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Copepod nauplii move in a world dominated by viscosity. Their swimming-by-jumping propulsion mode, with alternating power and recovery strokes of three pairs of cephalic appendages, is fundamentally different from the way other microplankters move. Protozoans move using cilia or flagella, and copepodites are equipped with highly specialized swimming legs. In some species the nauplius may also propel itself more slowly through the water by beating and rotating the appendages in a different, more complex pattern. We use high-speed video to describe jumping and swimming in nauplii of three species of pelagic copepods: Temora longicornis, Oithona davisae and Acartia tonsa. The kinematics of jumping is similar between the three species. Jumps result in a very erratic translation with no phase of passive coasting and the nauplii move backwards during recovery strokes. This is due to poorly synchronized recovery strokes and a low beat frequency relative to the coasting time scale. For the same reason, the propulsion efficiency of the nauplii is low. Given the universality of the nauplius body plan, it is surprising that they seem to be inefficient when jumping, which is different from the very efficient larger copepodites. A slow-swimming mode is only displayed by T. longicornis. In this mode, beating of the appendages results in the creation of a strong feeding current that is about 10 times faster than the average translation speed of the nauplius. The nauplius is thus essentially hovering when feeding, which results in a higher feeding efficiency than that of a nauplius cruising through the water.

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.

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.)

The ecology of senescence in marine zooplankton is not well known. Here we demonstrate senescence effects in the marine copepod Oithona davisae and show how sex and sexual selection accelerate the rate of ageing in the males. We show that adult mortality increases and male mating capacity and female fertility decrease with age and that the deterioration in reproductive performance is faster for males. Males have a limited mating capacity because they can fertilize < 2 females day(-1) and their reproductive life span is 10 days on average. High female encounter rates in nature (>10 day(-1)), a rapid age-dependent decline in female fertility, and a high mortality cost of mating in males are conducive to the development of male choosiness. In our experiments males in fact show a preference for mating with young females that are 3 times more fertile than 30-day old females. We argue that this may lead to severe male-male competition for young virgin females and a trade-off that favours investment in mate finding over maintenance. In nature, mate finding leads to a further elevated mortality of males, because these swim rapidly in their search for attractive partners, further relaxing fitness benefits of maintenance investments. We show that females have a short reproductive period compared to their average longevity but virgin females stay fertile for most of their life. We interpret this as an adaptation to a shortage of males, because a long life increases the chance of fertilization and/or of finding a high quality partner. The very long post reproductive life that many females experience is thus a secondary effect of such an adaptation.

Chain formation is common among phytoplankton organisms but the underlying reasons and consequences are poorly understood. Here we show that chain formation is strongly impaired by waterborne cues from copepod grazers in the dinoflagellate Alexandrium tamarense. Chains of Alexandrium cells exposed to copepod cues responded by splitting into single cells or shorter chains. Motion analysis revealed significantly lower swimming velocities for single cells compared with chains, with two- to fivefold higher simulated predator encounter rates for two- and four-cell chains, respectively. In addition, the few remaining two-cell chains in grazed treatments were swimming at approximately half the speed of two-cell chains in treatments without grazers, which reduced encounter rates with grazers to values similar to that of single cells. Chain length plasticity and swimming behavior constitute unique mechanisms to reduce encounters with grazers. We argue that dinoflagellates can regulate the balance between motility and predator avoidance by adjusting chain length. The high predator encounter rate for motile chains may have contributed to the low prevalence of chain formation in motile phytoplankton compared with in nonmotile phytoplankton where chain formation is more common.

Pelagic copepods jump to relocate, to attack prey and to escape predators. However, there is a price to be paid for these jumps in terms of their energy costs and the hydrodynamic signals they generate to rheotactic predators. Using observed kinematics of various types of jumps, we computed the imposed flow fields and associated energetics of jumps by means of computational fluid dynamics simulations by modeling the copepod as a self-propelled body. The computational fluid dynamics simulation was validated by particle image velocimetry data. The flow field generated by a repositioning jump quickly evolves into two counter-rotating viscous vortex rings that are near mirror image of one another, one in the wake and one around the body of the copepod; this near symmetrical flow may provide hydrodynamic camouflage because it contains no information about the position of the copepod prey within the flow structure. The flow field associated with an escape jump sequence also includes two dominant vortex structures: one leading wake vortex generated as a result of the first jump and one around the body, but between these two vortex structures is an elongated, long-lasting flow trail with flow velocity vectors pointing towards the copepod; such a flow field may inform the predator of the whereabouts of the escaping copepod prey. High Froude propulsion efficiency (0.94-0.98) was obtained for individual power stroke durations of all simulated jumps. This is unusual for small aquatic organisms but is caused by the rapidity and impulsiveness of the jump that allows only a low-cost viscous wake vortex to travel backwards.

The recent invasion of the comb jelly Mnemiopsis leidyi into northern European waters is of major public and scientific concern. One of the key features making M. leidyi a successful invader is its high fecundity combined with fast growth rates. However, little is known about physiological limitations to its reproduction and consequent possible abiotic restrictions to its dispersal. To evaluate the invasion potential of M. leidyi into the brackish Baltic Sea we studied in situ egg production rates in different regions and at different salinities in the laboratory, representing the salinity gradient of the Baltic Sea. During October 2009 M. leidyi actively reproduced over large areas of the Baltic Sea. Egg production rates scaled with animal size but decreased significantly with decreasing salinity, both in the field (7-29) and in laboratory experiments (6-33). Temperature and zooplankton, i.e. food abundance, could not explain the observed differences. Reproduction rates at conditions representing the Kattegat, south western and central Baltic Sea, respectively, were 2.8 fold higher at the highest salinities (33 and 25) than at intermediate salinities (10 and 15) and 21 times higher compared from intermediate to the lowest salinity tested (6). Higher salinity areas such as the Kattegat, and to a lower extent the south western Baltic, seem to act as source regions for the M. leidyi population in the central Baltic Sea where a self-sustaining population, due to the low salinity, cannot be maintained.

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.

We describe the kinematics of escape jumps in three species of 0.3-3.0 mm-sized planktonic copepods. We find similar kinematics between species with periodically alternating power strokes and passive coasting and a resulting highly fluctuating escape velocity. By direct numerical simulations, we estimate the force and power output needed to accelerate and overcome drag. Both are very high compared with those of other organisms, as are the escape velocities in comparison to startle velocities of other aquatic animals. Thus, the maximum weight-specific force, which for muscle motors of other animals has been found to be near constant at 57 N (kg muscle)(-1), is more than an order of magnitude higher for the escaping copepods. We argue that this is feasible because most copepods have different systems for steady propulsion (feeding appendages) and intensive escapes (swimming legs), with the muscular arrangement of the latter probably adapted for high force production during short-lasting bursts. The resulting escape velocities scale with body length to power 0.65, different from the size-scaling of both similar sized and larger animals moving at constant velocity, but similar to that found for startle velocities in other aquatic organisms. The relative duration of the pauses between power strokes was observed to increase with organism size. We demonstrate that this is an inherent property of swimming by alternating power strokes and pauses. We finally show that the Strouhal number is in the range of peak propulsion efficiency, again suggesting that copepods are optimally designed for rapid escape jumps.

Sexual selection is potentially important in marine zooplankton, presumably the most abundant metazoans on earth, but it has never been documented. We examine the conditions for sexual selection through mate choice and describe mating preferences in relation to size in a marine zooplankter, the pelagic copepod Acartia tonsa. Males produce spermatophores at a rate (~1 day(-1)) much lower than known female encounter rates for most of the year and the decision to mate a particular female thus implies lost future opportunities. Female egg production increases with female size, and males mating larger females therefore sire more offspring per mating event. Similarly, females encounter males more frequently than they need to mate. Large males produce larger spermatophores than small males and the offspring production of female increases with the size of the spermatophore she receives. Additionally, large spermatophores allow females to fertilize eggs for a longer period. Thus, mating with large males reduces the female's need for frequent matings and she may sire sons that produce more offspring because size is heritable in copepods. Finally, we show that both males and females mate preferentially with large partners. This is the first demonstration of sexual selection by mate choice in a planktonic organism.

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).

Male copepods must swim to find females, but swimming increases the risk of meeting predators and is expensive in terms of energy expenditure. Here I address the trade-offs between gains and risks and the question of how much and how fast to swim using simple models that optimise the number of lifetime mate encounters. Radically different swimming strategies are predicted for different feeding behaviours, and these predictions are tested experimentally using representative species. In general, male swimming speeds and the difference in swimming speeds between the genders are predicted and observed to increase with increasing conflict between mate searching and feeding. It is high in ambush feeders, where searching (swimming) and feeding are mutually exclusive and low in species, where the matured males do not feed at all. Ambush feeding males alternate between stationary ambush feeding and rapid search swimming. Swimming speed and the fraction of time spent searching increase with food availability, as predicted. This response is different from the pattern in other feeding types. The swimming speeds of non-feeding males are predicted and observed to be independent of the magnitude of their energy storage and to scale with the square root of body length in contrast to the proportionality scaling in feeding copepods. Suspension feeding males may search and feed at the same time, but feeding is more efficient when hovering than when cruising. Therefore, females should mainly be hovering and males cruising, which is confirmed by observations. Differences in swimming behaviour between genders and feeding types imply different mortality rates and predict well the observed patterns in population sex ratios. Sex ratios may become so female-biased that male abundances limit population growth, demonstrating that behaviours that are optimal to the individual may be suboptimal to the population.

Marine snow aggregates are microbial hotspots that support high bacterial abundance and activities. We conducted laboratory experiments to compare cell-specific bacterial protein production (BPP) and protease activity between free-living and attached bacteria. Natural bacterial assemblages attached to model aggregates (agar spheres) had threefold higher BPP and two orders of magnitude higher protease activity than their free-living counterpart. These observations could be explained by preferential colonization of the agar spheres by bacteria with inherently higher metabolic activity and/or individual bacteria increasing their metabolism upon attachment to surfaces. In subsequent experiments, we used four strains of marine snow bacteria isolates to test the hypothesis that bacteria could up- and down-regulate their metabolism while on and off an aggregate. The protease activity of attached bacteria was 10-20 times higher than that of free-living bacteria, indicating that the individual strains could increase their protease activity within a short time (2 h) upon attachment to surfaces. Agar spheres with embedded diatom cells were colonized faster than plain agar spheres and the attached bacteria were clustered around the agar-embedded diatom cells, indicating a chemosensing response. Increased protease activity and BPP allow attached bacteria to quickly exploit aggregate resources upon attachment, which may accelerate remineralization of marine snow and reduce the downward carbon fluxes.

In this paper we consider the advective/diffusive transport of a solute near a hovering zooplankter. We approximate the fluid flow with that of a Stokeslet, corresponding to the plankter exerting a point force on the water, and assume that the plankter acts as a point source for the transported solute, located at the same point as the force. We find an analytical expression in closed form for the steady-state concentration of the solute. We also discuss the situation where the plankter performs Brownian motion. Finally we apply the results to the courtship of the marine copepod Pseudocalanus elongatus, where the male performs a mating dance below the hovering female. For this situation, our model supports the hypothesis that the mating dance is guided by the plume of a signalling pheromone.

Many planktonic organisms have motility patterns with correlation run lengths (distances traversed before direction changes) of the same order as their reaction distances regarding prey, mates and predators (distances at which these organisms are remotely detected). At these scales, the relative measure of run length to reaction distance determines whether the underlying encounter is ballistic or diffusive. Since ballistic interactions are intrinsically more efficient than diffusive, we predict that organisms will display motility with long correlation run lengths compared to their reaction distances to their prey, but short compared to the reaction distances of their predators. We show motility data for planktonic organisms ranging from bacteria to copepods that support this prediction. We also present simple ballistic and diffusive motility models for estimating encounter rates, which lead to radically different predictions, and we present a simple criterion to determine which model is the more appropriate in a given case.

I examine how the population biology of pelagic copepods depends on their mating biology using field data and a simple demographic model. Among calanoid copepods, two distinct patterns emerge. First, copepods that lack seminal receptacle and require repeated mating to stay fertilized have near equal adult sex ratios in field populations. Winter population densities are orders of magnitude less than the critical population density required for population persistence, but populations survive winter seasons as resting eggs in the sediment. Population growth in these species is potentially high because they have on average a factor of 2 higher egg production rates than other pelagic copepods. Second, other copepods require only one mating to stay fertile, and populations of these species have strongly female-skewed adult sex-ratios in field populations. Resting eggs have not been described within this group. Winter population sizes are well predicted by the critical density required for population persistence which, in turn, is closely related to the body-size-dependent mate-search capacity. Thus, the different requirements for mating lead in the first case to a more opportunistic reproductive strategy that implies rapid colonization of the pelagic during productive seasons, and in the second case to a strategy that allows maintenance of a pelagic populations during unproductive seasons. Positive density dependent population growth during periods of low population density ('Allee effect') amplifies population density variation during winter into the subsequent summer, thus explaining why summer densities appear to depend more on winter densities than on current growth opportunities in pelagic copepods.

Marine particles in the ocean are exposed to diverse bacterial communities, and colonization and growth of attached bacteria are important processes in the degradation and transformation of the particles. In an earlier study, we showed that the initial colonization of model particles by individual bacterial strains isolated from marine aggregates was a function of attachment and detachment. In the present study, we have investigated how this colonization process was further affected by growth and interspecific interactions among the bacteria. Long-term incubation experiments showed that growth dominated over attachment and detachment after a few hours in controlling the bacterial population density on agar particles. In the absence of grazing mortality, this growth led to an equilibrium population density consistent with the theoretical limit due to oxygen diffusion. Interspecific interaction experiments showed that the presence of some bacterial strains ("residents") on the agar particles either increased or decreased the colonization rate of other strains ("newcomers"). Comparison between an antibiotic-producing strain and its antibiotic-free mutant showed no inhibitory effect on the newcomers due to antibiotic production. On the contrary, hydrolytic activity of the antibiotic-producing strain appeared to benefit the newcomers and enhance their colonization rate. These results show that growth- and species-specific interactions have to be taken into account to adequately describe bacterial colonization of marine particles. Changes in colonization pattern due to such small-scale processes may have profound effects on the transformation and fluxes of particulate matter in the ocean.

We studied the dynamics of microbial communities attached to model aggregates (4-mm-diameter agar spheres) and the component processes of colonization, detachment, growth, and grazing mortality. Agar spheres incubated in raw seawater were rapidly colonized by bacteria, followed by flagellates and ciliates. Colonization can be described as a diffusion process, and encounter volume rates were estimated at about 0.01 and 0.1 cm(3) h(-1) for bacteria and flagellates, respectively. After initial colonization, the abundances of flagellates and ciliates remained approximately constant at 10(3) to 10(4) and approximately 10(2) cells sphere(-1), respectively, whereas bacterial populations increased at a declining rate to >10(7) cells sphere(-1). Attached microorganisms initially detached at high specific rates of approximately 10(-2) min(-1), but the bacteria gradually became irreversibly attached to the spheres. Bacterial growth (0 to 2 day(-1)) was density dependent and declined hyperbolically when cell density exceeded a threshold. Bacterivorous flagellates grazed on the sphere surface at an average saturated rate of 15 bacteria flagellate(-1) h(-1). At low bacterial densities, the flagellate surface clearance rate was approximately 5 x 10(-7) cm(2) min(-1), but it declined hyperbolically with increasing bacterial density. Using the experimentally estimated process rates and integrating the component processes in a simple model reproduces the main features of the observed microbial population dynamics. Differences between observed and predicted population dynamics suggest, however, that other factors, e.g., antagonistic interactions between bacteria, are of importance in shaping marine snow microbial communities.

Quantifying the rate at which bacteria colonize aggregates is a key to understanding microbial turnover of aggregates. We used encounter models based on random walk and advection-diffusion considerations to predict colonization rates from the bacteria's motility patterns (swimming speed, tumbling frequency, and turn angles) and the hydrodynamic environment (stationary versus sinking aggregates). We then experimentally tested the models with 10 strains of bacteria isolated from marine particles: two strains were nonmotile; the rest were swimming at 20 to 60 microm s(-1) with different tumbling frequency (0 to 2 s(-1)). The rates at which these bacteria colonized artificial aggregates (stationary and sinking) largely agreed with model predictions. We report several findings. (i) Motile bacteria rapidly colonize aggregates, whereas nonmotile bacteria do not. (ii) Flow enhances colonization rates. (iii) Tumbling strains colonize aggregates enriched with organic substrates faster than unenriched aggregates, while a nontumbling strain did not. (iv) Once on the aggregates, the bacteria may detach and typical residence time is about 3 h. Thus, there is a rapid exchange between attached and free bacteria. (v) With the motility patterns observed, freely swimming bacteria will encounter an aggregate in <1 day at typical upper-ocean aggregate concentrations. This is faster than even starving bacteria burn up their reserves, and bacteria may therefore rely solely on aggregates for food. (vi) The net result of colonization and detachment leads to a predicted equilibrium abundance of attached bacteria as a function of aggregate size, which is markedly different from field observations. This discrepancy suggests that inter- and intraspecific interactions among bacteria and between bacteria and their predators may be more important than colonization in governing the population dynamics of bacteria on natural aggregates.

We report here, for the first time, that bacteria associated with marine snow produce communication signals involved in quorum sensing in gram-negative bacteria. Four of 43 marine microorganisms isolated from marine snow were found to produce acylated homoserine lactones (AHLs) in well diffusion and thin-layer chromatographic assays based on the Agrobacterium tumefaciens reporter system. Three of the AHL-producing strains were identified by 16S ribosomal DNA gene sequence analysis as Roseobacter spp., and this is the first report of AHL production by these alpha-PROTEOBACTERIA: It is likely that AHLs in Roseobacter species and other marine snow bacteria govern phenotypic traits (biofilm formation, exoenzyme production, and antibiotic production) which are required mainly when the population reaches high densities, e.g., in the marine snow community.