Teamwork in the viscous oceanic microscale.

Nutrient acquisition is crucial for oceanic microbes, and competitive solutions to solve this challenge have evolved among a range of unicellular protists. However, solitary solutions are not the only approach found in natural populations. A diverse array of oceanic protists form temporary or even long-lasting attachments to other protists and marine aggregates. Do these planktonic consortia provide benefits to their members? Here, we use empirical and modeling approaches to evaluate whether the relationship between a large centric diatom, Coscinodiscus wailesii, and a ciliate epibiont, Pseudovorticella coscinodisci, provides nutrient flux benefits to the host diatom. We find that fluid flows generated by ciliary beating can increase nutrient flux to a diatom cell surface four to 10 times that of a still cell without ciliate epibionts. This cosmopolitan species of diatom does not form consortia in all environments but frequently joins such consortia in nutrient-depleted waters. Our results demonstrate that symbiotic consortia provide a cooperative alternative of comparable or greater magnitude to sinking for enhancement of nutrient acquisition in challenging environments.

Predatory posture and performance in a precocious larval fish targeting evasive copepods.

Predatory fishes avoid detection by prey through a stealthy approach, followed by a rapid and precise fast-start strike. Although many first-feeding fish larvae strike at non-evasive prey using an S-start, the clownfish Amphiprion ocellaris feeds on highly evasive calanoid copepods from a J-shaped position, beginning 1 day post-hatch (dph). We quantified this unique strike posture by observing successful predatory interactions between larval clownfish (1 to 14 dph) and three developmental stages of the calanoid copepod Bestiolina similis The J-shaped posture of clownfish became less tightly curled (more L-shaped) during larval development. Larvae were also less tightly curled when targeting adult copepods, which are more evasive than younger copepod stages. Strike performance measured as time to capture and as peak speed improved only slightly with larval age. Therefore, the J-posture may allow first-feeding larvae to minimize disturbance during their approach of sensitive prey, and may represent an alternative predatory strategy to the prototypical S-start.

Escapes in copepods: comparison between myelinate and amyelinate species.

Rapid conduction in myelinated nerves keeps distant parts of large organisms in timely communication. It is thus surprising to find myelination in some very small organisms. Calanoid copepods, while sharing similar body plans, are evenly divided between myelinate and amyelinate taxa. In seeking the selective advantage of myelin in these small animals, representatives from both taxa were subjected to a brief hydrodynamic stimulus that elicited an escape response. The copepods differed significantly in their ability to localize the stimulus: amyelinate copepods escaped in the general direction of their original swim orientation, often ending up closer to the stimulus. However, myelinate species turned away from the stimulus and distanced themselves from it, irrespective of their original orientation. We suggest that faster impulse conduction of myelinated axons leads to better precision in the timing and processing of sensory information, thus allowing myelinate copepods to better localize stimuli and respond appropriately.

Olfaction in a viscous environment: the "color" of sexual smells in Temora longicornis.

We investigate chemical aspects of mating in the marine copepod Temora longicornis (Copepoda, Calanoidea). Our emphasis is the female pheromone signaling in form of well-defined trails for males to follow, observed in Doall et al. (Phil Trans R Soc Lond B 353:681-689, 1998). The viscous environment and the properties of the odorants play important roles as the spread of the pheromone trail limits the time during which it is useful for tracing. A key observation from our earlier work is the ability of a searching male to detect the direction of the female and to correct its swimming direction if necessary. We propose a simple mathematical model for the spread of a pheromone from a moving source and carry out numerical simulations of two possible detection mechanisms. We find that a searching agent that is capable to detect a ratio outperforms a searcher that depends on the gradient of a single compound. This suggests that copepod sex pheromones consist of blends of chemical compounds, and that a ratio detection mechanism similar to that in airborne insects is at work.

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.

Comparative analysis of Microcystis buoyancy in western Lake Erie and Saginaw Bay of Lake Huron.

Microcystis is the predominant genus of harmful cyanobacterium in both Lake Erie and Saginaw Bay of Lake Huron and has the capacity to regulate the buoyancy of its colonies, sinking under certain conditions while floating towards the surface in others. Understanding the factors that control buoyancy is critical for interpretation of remote sensing data, modeling and forecasting harmful algal blooms within these two systems. To determine if Microcystis colony buoyancy in the two lakes responds similarly to diurnal light cycles, colony buoyant velocity (floating/sinking terminal velocity in a quiescent water column) and size were measured after manipulating the intensity of sunlight. Overall, there were more positively buoyant (floating) colonies in Lake Erie while most of the colonies in Saginaw Bay were negatively buoyant (sinking). In Lake Erie the colonies became less buoyant at increased light intensities and were less buoyant in the afternoon than in the morning. In both lakes, apparent colony density was more variable among small colonies (< 200 µm), whereas larger colonies showed a diminished response of density to light intensity and duration. These findings suggest that colony density becomes less plastic as colonies increase in size, leading to a weak relationship between size and velocity. These relationships may ultimately affect how the bloom is transported throughout each system and will help explain observed differences in vertical distribution and movement of Microcystis in the two lakes.

Active hydrodynamic imaging of a rigid spherical particle.

A body with mechanical sensors may remotely detect particles suspended in the surrounding fluid via controlled agitation. Here we propose a sensory mode that relies on generating unsteady flow and sensing particle-induced distortions in the flow field. We demonstrate the basic physical principle in a simple analytical model, which consists of a small spherical particle at some distance from a plate undergoing impulsive or oscillatory motion. The model shows that changes in pressure or shear on the plate can be used to infer the location and size of the sphere. The key ingredient is to produce strong shear or strain around the sphere, which requires careful tuning of the viscous boundary layer on the moving plate. This elucidates how some organisms and devices may control their unsteady dynamics to enhance their range of perception.

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.

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.

Going with the flow: hydrodynamic cues trigger directed escapes from a stalking predator.

In the coevolution of predator and prey, different and less well-understood rules for threat assessment apply to freely suspended organisms than to substrate-dwelling ones. Particularly vulnerable are small prey carried with the bulk movement of a surrounding fluid and thus deprived of sensory information within the bow waves of approaching predators. Some planktonic prey have solved this apparent problem, however. We quantified cues generated by the slow approach of larval clownfish ( Amphiprion ocellaris) that triggered a calanoid copepod ( Bestiolina similis) to escape before the fish could strike. To estimate water deformation around the copepod immediately preceding its jump, we represented the body of the fish as a rigid sphere in a hydrodynamic model that we parametrized with measurements of fish size, approach speed and distance to the copepod. Copepods of various developmental stages (CII-CVI) were sensitive to the water flow caused by the live predator, at deformation rates as low as 0.04 s-1. This rate is far lower than that predicted from experiments that used artificial predator-mimics. Additionally, copepods localized the source, with 87% of escapes directed away (greater than or equal to 90°) from the predator. Thus, copepods' survival in life-threatening situations relied on their detection of small nonlinear signals within an environment of locally linear deformation.

Real-time assessment of fluid flow generated by appendage movements of Daphnia using standing square-wave chronamperometry.

Standing square-wave chronoamperometry (SSWCA) was applied to the analysis of the microfluid flow generated by the movement of the appendages of the Crustacea Daphnia. This novel approach provided for the first time real-time assessment and analysis of the breathing rate/fluid flow of individual organisms. An electrochemical tracer was delivered into the fluid inflow of the organism and a carbon fiber microelectrode placed in the fluid outflow's path. The variation of the net concentration/flux of the electroactive tracer, dopamine, at the electrode surface was measured with SSWCA. The observed chronoamperometric peaks (with fine structure) of the outflow are seen as a direct representation of appendage movement and, too, the workings and responses of the organism to its environment, e.g., external stimuli such as food or chemicals. It was concluded that SSWCA follows primarily the variation of the convective component of the Nernst-Plank equation for flux and, to lesser extent, diffusion and migration. In this work, SSWCA can clearly be used to monitor changes in the Daphnia-generated fluid outflow on a different time scale than was previously possible. This new application of SSWCA is faster and likely more accurate than using high-speed video.

Optimal foraging by zooplankton within patches: the case of Daphnia.

The motions of many physical particles as well as living creatures are mediated by random influences or 'noise'. One might expect that over evolutionary time scales internal random processes found in living systems display characteristics that maximize fitness. Here we focus on animal random search strategies [G.M. Viswanathan, S.V. Buldyrev, S. Havlin, M.G.E. Da Luz, E.P. Raposo, H.E. Stanley, Optimizing the success of random searches, Nature 401 (1999) 911-914; F. Bartumeus, J. Catalan, U.L. Fulco, M.L. Lyra, G.M. Viswanathan, Optimizing the encounter rate in biological interactions: Lévy versus Brownian stratagies, Phys. Rev. Lett. 88 (2002) 097901 and 89 (2002) 109902], and we describe experiments with the following Daphnia species: D. magna, D. galeata, D. lumholtzi, D. pulicaria, and D. pulex. We observe that the animals, while foraging for food, choose turning angles from distributions that can be described by exponential functions with a range of widths. This observation leads us to speculate and test the notion that this characteristic distribution of turning angles evolved in order to enhance survival. In the case of theoretical agents, some form of randomness is often introduced into search algorithms, especially when information regarding the sought object(s) is incomplete or even misleading. In the case of living animals, many studies have focused on search strategies that involve randomness [H.C. Berg, Random Walks in Biology, Princeton University, Princeton, New Jersey, 1993; A. Okubo, S.A. Levin (Eds.), Diffusion and Ecological Problems: Modern Perspectives, second ed., Springer, New York, 2001]. A simple theory based on stochastic differential equations of the motion backed up by a simulation shows that the collection of material (information, energy, food, supplies, etc.) by an agent executing Brownian-type hopping motions is optimized while foraging for a finite time in a supply patch of limited spatial size if the agent chooses turning angles taken from an exponential distribution with a specific stochastic intensity or 'noise width'. Search strategies that lead to optimization is a topic of high current interest across many disciplines [D. Wolpert, W. MacReady, No free lunch theorems for optimization, IEEE Transactions on Evolutionary Computation 1 (1997) 67].

Convex Grooves in Staggered Herringbone Mixer Improve Mixing Efficiency of Laminar Flow in Microchannel.

The liquid streams in a microchannel are hardly mixed to form laminar flow, and the mixing issue is well described by a low Reynolds number scheme. The staggered herringbone mixer (SHM) using repeated patterns of grooves in the microchannel have been proved to be an efficient passive micro-mixer. However, only a negative pattern of the staggered herringbone mixer has been used so far after it was first suggested, to the best of our knowledge. In this study, the mixing efficiencies from negative and positive staggered herringbone mixer patterns as well as from opposite flow directions were tested to investigate the effect of the micro-structure geometry on the surrounding laminar flow. The positive herringbone pattern showed better mixing efficiency than the conventionally used negative pattern. Also, generally used forward flow gives better mixing efficiency than reverse flow. The mixing was completed after two cycles of staggered herringbone mixer with both forward and reverse flow in a positive pattern. The traditional negative pattern showed complete mixing after four and five cycles in forward and reverse flow direction, respectively. The mixing effect in all geometries was numerically simulated, and the results confirmed more efficient mixing in the positive pattern than the negative. The results can further enable the design of a more efficient microfluidic mixer, as well as in depth understanding of the phenomena of positive and negative patterns existing in nature with regards to the surrounding fluids.

Statistical Mechanics of Zooplankton.

Statistical mechanics provides the link between microscopic properties of many-particle systems and macroscopic properties such as pressure and temperature. Observations of similar "microscopic" quantities exist for the motion of zooplankton, as well as many species of other social animals. Herein, we propose to take average squared velocities as the definition of the "ecological temperature" of a population under different conditions on nutrients, light, oxygen and others. We test the usefulness of this definition on observations of the crustacean zooplankton Daphnia pulicaria. In one set of experiments, D. pulicaria is infested with the pathogen Vibrio cholerae, the causative agent of cholera. We find that infested D. pulicaria under light exposure have a significantly greater ecological temperature, which puts them at a greater risk of detection by visual predators. In a second set of experiments, we observe D. pulicaria in cold and warm water, and in darkness and under light exposure. Overall, our ecological temperature is a good discriminator of the crustacean's swimming behavior.

Indium tin oxide-coated glass modified with reduced graphene oxide sheets and gold nanoparticles as disposable working electrodes for dopamine sensing in meat samples.

Sensitive, rapid, and accurate detection of dopamine (DA) at low cost is needed for clinical diagnostic and therapeutic purposes as well as to prevent illegal use of DA in animal feed. We employed a simple approach to synthesize reduced graphene oxide sheets (rGOS) and gold nanoparticles (AuNPs) at room temperature on indium tin oxide-coated glass (ITO) slides as disposable working electrodes for sensing DA. Graphene oxide (GO) was directly reduced on ITO to remove oxygenated species via a rapid and green process without using chemical reducing reagents. AuNPs were electrochemically deposited in situ on rGOS-ITO with fairly uniform density and size. The sensitivity of the AuNPs-rGOS-ITO sensor for DA detection is 62.7 µA mM(-1) cm(-2) with good selectivity against common electrochemically interfering species such as ascorbic acid (AA) and uric acid (UA), and the detection limit measured by differential pulse voltammetry (DPV), at a signal-noise ratio of 3, was 6.0 × 10(-8) M. The electrochemical catalysis of DA was proven to be a surface process with an electron transfer coefficient (α) of 0.478 and a rate constant (k(s)) of 1.456 s(-1). It correlates well with the conventional UV-vis spectrophotometric approach (R = 0.9973) but with more than thrice the dynamic range (up to 4.5 mM). The sensor also exhibited good stability and capability to detect DA in beef samples, and thus is a promising candidate for simple and inexpensive sub-nanomolar detection of DA, especially in the presence of UV-absorbing compounds.

The ciliate Paramecium shows higher motility in non-uniform chemical landscapes.

We study the motility behavior of the unicellular protozoan Paramecium tetraurelia in a microfluidic device that can be prepared with a landscape of attracting or repelling chemicals. We investigate the spatial distribution of the positions of the individuals at different time points with methods from spatial statistics and Poisson random point fields. This makes quantitative the informal notion of "uniform distribution" (or lack thereof). Our device is characterized by the absence of large systematic biases due to gravitation and fluid flow. It has the potential to be applied to the study of other aquatic chemosensitive organisms as well. This may result in better diagnostic devices for environmental pollutants.

Copepod flow modes and modulation: a modelling study of the water currents produced by an unsteadily swimming copepod.

Video observation has shown that feeding-current-producing calanoid copepods modulate their feeding currents by displaying a sequence of different swimming behaviours during a time period of up to tens of seconds. In order to understand the feeding-current modulation process, we numerically modelled the steady feeding currents for different modes of observed copepod motion behaviours (i.e. free sinking, partial sinking, hovering, vertical swimming upward and horizontal swimming backward or forward). Based on observational data, we also reproduced numerically a modulated feeding current associated with an unsteadily swimming copepod. We found that: (i) by changing its propulsive force, a copepod can switch between different swimming behaviours, leading to completely different flow-field patterns in self-generated surrounding flow; (ii) by exerting a time-varying propulsive force, a copepod can modulate temporally the basic flow modes to create an unsteady feeding current which manipulates precisely the trajectories of entrained food particles over a long time period; (iii) the modulation process may be energetically more efficient than exerting a constant propulsive force onto water to create a constant feeding current of a wider entrainment range. A probable reason is that the modulated unsteady flow entrains those water parcels containing food particles and leaves behind those without valuable food in them.

Planktonic copepods reacting selectively to hydrodynamic disturbances.

In the water column, planktonic copepods encounter small-scale hydrodynamic disturbances generated by fellow zooplankters. Our question is whether or not the copepods can distinguish between hydrodynamic disturbances created by predators, prey, conspecifics and/or mates. We used a Schlieren optical system with a density gradient in the water volume and filmed at 48 frames per second to record the behaviour of copepods during encounters with an artificial hydrodynamic disturbance. We observed the reactions of Cyclops scutifer and Epischura nordenskioldi towards disturbances of different strengths. We also re-examined an earlier report on tandem swimming in C. scutifer while attempting to mate, using novel mathematical tools to analyse possible correlations between the two mates. We conclude that the information within the hydrodynamic disturbances created by swimming zooplankters has enough content for differentiated reactions. We also suggest that the adaptive value of tandem swimming during mating results in offspring capable of executing escape reactions comparable in strength to the disturbances.

Behavioral and physiological changes in Daphnia magna when exposed to nanoparticle suspensions (titanium dioxide, nano-C60, and C60HxC70Hx).

Little is known aboutthe impact manufactured nanoparticles will have on aquatic organisms. Previously, we demonstrated that toxicity differs with nanoparticle type and preparation and observed behavioral changes upon exposure to the more lethal nanoparticle suspensions. In this experiment, we quantified these behavioral and physiological responses of Daphnia magna at sublethal nanoparticle concentrations. Titanium dioxide (TiO2) and fullerenes (nano-C60) were chosen for their potential use in technology. Other studies suggest that addition of functional groups to particles can affect their toxicity to cell cultures, but it is unknown if the same is true at the whole organism level. Therefore, a fullerene derivative, C60HxC70Hx, was also used to examine how functional groups affect Daphnia response. Using a high-speed camera, we quantified several behavior and physiological parameters including hopping frequency, feeding appendage and postabdominal curling movement, and heart rate. Nano-C60 was the only suspension to cause a significant change in heart rate. Exposure to both nano-C60 and C60HxC70Hx suspensions caused hopping frequency and appendage movement to increase. These results are associated with increased risk of predation and reproductive decline. They indicate that certain nanoparticle types may have impacts on population and food web dynamics in aquatic systems.