The swim-and-sink behaviour of copepods: a revisit to mechanical power requirement and a new hypothesis on function.

Many copepods display a swim-and-sink behaviour, which is not energetically efficient but probably aids in perceiving and capturing diatom chains. Here, computational fluid dynamics was employed to calculate the mechanical power required by a negatively buoyant, self-propelled copepod in swim-and-sink versus hovering. The results show that upward swim-and-sink about a fixed depth always demands more power than hovering. Subsequently, high-speed microscale imaging was employed to observe the copepod Centropages sp. in swim-and-sink, specifically its encounter and handling of diatom chains for capture, along with the measured alternating swimming and sinking currents imposed by the swim-and-sink copepod. The findings suggest that during upward swimming, the copepod uses its swimming current to scan the fluid for detecting embedded diatom chains, presumably through chemoreception. Once a diatom chain is perceived, the copepod sinks and uses its sinking current to manipulate the orientation of the diatom chain before swimming upward to capture it. Overall, these results propose a hypothesis that swim-and-sink is an innate behaviour that assists copepods in perceiving and manoeuvring diatom chains for capture. In contrast with near-spherical algae, diatom chains predominately exhibit a horizontal orientation in the ocean, necessitating vertically oriented copepods to possess a handling behaviour that manoeuvres diatom chains for capture.

Feeling for food: Can rostro-mental hair arrays sense hydrodynamic cues for foraging North Atlantic right whales?

North Atlantic right whales (NARWs; Eubalaena glacialis) possess an arrangement of fine hairs on the rostrum and chin that may be used for hydrodynamic sensing during feeding. These hairs occur across mysticete species and are known to possess adequate innervation in the subdermal follicle to support their consideration as sensory hairs (vibrissae). However, the small size of the hair structure with respect to the enormous scale of the animal's body has caused doubts regarding their utility and prompted speculation that the hairs may be vestigial or minimally functional. Here we show that NARW hairs occur in abundance on the leading surface of the head in a unique and characteristic arrangement. We consider the sensory hairs in context of the fluid environment in which this species forages and argue that the size of the hair is scaled to the size of the animal's small planktonic prey, thus suggesting that the hairs play an important role in the sensory ecology of these animals.

Copepod feeding strategy determines response to seawater viscosity: videography study of two calanoid copepod species.

Calanoid copepods, depending on feeding strategy, have different behavioral and biological controls on their movements, thereby responding differently to environmental conditions such as changes in seawater viscosity. To understand how copepod responses to environmental conditions are mediated through physical, physiological and/or behavioral pathways, we used high-speed microvideography to compare two copepod species, Acartia hudsonica and Parvocalanus crassirostris, under different temperature, viscosity and dietary conditions. Acartia hudsonica exhibited 'sink and wait' feeding behavior and typically responded to changes in seawater viscosity; increased seawater viscosity reduced particle-capture behavior and decreased the size of the feeding current. In contrast, P. crassirostris continuously swam and did not show any behavioral or physical responses to changes in viscosity. Both species showed a physiological response to temperature, with reduced appendage beating frequency at cold temperatures, but this did not generally translate into effects on swimming speed, feeding flux or active time. Both copepod species swam slower when feeding on diatom rather than dinoflagellate prey, showing that prey type mediates copepod behavior. These results differentiate species-specific behaviors and responses to environmental conditions, which may lead to better understanding of niche separation and latitudinal patterns in copepod feeding and movement strategies.

Oscillations in the near-field feeding current of a calanoid copepod are useful for particle sensing.

Calanoid copepods are small crustaceans that constitute a major element of aquatic ecosystems. Key to their success is their feeding apparatus consisting of sensor-studded mouth appendages that are in constant motion. These appendages generate a feeding current to enhance the encounter probability with food items. Additionally, sensing enables the organism to determine the position and quality of food particles, and to alter the near-field flow to capture and manipulate the particles for ingestion or rejection. Here we observe a freely swimming copepod Leptodiaptomus sicilis in multiple perspectives together with suspended particles that allow us to analyse the flow field created by the animal. We observe a highly periodic motion of the mouth appendages that is mirrored in oscillations of nearby tracer particles. We propose that the phase shift between the fluid and the particle velocities is sufficient for mechanical detection of the particles entrained in the feeding current. Moreover, we propose that an immersed algal cell may benefit from the excitation by increased uptake of dissolved inorganic compounds.

Canal neuromasts enhance foraging in zebrafish (Danio rerio).

Aquatic animals commonly sense flow using superficial neuromasts (SNs), which are receptors that extend from the body's surface. The lateral line of fishes is unique among these systems because it additionally possesses receptors, the canal neuromasts (CNs), that are recessed within a channel. The lateral line has inspired the development of engineered sensors and concepts in the analysis of flow fields for submersible navigation. The biophysics of CNs are known to be different from the SNs and thereby offer a distinct submodality. However, it is generally unclear whether CNs play a distinct role in behavior. We therefore tested whether CNs enhance foraging in the dark by zebrafish (Danio rerio), a behavior that we elicited with a vibrating rod. We found that juvenile fish, which have only SNs, bite at this rod at about one-third the rate and from as little as one-third the distance of adults for a high-frequency stimulus (50 < f  < 100 Hz). We used novel techniques for manipulating the lateral line in adults to find that CNs offered only a modest benefit at a lower frequency (20 Hz) and that foraging was mediated entirely by cranial neuromasts. Consistent with our behavioral results, biophysical models predicted CNs to be more than an order of magnitude more sensitive than SNs at high frequencies. This enhancement helps to overcome the rapid spatial decay in high-frequency components in the flow around the stimulus. These findings contrast what has been previously established for fishes that are at least ten-times the length of zebrafish, which use trunk CNs to localize prey. Therefore, CNs generally enhance foraging, but in a manner that varies with the size of the fish and its prey. These results have the potential to improve our understanding of flow sensing in aquatic animals and engineered systems.

Copepod manipulation of oil droplet size distribution.

Oil spills are one of the most dangerous sources of pollution in aquatic ecosystems. Owing to their pivotal position in the food web, pelagic copepods can provide crucial intermediary transferring oil between trophic levels. In this study we show that the calanoid Paracartia grani can actively modify the size-spectrum of oil droplets. Direct manipulation through the movement of the feeding appendages and egestion work in concert, splitting larger droplets (Ø = 16 µm) into smaller ones (Ø = 4-8 µm). The copepod-driven change in droplet size distribution can increase the availability of oil droplets to organisms feeding on smaller particles, sustaining the transfer of petrochemical compounds among different compartments. These results raise the curtain on complex small-scale interactions which can promote the understanding of oil spills fate in aquatic ecosystems.

The Land-Sea Breeze of the Red Sea: Observations, Simulations, and Relationships to Regional Moisture Transport.

Unique in situ observations of atmospheric conditions over the Red Sea and the coastal Arabian Peninsula are examined to study the dynamics and regional impacts of the local land-sea breeze cycle (LSBC). During a 26-month data record spanning 2008-2011, observed LSBC events occurred year-round, frequently exhibiting cross-shore wind velocities in excess of 8 m/s. Observed onshore and offshore features of both the land- and sea-breeze phases of the cycle are presented, and their seasonal modulation is considered. Weather Research and Forecasting climate downscaling simulations and satellite measurements are used to extend the analysis. In the model, the amplitude of the LSBC is significantly larger in the vicinity of the steeper terrain elements encircling the basin, suggesting an enhancement by the associated slope winds. Observed and simulated conditions also reflected distinct gravity-current characteristics of the intrinsic moist marine air mass during both phases of the LSBC. Specifically, the advance and retreat of marine air mass was directly tied to the development of internal boundary layers onshore and offshore throughout the period of study. Convergence in the lateral moisture flux resulting from this air mass ascending the coastal topography (sea-breeze phase) as well as colliding with air masses from the opposing coastline (land-breeze phase) further resulted in cumulous cloud formation and precipitation.

Behavioral and mechanistic characteristics of the predator-prey interaction between the dinoflagellate Dinophysis acuminata and the ciliate Mesodinium rubrum.

Predator-prey interactions of planktonic protists are fundamental to plankton dynamics and include prey selection, detection, and capture as well as predator detection and avoidance. Propulsive, morphology-specific behaviors modulate these interactions and therefore bloom dynamics. Here, interactions between the mixotrophic, harmful algal bloom (HAB) dinoflagellate Dinophysis acuminata and its ciliate prey Mesodinium rubrum were investigated through quantitative microvideography using a high-speed microscale imaging system (HSMIS). The dinoflagellate D. acuminata is shown to detect its M. rubrum prey via chemoreception while M. rubrum is alerted to D. acuminata via mechanoreception at much shorter distances (89 ±â€¯39 µm versus 41 ±â€¯32 µm). On detection, D. acuminata approaches M. rubrum with reduced speed. The ciliate M. rubrum responds through escape jumps that are long enough to detach its chemical trail from its surface, thereby disorienting the predator. To prevail, D. acuminata uses capture filaments and/or releases mucus to slow and eventually immobilize M. rubrum cells for easier capture. Mechanistically, results support the notion that the desmokont flagellar arrangement of D. acuminata lends itself to phagotrophy. In particular, the longitudinal flagellum plays a dominant role in generating thrust for the cell to swim forward, while at other times, it beats to supply a tethering or anchoring force to aid the generation of a posteriorly-directed, cone-shaped scanning current by the transverse flagellum. The latter is strategically positioned to generate flow for enhanced chemoreception and hydrodynamic camouflage, such that D. acuminata can detect and stealthily approach resting M. rubrum cells in the water column.

Overcoming hydrodynamic challenges in suspension feeding by juvenile Mya arenaria clams.

We present some of the few suspension-feeding measurements and to our knowledge the first velocity-field measurements for early post-settlement juvenile bivalve clams. We verify and extend our experimental results with numerical simulations. For 1.8-2.8 mm shell length Mya arenaria clams, pumping rates ranged 0.03-0.22 µl s-1, inhalant siphon Reynolds numbers (Re) ranged 0.16-0.79 and mean inhalant velocities ranged 0.8-3.2 mm s-1 Owing to the low Re at which they pump and the small diameters of their siphons, juvenile clams are subject to unique hydrodynamic challenges, including high siphon resistance and susceptibility to refiltration. At least three features of juvenile clam siphons differentiate them from those of adults-shorter inhalant siphon length, a more rapid increase in inhalant siphon diameter with shell length, and the presence of a prominent exhalant siphon extension. These features are probably adaptations to the challenges of suspension feeding at low Re.

A tale of the ciliate tail: investigation into the adaptive significance of this sub-cellular structure.

Ciliates can form an important link between the microbial loop and higher trophic levels primarily through consumption by copepods. This high predation pressure has resulted in a number of ciliate species developing rapid escape swimming behaviour. Several species of these escaping ciliates also possess a long contractile tail for which the functionality remains unresolved. We use high-speed video, specialized optics and novel fluid visualization tools to evaluate the role of this contractile appendage in two free-swimming ciliates, Pseudotontonia sp. and Tontonia sp., and compare the performance to escape swimming behaviour of a non-tailed species, Strobilidium sp. Here, we show that 'tailed' species respond to hydrodynamic disturbances with extremely short response latencies (less than or equal to 0.89 ms) by rapidly contracting the tail which carries the cell body 2-4 cell diameters within a few milliseconds. This provides an advantage over non-tailed species during the critical first 10-30 ms of an escape. Two small, short-lived vortex rings are created during contraction of the tail. The flow imposed by the ciliate jumping can be described as two well-separated impulsive Stokeslets and the overall flow attenuates spatially as r(-3). The high initial velocities and spatio-temporal arrangement of vortices created by tail contractions appear to provide a means for rapid escape as well as hydrodynamic 'camouflage' against fast striking, mechanoreceptive predators such as copepods.

Ontogenetic propulsive transitions by Sarsia tubulosa medusae.

While swimming in their natural environment, marine organisms must successfully forage, escape from predation, and search for mates to reproduce. In the process, planktonic organisms interact with their fluid environment, generating fluid signatures around their body and in their downstream wake through ontogeny. In the early stages of their life cycle, marine organisms operate in environments where viscous effects dominate and govern physical processes. Ontogenetic propulsive transitions in swimming organisms often involve dramatic changes in morphology and swimming behavior. However, for organisms that do not undergo significant changes in morphology, swimming behavior or propulsive mode, how is their swimming performance affected? We investigated the ontogenetic propulsive transitions of the hydromedusa Sarsia tubulosa, which utilizes jet propulsion and possesses a similar bell morphology throughout its life cycle. We used digital particle image velocimetry and high-speed imaging to measure the body kinematics, velocity fields and wake structures induced by swimming S. tubulosa with bell exit diameters from 1 to 10 mm. Our experimental observations revealed three distinct classes of hydrodynamic wakes: elongated vortex rings for 1030 (larger than 2 mm bell exit diameter) and elliptical vortex rings (or leading vortex rings) followed by trailing jets for most instances where Re>100 (larger than 4 or 5 mm bell exit diameter). The relative travel distance and propulsive efficiency remained unchanged throughout ontogeny, and the swimming proficiency and hydrodynamic cost of transport decreased non-linearly.

Predicting the response of the deep-ocean microbiome to geochemical perturbations by hydrothermal vents.

Submarine hydrothermal vents perturb the deep-ocean microbiome by injecting reduced chemical species into the water column that act as an energy source for chemosynthetic organisms. These systems thus provide excellent natural laboratories for studying the response of microbial communities to shifts in marine geochemistry. The present study explores the processes that regulate coupled microbial-geochemical dynamics in hydrothermal plumes by means of a novel mathematical model, which combines thermodynamics, growth and reaction kinetics, and transport processes derived from a fluid dynamics model. Simulations of a plume located in the ABE vent field of the Lau basin were able to reproduce metagenomic observations well and demonstrated that the magnitude of primary production and rate of autotrophic growth are largely regulated by the energetics of metabolisms and the availability of electron donors, as opposed to kinetic parameters. Ambient seawater was the dominant source of microbes to the plume and sulphur oxidisers constituted almost 90% of the modelled community in the neutrally-buoyant plume. Data from drifters deployed in the region allowed the different time scales of metabolisms to be cast in a spatial context, which demonstrated spatial succession in the microbial community. While growth was shown to occur over distances of tens of kilometers, microbes persisted over hundreds of kilometers. Given that high-temperature hydrothermal systems are found less than 100 km apart on average, plumes may act as important vectors between different vent fields and other environments that are hospitable to similar organisms, such as oil spills and oxygen minimum zones.

Prey fish escape by sensing the bow wave of a predator.

Prey fish possess a remarkable ability to sense and evade an attack from a larger fish. Despite the importance of these events to the biology of fishes, it remains unclear how sensory cues stimulate an effective evasive maneuver. Here, we show that larval zebrafish (Danio rerio) evade predators using an escape response that is stimulated by the water flow generated by an approaching predator. Measurements of the high-speed responses of larvae in the dark to a robotic predator suggest that larvae respond to the subtle flows in front of the predator using the lateral line system. This flow, known as the bow wave, was visualized and modeled with computational fluid dynamics. According to the predictions of the model, larvae direct their escape away from the side of their body exposed to more rapid flow. This suggests that prey fish use a flow reflex that enables predator evasion by generating a directed maneuver at high speed. These findings demonstrate a sensory-motor mechanism that underlies a behavior that is crucial to the ecology and evolution of fishes.

Flow disturbances generated by feeding and swimming zooplankton.

Interactions between planktonic organisms, such as detection of prey, predators, and mates, are often mediated by fluid signals. Consequently, many plankton predators perceive their prey from the fluid disturbances that it generates when it feeds and swims. Zooplankton should therefore seek to minimize the fluid disturbance that they produce. By means of particle image velocimetry, we describe the fluid disturbances produced by feeding and swimming in zooplankton with diverse propulsion mechanisms and ranging from 10-µm flagellates to greater than millimeter-sized copepods. We show that zooplankton, in which feeding and swimming are separate processes, produce flow disturbances during swimming with a much faster spatial attenuation (velocity u varies with distance r as u ∝ r(-3) to r(-4)) than that produced by zooplankton for which feeding and propulsion are the same process (u ∝ r(-1) to r(-2)). As a result, the spatial extension of the fluid disturbance produced by swimmers is an order of magnitude smaller than that produced by feeders at similar Reynolds numbers. The "quiet" propulsion of swimmers is achieved either through swimming erratically by short-lasting power strokes, generating viscous vortex rings, or by "breast-stroke swimming." Both produce rapidly attenuating flows. The more "noisy" swimming of those that are constrained by a need to simultaneously feed is due to constantly beating flagella or appendages that are positioned either anteriorly or posteriorly on the (cell) body. These patterns transcend differences in size and taxonomy and have thus evolved multiple times, suggesting a strong selective pressure to minimize predation risk.

Swimming speed of larval snail does not correlate with size and ciliary beat frequency.

Many marine invertebrates have planktonic larvae with cilia used for both propulsion and capturing of food particles. Hence, changes in ciliary activity have implications for larval nutrition and ability to navigate the water column, which in turn affect survival and dispersal. Using high-speed high-resolution microvideography, we examined the relationship between swimming speed, velar arrangements, and ciliary beat frequency of freely swimming veliger larvae of the gastropod Crepidula fornicata over the course of larval development. Average swimming speed was greatest 6 days post hatching, suggesting a reduction in swimming speed towards settlement. At a given age, veliger larvae have highly variable speeds (0.8-4 body lengths s(-1)) that are independent of shell size. Contrary to the hypothesis that an increase in ciliary beat frequency increases work done, and therefore speed, there was no significant correlation between swimming speed and ciliary beat frequency. Instead, there are significant correlations between swimming speed and visible area of the velar lobe, and distance between centroids of velum and larval shell. These observations suggest an alternative hypothesis that, instead of modifying ciliary beat frequency, larval C. fornicata modify swimming through adjustment of velum extension or orientation. The ability to adjust velum position could influence particle capture efficiency and fluid disturbance and help promote survival in the plankton.

To eat and not be eaten: optimal foraging behaviour in suspension feeding copepods.

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.

Plankton reach new heights in effort to avoid predators.

The marine environment associated with the air-water interface (neuston) provides an important food source to pelagic organisms where subsurface prey is limited. However, studies on predator-prey interactions within this environment are lacking. Copepods are known to produce strong escape jumps in response to predators, but must contend with a low-Reynolds-number environment where viscous forces limit escape distance. All previous work on copepod interaction with predators has focused on a liquid environment. Here, we describe a novel anti-predator behaviour in two neustonic copepod species, where individuals frequently exit the water surface and travel many times their own body length through air to avoid predators. Using both field recordings with natural predators and high-speed laboratory recordings, we obtain detailed kinematics of this behaviour, and estimate energetic cost associated with this behaviour. We demonstrate that despite losing up to 88 per cent of their initial kinetic energy, copepods that break the water surface travel significantly further than those escaping underwater and successfully exit the perceptive field of the predator. This behaviour provides an effective defence mechanism against subsurface-feeding visual predators and the results provide insight into trophic interactions within the neustonic environment.

The fluid dynamics of swimming by jumping in copepods.

Copepods swim either continuously by vibrating their feeding appendages or erratically by repeatedly beating their swimming legs, resulting in a series of small jumps. The two swimming modes generate different hydrodynamic disturbances and therefore expose the swimmers differently to rheotactic predators. We developed an impulsive stresslet model to quantify the jump-imposed flow disturbance. The predicted flow consists of two counter-rotating viscous vortex rings of similar intensity, one in the wake and one around the body of the copepod. We showed that the entire jumping flow is spatially limited and temporally ephemeral owing to jump-impulsiveness and viscous decay. In contrast, continuous steady swimming generates two well-extended long-lasting momentum jets both in front of and behind the swimmer, as suggested by the well-known steady stresslet model. Based on the observed jump-swimming kinematics of a small copepod Oithona davisae, we further showed that jump-swimming produces a hydrodynamic disturbance with much smaller spatial extension and shorter temporal duration than that produced by a same-size copepod cruising steadily at the same average translating velocity. Hence, small copepods in jump-swimming are in general much less detectable by rheotactic predators. The present impulsive stresslet model improves a previously published impulsive Stokeslet model that applies only to the wake vortex.