Thomas Kiørboe

Turbulence, phytoplankton cell size, and the structure of pelagic food webs

Publisher Summary This chapter explores that the pelagic food chain is mainly linear and short, and there is a relatively close coupling between the primary production and the production of (pelagic) fish in the oceans. It has been realized that pico- and nano-sized phytoplankton (e.g. cyanobacteria) and heterotrophic micro-organisms (heterotrophic bacteria, heterotrophic nanoflagellates and ciliates) play a much larger quantitative role in production and mineralization, respectively, of the phytoplankton than formerly believed. Moreover, as microbial food webs are typically long and primarily based upon regenerated phytoplankton production, microbial production contributes insignificantly to fish production in the oceans. This chapter illustrates the significance of net-phytoplankton blooms to the fisheries production in the ocean, first of all blooms associated with larger-scale physical processes, such as the major upwelling regions and the vernal temperature stratification in temperate waters.

How zooplankton feed: mechanisms, traits and trade-offs.

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 106 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).

Population regulation and role of mesozooplankton in shaping marine pelagic food webs

Copepods constitute the majority of the mesozooplankton in the oceans.By eating and being eaten copepods have implications for the flow of matterand energy in the pelagic environment. I first consider populationregulation mechanisms in copepods by briefly reviewing estimates of growthand mortality rates and evidence of predation and resource limitation. Theeffects of variations in fecundity and mortality rates for the demography ofcopepod populations are then examined by a simple model, which demonstratesthat population growth rates are much more sensitive to variations inmortality than to variations in fecundity. This is consistent with theobserved tremendous variation in copepod fecundity rates, relatively low andconstant mortality rates and with morphological and behavioralcharacteristics of pelagic copepods (e.g., predator perception and escapecapability, vertical migration), which can all be considered adaptations topredator avoidance. The prey populations of copepods, mainly protozoa(ciliates) and phytoplankton, may be influenced by copepod predation tovarying degrees. The highly variable morphology and the population dynamics(e.g., bloom formation) of the most important phytoplankton prey populations(diatoms, dinoflagellates) suggest that predation plays a secondary role incontrolling their dynamics; availability of light and nutrients as well ascoagulation and sedimentation appear generally to be more important. Thelimited morphological variation of planktonic ciliates, the well developedpredator perception and escape capability of some species, and the oftenresource-unlimited in situ growth rates of ciliates, on the other hand,suggest that copepod predation is important for the dynamics of theirpopulations. I finally examine the implications of mesozooplankton activityfor plankton food webs, particularly their role in retarding vertical fluxesand, thus, the loss of material from the euphotic zone.

Plankton motility patterns and encounter rates.

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.

Sex, sex-ratios, and the dynamics of pelagic copepod populations.

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. Firstly, 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. Secondly, 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.

Optimal swimming strategies in mate-searching pelagic copepods.

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.

Propagation of planktonic copepods: production and mortality of eggs

Data on fecundity and egg mortality of neritic copepods were collected in various seasons, areas and under various hydrographical conditions. On a seasonal basis variations in fecundity (F) were related to temperature rather than to the abundance of phytoplankton (P). However, a strong correlation between F and P was evident when water column stability varied horisontally or temporally (i.e. at a tidal front or subsequent to a storm). Estimated specific egg-mortalities were variable and occasionally very severe, up to 9.1 d−1, implying that down to 10−4% of the eggs survive to hatching. The implications for phenology and distribution of copepods are discussed.

Unsteady motion: escape jumps in planktonic copepods, their kinematics and energetics.

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.

Shifts in Mass Scaling of Respiration, Feeding, and Growth Rates across Life-Form Transitions in Marine Pelagic Organisms

The metabolic rate of organisms may be viewed as a basic property from which other vital rates and many ecological patterns emerge and that follows a universal allometric mass scaling law, or it may be considered a property of the organism that emerges as a result of the adaptation to the environment, with consequently fewer universal mass scaling properties. Here, we examine the mass scaling of respiration and maximum feeding (clearance and ingestion rates) and growth rates of heterotrophic pelagic organisms over an ∼1015 range in body mass. We show that clearance and respiration rates have life-form-dependent allometries that have similar scaling but different intercepts, such that the mass-specific rates converge on a rather narrow size-independent range. In contrast, ingestion and growth rates follow a near-universal taxa-independent ∼3/4 mass scaling power law. We argue that the declining mass-specific clearance rates with size within taxa is related to the inherent decrease in feeding efficiency of any particular feeding mode. The transitions between feeding mode and simultaneous transitions in clearance and respiration rates may then represent adaptations to the food environment and be the result of the optimization of trade-offs that allow sufficient feeding and growth rates to balance mortality.

Flow disturbances generated by feeding and swimming zooplankton

Significance Plankton compromise their survival when they swim and feed because the fluid disturbances that they generate may be perceived by predators. Because the abundance and population dynamics of zooplankton in the ocean are governed by their access to food and exposure to predators, an important question is to what extent and how zooplankton may minimize the fluid disturbances that they generate. We show that when swimming and feeding are integrated processes, zooplankton generate fluid disturbances that extend much farther in the water than is the case for zooplankton that swim only to relocate. Quiet swimming is achieved through “breast swimming” or by swimming by jumping, whereas other propulsion modes are much noisier. This pattern applies independent of organism size and species. 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.