the ocean are all small, while larger species invariably use hovering or cruising feeding strategies.

Many marine zooplankters, particularly among copepods, are "ambush feeders" that passively wait for their prey and capture them by fast surprise attacks. This strategy must be very demanding in terms of muscle power and sensing capabilities, but the detailed mechanisms of the attacks are unknown. Using high-speed video we describe how copepods perform spectacular attacks by precision maneuvering during a rapid jump. We show that the flow created by the attacking copepod is so small that the prey is not pushed away, and that the attacks are feasible because of their high velocity (approximately 100 mm x s(-1)) and short duration (few ms), which leaves the prey no time for escape. Simulations and analytical estimates show that the viscous boundary layer that develops around the attacking copepod is thin at the time of prey capture and that the flow around the prey is small and remains potential flow. Although ambush feeding is highly successful as a feeding strategy in the plankton, we argue that power requirements for acceleration and the hydrodynamic constraints restrict the strategy to larger (> 0.25 mm), muscular forms with well-developed prey perception capabilities. The smallest of the examined species is close to this size limit and, in contrast to the larger species, uses its largest possible jump velocity for such attacks. The special requirements to ambush feeders with such attacks may explain why this strategy has evolved to perfection only a few times among planktonic suspension feeders (few copepod families and chaetognaths).