SCI. MAR., 61 (Supl. 1): 177-195 SCIENTIA MARINA 1997 LECTURES ON PLANKTON AND TURBULENCE, C. MARRASÉ, E. SAIZ and J.M. REDONDO (eds.) Copepods under turbulence: grazing, behavior and metabolic rates* MIGUEL ALCARAZ Institut de Ciències del Mar, CSIC, P. Joan de Borbó S/N, 08039 Barcelona, Spain SUMMARY: This review focuses on the effects of small-scale turbulence on the rate processes of copepods, an important group of planktonic animals, and on their consequences for the dynamics of pelagic ecosystems. Turbulent water motion enhances the encounter rates between planktonic organisms and their food, changing the perception of the food environment for copepods and other planktonic animals. As a consequence, their feeding behaviour is affected, and the grazing rates significantly increased. Direct effects of small-scale turbulence for planktonic copepods also include the enhancement of metabolic energy expenditure, excretion rates, growth, and development rates. Through complex cumulative processes of the changes on individual rate-processes, the structural and functional properties of planktonic ecosystems are modified, with important consequences for the ultimate fate of biogenic carbon in aquatic systems. Key words: Turbulence, copepods, rate processes, plankton ecosystems. INTRODUCTION Water bodies of any size are basically turbulent environments. In them, mechanical energy, driven mainly by solar heat and wind (and in large water bodies earth rotation), induces water movements that resolve into swirls of decreasing size. The turbulent kinetic energy associated with the turbulent eddies cascades from the larger eddies to the smaller, until dissipating into molecular viscosity (Ozmidov 1965). Aquatic environments support a community of organisms, the plankton, very diverse from the taxonomic and life-style points of view. Nevertheless, they all share the common characteristic of living suspended in a three-dimensional space, at the *Received July 11, 1996. Accepted September 12, 1996. mercy of water displacements, and without any relation to solid surfaces. Planktonic organisms cover a broad size spectrum (Fig. 1), from the sub-micrometer range to hundreds of centimeters, and occupy different trophic positions, from primary producers to first- and second order carnivores, detritivores and microheterotrophs. The almost unique source of matter and energy for the successive trophic levels in planktonic systems is provided by microscopic autotrophs. They consist of protists and unicellular algae (phytoplankton) which inhabit the upper water layers, where light conditions allow photosynthetic activity. The concentration of primary producers is in general very low (i.e., from 0.1 to 10 ppm by volume), and their size-range covers about 3 orders of magnitude (see Fig. 1). Amongst the consumers, heterotrophic unicellular organisms and metazoans (zooplankton) are repCOPEPODS UNDER TURBULENCE 177 FIG. 1. – The categories in which plankton is divided according to size classes, and the corresponding functional groups, from viruses to large planktonic metazoan. The different functional groups overlap into different plankton-size categories, which are somewhat artificial and in part derived from the mesh-sizes used to sample them (redrawn from Sieburt et al., 1978). resented by a taxonomically diverse community. Their success depends on the probabilities of finding food and mates and of escaping predation; these probabilities are highly conditioned by the characteristics of the physical environment. The effects of turbulent water motion on the organisms which are free-living in the water column differ according to the relationships between individual size and the scale length of turbulent eddies. Mesoscale eddies represent mainly advection for small (<10-2 m) organisms (Haury et al. 1978). However, small-scale turbulence eddies, which are in the size range of planktonic organisms and their food, induce changes in the structural and functional properties of primary producers and consumers. It seems that the complex nature of pelagic food webs, and even the ultimate fate of biogenic carbon, would be partially controlled by environmental turbulence conditions (Kiørboe, 1993). Taxonomically, the zooplankton is also very complex. The majority of phyla are represented, from protozoa to small fishes, although crustaceans are most abundant. Amongst them, copepods are the dominant group and play a fundamental role in herbivorous food webs. The characteristics of planktonic primary producers (small size, generally low energetic value, and extreme dilution) impose severe conditions for its efficient exploitation by herbivorous copepods (Conover, 1968). In principle, the simplest solution to exploit the small, dispersed food particles would consist of filtering large amounts of water through adequate structures. Regarding crustacean zooplankton, and in particular copepods, the morphology and quick motion of their feeding appendages (Fig. 2 and 3) suggested an automatic, mechanical filter-feeding system. With the rows of bristles in the setae of their LIFE IN THE PLANKTONIC DOMAIN Problems of living in a nutritionally dilute environment Phytoplankton is assumed to be exploited mainly by the zooplankton, which constitute the first level of consumers and is one of the most important contributors to energy transfer in aquatic food webs. From a trophic point of view, however, zooplankton is far from uniform and includes, besides herbivores, omnivores, detritivores (feeding on phyto and zooplankton remains) and carnivores of first- and second-order. 178 M. ALCARAZ FIG. 2. – A marine planktonic copepod, Centropages violaceus, with the maxilipedes extended. The rows of bristles in the setae are visible. (Photograph by A. Calbet). FIG. 3. – Scanning electron micrographs of planktonic marine copepods showing the appendages related with the feeding processes; a: Maxillipedes of a microphage, herbivorous Copepod, Temora stylifera; b: Maxilipedes of a herbivorous (omnivorous) copepod, Acartia grani; c: Maxilipedes of an omnivorous copepod (Oithona sp); d: Maxilipedes of a carnivorous copepod (Candacia sp.). There is a transition in the setal strength and bristle density and intersetule distance from microphagous herbivores (with thin setae provided with dense rows of bristles), to carnivores, which have setae transformed into robust spines and almost no bristles. mouthparts, copepods would sieve food particles. The lower size of the particles would be determined by the distance between the bristles (Nival and Nival, 1976; Boyd, 1976). However, given the small size of the moving appendages, and despite their relatively high velocity, the water flow regime results in low Reynolds numbers (Lam and Frost, 1976; Koehl and Strickler, 1981). Reynolds number (Re) represents the dimensionless ratio between inertial and viscosity forces. For low Re values (i.e., viscosity dominating over inertia forces, large boundary layer, and laminar, reversible flow) water filtration requires high amounts of energy, which cannot be compensated for by the energy obtained from the food particles (Alcaraz et al., 1980; Hansen and Tiselius, 1992). Despite the problems of living in a viscous world, where food is highly diluted and has a relatively low nutritive value, copepods have developed fairly sophisticated sensory systems and rather complex behavioural patterns (Strickler, 1984) which have determined for their success in aquatic systems. How do copepods find food and mates, and escape predation? The first, direct observations of tethered copepods feeding on a suspension of phytoplankton, were made possible by using high-speed filming techniques (Alcaraz et al., 1980). The method allowed the observation and quantification of the exact movements performed by each feeding appendage, as well as the path followed by the food particles until captured and ingested or rejected. Further laboratory experiments using the same or similar methodology (Paffenhöfer et al., COPEPODS UNDER TURBULENCE 179 1982; Strickler, 1982; Cowles and Strickler, 1983) confirmed that copepods are not mere mechanical filtering machines. They create feeding currents by moving their different feeding appendages in a synchronous, although out of phase, “fling and clap” motion. The temporal sequence of movements ensures the creation and maintenance of a laminar flow field of constant structure, almost parallel to the body axis. This current is necessary to direct food particles towards the organism, and to detect them via chemo- or mechanoreception (Strickler, 1982; Buskey, 1984). In the laminar feeding current created by a freeswimming calanoid copepod, Strickler (1985) identified different areas or “cores” according to the characteristics of water flow and the function of the interacting appendages (Fig 4). The motion core is the central kernel or volume and is defined by the cross-section surface of the capture area. The viscous core envelops the motion core and originates in a surface larger than its cross-section. In this viscous core, water velocity increases in the proximity of the organisms so that all the water goes through the capture area. Finally, the sensory core includes the volume of water scanned by the sensory structures in the antennae of the copepods. The volume of water actually searched by the organism is thus larger than the one defined by the product of the cross-section of the sensory area of the copepod times the water velocity relative to FIG. 4. – Zones or “cores” in the feeding currents created by a calanoid copepod. 1: Motion core. 2: Viscous core. 3: Sensitive core. 4: Sensory field of the first antenna. 5: Capture area. (Redrawn from Strickler, 1985). 180 M. ALCARAZ the organism. The size and stability of the flow fields generated by feeding copepods is speciesspecific (Strickler, 1985). In the laminar flow field, where viscosity dominates over inertia (low Reynolds numbers), the information necessary to perceive food particles in advance (mostly chemical cues forming an active sphere around food items) is adequately directed towards the receptory system of copepods. The precise location of the incoming information allows the organism to change the flow field in order to capture the food particles (Strickler, 1985; Paffenhöfer et al., 1982). Copepod feeding must be thus considered as the consequence of a chain of successive steps, starting with the encounter of a food item, followed by its recognition, capture, and eventual ingestion or rejection. It is still unknown the extent to which irregular water movements induced by small-scale turbulence modify the flow field of the feeding currents generated by copepods. In any case, hydrodynamic perturbations could represent changes in the efficiency of food perception, capture and ingestion. After feeding, finding mates and escaping predation are essential for the maintenance of copepods and for zooplankton in general. The interactions between copepods, either of the same or different species, are also very dependent on the physical properties of aquatic systems (Strickler, 1975 a, 1977). For a copepod, the encounter with another individual can have either a beneficial effect, when it finds a mate or a prey, or be disastrous, if the encounter is with a predator. For this reason, the existence of mechanisms to detect and identify the likely type of an encounter is essential (Strickler, 1977; Yen, 1988; Yen and Fields, 1992). Copepods use chemical cues (pheromones for sexual attraction, other chemicals for prey or predator detection) and mechanical cues (sex or species-specific hydrodynamical tracks) to identify the nature of approaching encounters. Although chemical or physical information should be persistent enough to trigger adequate behavioural responses (escape or attraction), their durability must be limited, otherwise they will accumulate as noise, thus limiting detection efficiency. Turbulent water dynamics, with its associated high diffusion rates, must significantly contribute to the disappearance of hydrodynamic and chemical cues, so changing the perception scenario of zooplankters. TURBULENCE, ENCOUNTER RATES AND COPEPOD FEEDING Turbulence and encounter rates An encounter is the first, limiting step for feeding and mating. In a theoretical model describing seasonal variation in oceanic production, Cushing (1959) based the grazing rates of copepods on this assumption. The rate at which a predator (copepod) contacts food (phytoplankton, its presumably non-motile prey) was considered to be a function of the copepod velocity, the “contact surface” (corresponding to the cross-section of the organism including the sensing appendages), and the concentration of phytoplankton. The contact surface can be generalized to the encounter surface defined by the predator’s reactive distance, Cr = π R2 N v π R2 N (u2 + 3 v2 ) 3v for v > u, and Cr = π R2 N ( v2 + 3 u2 ) 3u v = (v2 + w2)0.5, u = (u2 + w2)0.5 where w is root-mean square turbulent velocity. The contact rate between predators and prey when taking turbulence into account is then Cr = in which Cr is the encounter rate, R is the radius of the perception area of the predator, N is the food concentration, and v is the predator’s velocity. This model of predator-prey contact rate, which is valid for non-motile prey, was generalized by Gerritsen and Strickler (1977) considering that both predator and prey are motile. In their model, the density component (π R2 N) is the same, but in the velocity component (v), the velocities of predator and prey are also taken into account. Cr = Taking into account the isotropic nature of smallscale turbulence in the ocean (Gargett et al., 1984; Gargett, 1997), and the values of the root-mean square turbulent velocity, (which are uncorrelated with the swimming speed of planktonic organisms and of the same order), Rothschild and Osborn (1988) generalized the model of Gerritsen and Strickler (1977) by including the effects of smallscale turbulence. The new velocity components of predator and prey must thus be computed as: for u > v, where v and u are the respective velocities of predator and prey. The main consequences of the model arise from the fact that contact rates are mainly dependent on the higher of the two speeds. According to the model, and taking into account predation efficiency (that is, the higher catches in relation to the predator’s swimming energy expenditure), two predation “strategies” arise: slow-swimming (or even stationary), ambush predators, which will exploit fast-swimming prey; and cruising predators, preying on slow-swimming prey. The model also allows the prediction of the trophic community structure according to swimming speed and trophic position (Gerritsen and Strickler, 1977). π R2 N (u2 + 3 v2 + 4 w2 ) 3( v2 + w2 ) 0.5 for v > u, which reverts to the equation of Gerritsen and Strickler (1977) when root-mean square turbulent velocity w = 0. The first conclusion of the model is that the kinetic nature of the environment affects the contact rate between planktonic organisms. Under turbulence the contact rates are higher than predicted when only densities and relative swimming velocities of predator and prey are considered. As a consequence, in laboratory experiments where turbulence has not been taken into account, the functional responses that are dependent on contact rates (i.e., feeding rates) may have been underestimated. The extrapolation to natural systems of laboratory data on copepod feeding rates obtained under calm (nonturbulent) experimental conditions could be biased (Rothschild and Osborn, 1988; Kiørboe, 1993). Another important issue is the possibility of linking the physical-biological interaction for different temporal and spatial scales of variability. Further improvements of the model include the substitution of average, constant speeds of predator and prey by more realistic Gaussian 3-D variable velocity distributions (Evans, 1989) or different motility patterns and behaviours of predator and prey (Kiørboe and Saiz, 1995; Saiz and Kiørboe, 1995). Small-scale turbulence and copepod feeding The main issue of the models describing the effects of turbulent water motion on plankton contact COPEPODS UNDER TURBULENCE 181 FIG. 5. – Time series of the frequency of encounter rates with food particles, fast swimming (escape) events, and percent time allocated to slow swimming (feeding) of a tethered calanoid copepod (Centropages hamatus) under turbulent and calm conditions and low (70 cells/ml) and high (350 cells/ml) food concentrations (the dinoflagellate Gymnodinium sp.). C: Calm. T: Turbulence. (Redrawn from Costello et al., 1990). rates, is an increase in the “perceived” food abundance from the predator’s point of view, which could, as a consequence, induce higher feeding rates. Calanoid copepods create laminar flow fields (feeding currents) which entrain food particles as well as the cues to perceive them in advance. It is still unknown whether the irregular water movements induced by small-scale turbulence modify the flow field of the feeding currents generated by copepods, or can negatively interfere with their perception systems. Theoretical models, however, suggest that small-scale turbulence has positive effects when predators (copepods) feed on a “swept clear” mode as considered in the Rothschild and Osborn (1988) model which depends on direct contact rates. According the Osborn (1996) model, the feeding currents 182 M. ALCARAZ created by a copepod would be at scales appropriate to act in concert with the turbulent motion and diffusion of prey. Feeding currents represent a significant expansion of the capture radius of copepods, which will take advantage of the increase in the flux of food directed by turbulent diffusion (Osborn, 1996). The effects of turbulence on encounter rates between copepods and their food, as predicted by theoretical models, have been confirmed by laboratory experiments. The rate at which food particles reached the capture area of calanoid copepods was quantitatively estimated through visual observation (Marrasé et al., 1990; Costello et al., 1990; Saiz, 1991). In tethered individuals submitted to alternating calm and experimentally induced turbulence conditions (dissipation rates ranging from ε=0.05 and ε=0.15 cm2 s-3), the encounter rates were dependent on food concentration and local turbulence conditions (Fig. 5). However, higher encounter rates do not necessarily translate into higher feeding rates. Small-scale turbulence tends to reduce the “feeding efficacy index” (Marrasé et al., 1990). This was estimated as the ratio between the encounter rates of food particles with the copepod’s capture area during slow swimming (assimilated to feeding activity), versus the encounter rates in a “control” area far from the feeding activity of the copepod (Fig. 6). The “effective encounter rate”, equivalent to the frequency of encounters while the copepod was slow-swimming (feeding), was significantly higher under turbulence but only for low food concentrations (Fig. 6). On the other hand, the balance between energetic gains (as deduced from the feeding efficacy index), and losses (i.e., swimming energy expenditure) are modified by turbulence, but are also dependent on food concentration (Marrasé et al., 1990). While for low (undersaturating) food concentrations turbu- TABLE 1. – The energetic costs of different behavioural activities in a planktonic copepod, Centropages hamatus, in relative units, and ratios of the energy spent for the same behaviour under high and low food concentration . “Low” and “high” values correspond to the minimum and maximum energetic costs for the different activities. LFT: Low food concentration, turbulence. LF: Low food concentration, calm. HFT: High food concentration, turbulence. HF: High food concentration, calm. (From Marrasé et al., 1990). Energetic costs in relative units Low value High value Slow swimming and resting stage 1 1.25 Fast swimming 40 400 Ratio of energetic costs LFT/LF HFT/HF HF/LFT 1.04 1.82 1.04 1.42 6.78 1.27 lence increases the potential energy gains of copepods, at high (saturating) food conditions, the enhancement of energetic costs is much higher than the gains derived from the higher encounter rates (Table 1). The above results, however, were FIG. 6. – The effects of turbulence on A: The encounter rates between copepods and their food. B: Feeding (foraging) efficacy index. C: Effective encounter rates (see text). Experimental food concentrations as for Fig. 5. (Redrawn from Marrasé et al., 1990). COPEPODS UNDER TURBULENCE 183 obtained in tethered animals, which perceive a different velocity spectrum than in the case of freeswimming organisms. These cases provide indirect evidence of higher feeding rates under turbulence deduced from the observed higher contact rates with food particles on tethered copepods (Costello et al., 1990; Marrasé et al., 1990). Experimental confirmation of the effects of small-scale turbulence on grazing rates for freeswimming copepods were experimentally confirmed by Saiz et al. (1992 b). The functional response of grazing and clearance rates to different turbulent conditions (low turbulence, ε=0.06 cm2 s-3, high turbulence ε=0.12 cm2 s-3) were highly dependent on food concentration. The higher feeding and clearance rates of copepods at food concentrations below saturation (Table 2), confirm the hypothesis of Rothschild and Osborn (1988), regarding the increase in food concentration as perceived by organisms under turbulence. It is also in agreement with the observed dependence of the “feeding efficiency index” on food concentration (Marrasé et al., 1990). The degree at which feeding rates are enhanced by turbulence is species-specific (Table II), even for closely-related species of the same genus (Saiz et al., 1992), and probably also depends on the average turbulence conditions experienced by the copepods in their natural habitat. Those direct effects of turbulence, mainly attributable to changes in the food environment as perceived by copepods, are indirectly modulated by the TABLE 2. – Average clearance and ingestion rates under turbulent and calm conditions in relation to food concentration for two Acartia species. FC: Food concentration range, in ppm. by volume. F: Clearance rates, volume of water swept clear, in ml/ind/day. I: Food ingestion rates in algal volume, µm3/ind./day. 106. (From Saiz, 1991). modifications induced on phytoplankton by turbulent water motion. Phytoplankton cell size and chemical composition are affected by small-scale turbulence through changes in nutrient uptake kinetics and light environment (Kiørboe, 1993). Similarly, turbulence and other co-variant factors such as nutrients and light, are selective forces that can determine the dominance, in natural ecosystems, of the different phytoplankton life forms (non-motile forms like diatoms in turbulent, high-nutrient environments, and motile forms like dinoflagellates in low turbulent, poor nutrient conditions: Margalef, 1978). In conclusion, turbulent water movements induce changes in the velocity components affecting copepods and their food and increasing their rate of encounter. As a consequence of the higher concentrated food environment as perceived by copepods, feeding rates increase accordingly. However, given the functional relationships between food abundance and grazing, small-scale turbulence has an enhancing effect on feeding rates mainly for undersaturating food concentrations. The possible interaction between turbulent water motion and laminar flow field generated by feeding currents remain unknown, although theoretical models predict a more efficient use of turbulent water motion by copepods creating feeding currents. To those general, direct issues of small-scale turbulence on copepod feeding, indirect effects derived from turbulence-induced changes in food quality should be added. In any case, the consequences of turbulence from a trophodynamic point of view can be very complex, and dependent not only on food concentration, but also on the size and motility of food and the copepod, its feeding behaviour, and turbulence intensity. Acartia tonsa Calm FC 0.18-0.23 0.24-0.29 0.4-0.5 0.57-0.87 1.08-1.23 Turbulence F I F I 139.4 156.9 62.0 59.0 50.5 28.1 41.9 29.6 44.4 57.1 165.4 181.4 79.3 134.73 41.5 32.2 46.6 32.9 92.1 45.3 Acartia grani Calm FC 0.15-0.18 0.20-0.29 0.24-0.38 1.14-1.37 1.69-1.90 Turbulence F I F I 50.5 69.6 41.4 19.9 24.0 8.5 18.9 13.4 25.8 44.1 128.7 131.4 49.0 45.8 30.2 14.5 27.8 12.7 53.3 52.1 184 M. ALCARAZ TURBULENCE, COPEPOD BEHAVIOUR AND METABOLISM Swimming in copepods: behavioural pattern and energetic costs The most important fraction of the energetic budget of copepods corresponds to active metabolism. This includes the basal or maintenance metabolism, plus a variable amount of energy derived from the costs of swimming (Prosser, 1973). By definition, copepod swimming capacity appears as almost negligible if compared with large scale advective water movements. However, copepods, and in general planktonic animals, exhibit an almost constant activity in searching for food and mates, or escaping predation. The vertical migrations performed by the majority of zooplankters involve displacements of hundreds of meters and, when scaled to the relative size of organisms, the daily traveled distances are considerable (tens of thousands of body lengths per hour). Locomotion includes a diversity of swimming movements and propulsion mechanisms in planktonic copepods, with different consequences from the point of view of the energy consumed (Strickler, 1977). Normal cruising is characterized by almost constant or oscillating swimming speeds. In this swimming mode, displacement usually takes place in smooth gliding (slow swimming). This generally results from the creation of feeding currents, as in the majority of calanoid copepods. Oscillating swimming speeds are typical of cyclopoid copepods, which swim in a hop-and-sink pattern, a consequence of a series of powerful strokes of the swimming legs (Strickler, 1977). Apart from this undisturbed swimming model, some stimuli can trigger escape reactions (Singarajah, 1975), involving velocities about 500 body lengths per second, and accelerations as high as 1200 cm s-2 (Strickler, 1975 a). Escape reactions are generally the consequence of avoidance responses to an undesirable encounter. They occur after the detection of the flow disturbance created by another swimming zooplankter, a possible predator. The detection of changes in flow velocity is made possible by the existence of a sensory system able to measure very small disturbances of flow velocity (Strickler, 1975 a). In copepods, the sensory system is represented by chemoreceptors (aesthetascs) and mechanoreceptive sensilla (Bundy and Paffenhöfer, 1993) displayed in arrays mainly in the first antennae. Mechanoreceptors consist of modified ciliary structures able to detect the changes in inertial forces (Barrientos, 1980). Their arrangement, size and orientation (Fig. 7) are probably determined by the flow characteristics and intensity of the stimulus to detect (Haury and Kenyon, 1980; Yen and Nicoll, 1990). The neural activity recorded when antennal receptors are mechanically stimulated evidences a very high sensitivity. Neural responses have been obtained for frequencies ranging from 40 to 1000 Hz, and setal displacements as small as 10 nm (Yen et al., 1992). The main behavioural consequences of the stimulation of antennal mechanoreceptors are changes in the swimming pattern, with FIG. 7. – Scanning electron micrograph of the first antenna of a male calanoid copepod, Acartia clausi, showing the distribution of mechano- and chemoreceptors. an increase in the frequency of escape responses (Gill and Crisp, 1985). The evaluation of the proportion of the active metabolism that corresponds to swimming costs in copepods entrains serious difficulties. The available data are scarce and contradictory, and differ by orders of magnitude, depending on the methodological approach. The higher values correspond to indirect estimates based on the decrease on lipid contents of organisms after long, sustained vertical migrations (95% of total metabolism: Petipa, 1966). Other high values were obtained from the comparison of oxygen consumption rates on free-swimming and inactive (narcotized) copepods (30-40% of total metabolism: Klyastorin and Yarzombek, 1973; Paulova and Minkina, 1983). Values deduced from the evaluation of parameters of Newton’s quadratic resistance law, using data on velocity and acceleration obtained through high-speed filming, give much lower values (around 0.1% of total metabolism: Vlymen, 1970; Strickler, 1975 b). These low energetic costs coincide with direct measurements COPEPODS UNDER TURBULENCE 185 of the work done (deformation of a calibrated spring) by a restrained copepod in each swimming leap (Alcaraz and Strickler, 1988). Part of the disagreement between the estimations of the energetic costs of swimming arises from methodological problems and considerations about the efficiency of the work done by swimming organisms (Alcaraz and Strickler, 1988). However, part of the variability is probably due to differences in the swimming behavioural pattern displayed by the organisms. The various behavioural components of swimming activity (i.e., resting, non-disturbed swimming, and escape reactions) require different energetic costs, so their relative frequency and duration can significantly modify metabolic expenditure. While for non-disturbed swimming the energetic consumption corresponds to the lower values here reported, a single escape reaction requires about 400 times more energy per unit time than normal cruising speed (Strickler, 1977). The most conspicuous direct effects of smallscale turbulence on copepod activity refer to changes in the pattern of swimming behaviour (Costello et al., 1990; Marrasé et al., 1990). Visual observations of tethered copepods indicate an increase in the proportion of time allocated to the “slow swimming”. This behaviour, which is assimilated to feeding, or at least to the creation of feeding currents, appears to be triggered by the higher rate of encounter of the copepod with food particles, and is more conspicuous for low food concentration (see Fig. 6). Simultaneously, the frequency of fast-swimming events (or escape reactions) also increases. Visual observations of video-recorded free-swimming calanoid copepods (Acartia clausi) confirmed the general character of behavioural changes, and allowed quantitative estimates of the effects of turbulence on swimming patterns. Turbulence levels similar to those observed in highly dynamic shelf and coastal ecosystems (low turbulence, ε= 1 mm2 s3, high turbulence, ε= 5 mm2 s-3) significantly increased the proportion of time allocated to slow swimming, even in the absence of food, when compared to calm conditions (about 2.5 times higher: Saiz and Alcaraz, 1992 a). Simultaneously, the frequency of escape reactions was about three times that observed under calm conditions, as was the velocity displayed, while the time allocated to rest proportionally decreased. The energy consumed under turbulence as compared with calm conditions due to the change in the frequency of the different swimming patterns represented a 83-115% increase. 186 M. ALCARAZ Effects of turbulence on zooplankton metabolism The turbulence-induced changes in the swimming behavioural pattern of planktonic copepods result in an enhancement of the frequency and intensity of high-energy consuming activities (Marrasé et al., 1990; Costello et al., 1990; Saiz and Alcaraz, 1992 a; Hwang et al., 1993), which must translate into higher respiration and excretion rates. The effects of small-scale turbulence on respiration rates of crustacean zooplankton have been experimentally confirmed through the study of the changes on heart-beat rates (Alcaraz et al., 1994a). The rate of heart-beating is an efficient descriptor of the respiration rates of crustaceans (Ingle et al., 1937; Pavlova and Minkina, 1983), and its almost immediate response is very adequate for the study of short-time metabolic responses to microscale perturbations. Small-scale turbulence (ε ranging from 0.002 to 0.32 cm2 s-3) increases heart-beat (respiratory) rates in a variety of planktonic crustaceans with a differentiated heart, from cladocerans to decapod crustacean larvae (Table 3). Although the experiments were performed on tethered organisms, and thus the experienced flow field must be different from that of free-swimming individuals (Tiselius and Jonsson, 1990), tethered copepods seem to display the same activity pattern as free-swimming ones (Hwang et al., 1993). The intensity at which heart-beat rate is enhanced by turbulence appears to be species-specific, and seems to be related to differences in sensitivity to hydrodynamic disturbances, probably due TABLE 3. – Effects of turbulence on heart-beat rates for different planktonic crustaceans. The heart beating was video-recorded on tethered individuals, and corresponds to average values of two alternate 15 min. periods of calm and turbulence for each individual. Experimental temperature in º C. Average increase of heart-beat rates under turbulence in %. Probability values for the two-tailed Wilcoxon ranked sign test. N is the number of individuals tested. (Modified from Alcaraz et al., 1994a). Organism Temp ºC Decapod larvae Porcellana longicornis 19.3 Brachinotus sexdentatus 25.0 HBR increase (%) N Probability 9.2 9.4 2 5 <0.005 <0.005 Cladocerans Daphina pulex Penilia avirrostris 18.0 15.6 14.6 5.9 12 4 <0.001 <0.001 Copepoda Calanus gracilis 22.0 93.7 1 <0.001 those observed in respiration (heart-beat rates) estimated for other copepod species (Table 3). To these direct effects of turbulent water movement, the enhancement of the nutritious value and cell size of phytoplankton, and changes in their pattern of spatial distribution and patchiness field (Kiørboe, 1993), indirectly modify zooplankton activity pattern under turbulence, with consequent changes in energy expenditure. TURBULENCE, GROWTH EFFICIENCY AND DEMOGRAPHIC STRUCTURE OF COPEPODS Turbulence and gross-growth efficiency FIG. 8. – Percent increase in the rate of heart beating under turbulence relative to calm conditions, for a planktonic crustacean Daphnia pulex, in relation to temperature. The shaded area corresponds to the average increase. The effect of turbulence is temperaturedependent, being maximum at 18 ºC, corresponding to the temperature at which Daphnia cultures were maintained in the laboratory. (Modified from Alcaraz et al., 1994). to differences in the mechanoreception system. The effects of small-scale turbulence appear to be modulated by temperature, with the higher percent increase in heart-beat rates around the environmental “in situ” temperature experienced by the organisms (Fig. 8). Laboratory measurements of excretion rates in copepods also confirm the higher metabolic activity induced by turbulence (unquantified turbulence levels: Saiz and Alcaraz, 1992 b). Under turbulence, ammonia and phosphate excretion rates increased about 60% with respect to calm conditions, equivalent to a temperature rise of about 7º C assuming a Q10 of 2 (Table 4). The percent increases in excretion rates are lower, although of the same order, than TABLE 4. – Increase of NH4-N and PO4-P weight-specific excretion rates under turbulence as compared to calm conditions for several planktonic copepods (Acartia). Average percent increase and standard deviation (STD). N= number of replicates. (Modified from Saiz and Alcaraz, 1992b). Species Ammonia excretion (ng NH4-N.µg bodyN-1.day-1) Average % increase STD A. margalefi A. clausi A grani 55.6 26.0 65.8 34.7 23.6 N 33 3 29 Phosphorus excretion (ng PO4-P.µg bodyN-1.day-1) A. margalefi 63.8 16.3 7 The energy obtained through the ingestion of food by planktonic copepods must supply, apart from the requirements for active metabolism (basal metabolism plus swimming), the costs for growth and reproduction. In the balanced equation, a term that remains almost constant, or at least that cannot suffer a drastic reduction, is basal metabolism. As swimming activity must also be maintained above a minimum level, any reduction in energy intake will affect mainly the production term. There are no satisfactory methods to estimate the amount of energy invested in zooplankton production. For planktonic copepods, however, it is commonly accepted that the rate of egg production by females is directly related to the amount of food ingested (Kiørboe et al., 1985; Berggreen et al., 1988), and can be considered as a robust estimator of secondary production (Poulet et al., 1995). The gross-growth efficiency (production/ingestion) is a crucial parameter in plankton production models. For copepods, it can be adequately estimated through the ratio egg produced/food ingested, either in units of carbon or energy (Kiørboe et al., 1985). As discussed above, turbulence has a direct enhancement effect on grazing (food intake) rates, and on metabolic energy consumption. The balance between the energy gains derived from the enhancement of grazing rates, and the corresponding losses resulting from increased metabolic rates, will thus determine the amount of energy allocated to zooplankton production. In simultaneous estimates of ingestion rates and egg production by female copepods, Saiz et al. (1992) observed a decline in the number of eggs laid by females under turbulence as compared with calm conditions. The importance of the reduction in the COPEPODS UNDER TURBULENCE 187 TABLE 5. – Effect of turbulence on the gross-growth efficiency of planktonic copepods (Acartia) as estimated through the quotient “carbon egg produced/carbon food ingested”. C: Calm. T: Turbulence. Average values ± standard deviation. Data pooled for all the experimental food concentrations. Test: one way ANOVA, or when its assumptions are not accomplished, Mann-Whitney two tailed test, (*). (Modified from Saiz et al., 1992). Species A. tonsa A. grani A. clausi Experimental conditions Calm Turbulence 0.37 ± 0.029 0.36 ± 0.035 0.70 ± 0.052 Significance 0.33 ± 0.024 Non-significant 0.26 ± 0.018 Significant, p<0.007* 0.49 ± 0.037 Significant, p<0.002 gross-growth efficiency under turbulence (Table 5) differed even for closely-related (congeneric) species, probably in relation to the turbulence conditions of their habitat. These results are in accordance with the stronger influence of turbulence on metabolic rates as compared with grazing (energy intake), and reflect a global reduction in the energy allocated to egg production, once the metabolic demands have been satisfied. Other effects of small-scale turbulence on zooplankton: Development rates, individual size, and sex ratio under turbulence The cumulative effects of turbulence on the copepod rate processes discussed above (grazing, swimming behaviour, metabolic expenses, excretion, gross-growth efficiency) result into changes in the extensive properties of their populations. The positive or negative effects of small-scale turbulence on secondary production (or, at least on the fraction of energy allocable for production) are highly dependent of the balance between energetic gains and losses. Energetic gains can be either induced directly by turbulence (higher feeding rates: Saiz et al., 1992) or indirectly, through the higher nutritious value, higher size or changes in the field patchiness of algal food (Kiørboe, 1993); losses are mainly the consequence of direct increases in metabolic expenses due to changes in swimming behaviour (Marrasé et al., 1990; Saiz and Alcaraz, 1992 a). Thus, the turbulence characteristics of the environment are a significant factor in the modulation of the dynamics of copepod populations. Other effects of small-scale turbulence on the dynamics and structure of copepod communities concern the development times for the different instars of copepods, and the final body size of adults. Alcaraz et al. (1988) and Saiz and Alcaraz 188 M. ALCARAZ FIG. 9. – Development times of two cohorts of Acartia grani (copepod) under calm and turbulent conditions, relative to the maximum time needed to reach the adult stage. The development of the two cohorts was made under similar food conditions. Under turbulence, there is an acceleration of the rate of development, more important for the younger stages. (Redrawn from Saiz and Alcaraz, 1992). (1991) observed a significant reduction in the development time for the different instars of Acartia grani in laboratory-reared cohorts submitted to turbulence (ε around 0.05 cm2 s-3) as compared to calm conditions (Fig. 9). Development under turbulent and calm conditions started simultaneously, from eggs laid by females belonging to the same population and in cultures with saturating food concentrations. The effects of turbulence appear to be agedependent, as the maximum reduction in the duration of successive instars occurs for naupliae and early copepodites. The acceleration in the development of copepods under turbulence can be a phenomenon comparable with the ageing effect and reduction in the life span observed by Shaw and Bercaw (1962) for other crustaceans, and related to temperature-induced higher metabolic expenses. The same explanation can be valid for the reduction of individual size observed when the cohort develops under turbulence (Saiz and Alcaraz, 1991). Although the size differences between equivalent instars for cohorts grown under calm and turbulent conditions are only significant for adult stages, the effects were also observed from the stage copepodite II onwards (Table 6). TABLE 6. – Effects of turbulence on individual size (µm) and biomass (µg dry weight) of a planktonic copepod, Acartia grani, in laboratory microcosms at equivalent food conditions. Only data for Copepodite II and onwards have been represented. Mean values and standard deviations for calm and turbulent conditions. *: Significant at the 0.01 level. (Modified from Saiz and Alcaraz, 1991). Instar Size Biomass Calm CII CIII CIV CV-VI (male) CV-VIf (female) Male Female Turbul. Calm Turbul. 450.9 ± 23.2 555.3 ± 19.3 677.0 ± 32.4 787.2 ± 16.2 863.5 ± 32.1 441.4 ± 20.0 555.9 ± 23.7 672.5 ± 28.2 788.2 ± 21.6 855.3 ± 26.3 0.938 1.776 3.259 5.176 6.873 0.879 1.782 3.194 5.197 6.675 883.7 ± 25.8 1013.7 ± 32.5 873.6 ± 23.2* 1006.6 ± 37.2 7.378 11.235 7.123 10.997 Other effects of small-scale turbulence on copepod demographic structure concern the determination of adult sex ratios (Alcaraz et al., 1988). In the same laboratory populations of copepods used as in the study of development rates, a lower proportion of males was observed under turbulence as compared with calm conditions (Table 7). Simultaneously, female fecundity was highly depressed, not only due to the already discussed reduction on grossgrowth efficiency (Saiz et al., 1992), but also due to the reduction of the male proportion. As observed by Wilson and Parrish (1971), Alcaraz (1977) and Alcaraz and Wagensberg (1978), the fecundity of Acartia species is very sensitive to changes in the sexual ratio. Nevertheless, these negative effects of turbulence on copepod communities were observed at saturating food concentrations, in which ingestion rates cannot benefit from the higher encounter rates between copepods and their food, and the higher energetic losses due to turbulence clearly reduce the energy allocated to reproduction. The final consequence of the above mentioned effects of turbulence on copepod communities is the increase in the turnover rate of their populations due TABLE 7. – Effects of turbulence on the mean adult sex ratios (male/male+female) and instantaneous values of the quotient eggs/female of Acartia grani in laboratory microcosms under similar food conditions. Day: number of days after starting the experiment. C: Calm. T: Turbulence. In parentheses, standard error of the mean. (Modified from Alcaraz et al., 1988). Day 0 4 8 12 16 Mean Sex ratio (/+) Calm Turbul Eggs/female Calm Turbul 0.23 0.29 0.26 0.40 0.48 0.23 0.36 0.17 0.07 0.19 61.6 111.0 84.8 119.7 89.86 72.6 50.3 41.4 0.33 (0.04) 0.20 (0.04) 94.2 (11.4) 63.5 (10.9) to the shorter cohort development time. Simultaneously, there is a tendency toward a reduction in copepod biomass as a result of the decrease in individual size and the decline in female fecundity. TURBULENCE, COPEPOD-PHYTOPLANKTON INTERACTIONS AND THE TROPHIC STRUCTURE OF PLANKTONIC COMMUNITIES The structure and dynamics of planktonic systems are the consequence of a complex web of positive and negative feed-back mechanisms between the elements conforming the different trophic groups. Copepods, as the most important component of the first level of consumers, exert a double control of qualitative and quantitative properties of phytoplankton. Apart from reducing phytoplankton biomass by grazing pressure, through selective feeding copepods can modify the size-spectrum and even the structure of phytoplankton communities. In turn, the nitrogen (mainly ammonia) and phosphorus (as soluble reactive phosphate) excreted by zooplankton can represent a significant contribution to the phytoplankton requirements of nutrients, thus allowing the increase of the regenerated production (Sterner, 1986). From rate processes to extensive properties: interaction between copepods and phytoplankton under turbulence Through the enhancing effects of turbulence on copepod activity (higher feeding and excretion rates, higher foraging activity by enhanced swimming pattern), the turnover rate of primary producers should increase. On the contrary, the turbulenceinduced lower gross-growth efficiency tends to depress the production rate of copepods. As a conCOPEPODS UNDER TURBULENCE 189 FIG. 10. – Effects of the interaction between turbulence and zooplankton on the evolution of natural phytoplankton communities. Time changes of phytoplankton biomass (chlorophyll) on natural marine communities developed in laboratory microcosms. Q: Calm conditions without zooplankton. QZ: Calm conditions with zooplankton added. A: Turbulent conditions without zooplankton. AZ: Turbulent conditions with zooplankton. Continous and dashed lines correspond to the two duplicates for each experimental condition. Abscissae: Time in days. Ordinate: µg Chla/l. While no significant differences were observed amongst microcosms under calm (Q), turbulent (A), or calm conditions with zooplankton (AZ), the pressence of zooplankton in turbulent microcosms significantly modified the temporal evolution of phytoplankton biomass. (Modified from Alcaraz et al., 1989). sequence of the reduction on the growth of copepod populations, the overall grazing pressure on primary producers is significantly reduced. To these direct effects of turbulence on copepod activity, other indirect effects must be added. The increase of phytoplankton production caused by turbulence (Margalef, 1974; Legendre, 1981), and the changes on qualitative properties of phytoplankton like cell size, life-forms selection, and chemical composition (Margalef, 1978; Marrasé, 1986; Kiørboe et al., 1990; Estrada et al., 1987 a; Estrada and Berdalet, 1997), would affect the feeding activity of herbivorous copepods. At the smaller length-scales, turbulence will have effects only at the individual level. However, its consequences accumulate and translate into changes in the planktonic community, modifying the structure and function for the whole ecosystem. The study of the effects directly induced by turbulence on natural systems is complicated, amongst other reasons, by the impossibility of controlling turbulence, or of separating its effects from other co190 M. ALCARAZ variant factors (i.e., nutrients and light: Estrada et al., 1987 a, b; Alcaraz et al., 1989; Marrasé, 1986). These inconveniences are partly prevented by the use of laboratory microcosms. The existence of well-defined boundaries, their replicability, and the possibility of controlling environmental factors, allow the study of the direct effects of turbulence on the evolution of the structure and dynamics of planktonic systems (Perez et al., 1977; Nixon et al., 1979; Oviatt, 1981; Alcaraz et al., 1989). Nevertheless, due to scale constraints and altered spatial and temporal variability patterns, microcosms must not be considered as laboratory replicates of natural ecosystems (Harte et al., 1980). In studies addressed to experimentally verify the Margalef (1978) model about the selection of phytoplankton life-forms in relation to the environmental turbulence and nutrient conditions (Estrada et al., 1987 a, 1988), the effects of trophic interactions with planktonic herbivores was also studied (Alcaraz et al., 1989). In all the microcosm experiments, and regard- less of the nutrient or turbulence conditions, the time-course of phytoplankton biomass followed a similar pattern. After few days of enclosing the experimental communities, there was the development of a phytoplankton burst composed by centric diatoms, similar to the spring phytoplankton bloom. This was followed by a decline in phytoplankton biomass to values similar to the initial conditions (Marrasé, 1986; Estrada et al., 1987 a, b; Alcaraz et al., 1988, 1989). No significant differences were observable when comparing calm microcosms (with and without copepods), or turbulent microcosms in which copepods had been removed. On the contrary, when the trophic structure of plankton was not changed (herbivorous copepods not excluded), turbulence induced significant changes in the time-course of phytoplankton biomass development (Alcaraz et al., 1988, 1989). There was a delay in the development of the phytoplankton bloom with respect to calm microcosms (Fig. 10), or secondary blooms occurred. The values of integrated phytoplankton biomass were also higher, and there was a tendency towards the selection of larger sized phytoplankton cells, independently of the possible formation of large aggregates of plankton and detritus due to the coagulative effects of turbulence (Oviatt, 1981; Alcaraz et al., 1989; Kiørboe, 1997). The evolution of the taxonomic composition of phytoplankton assemblages, although modulated by turbulence conditions, appeared more dependent on the successional stage of the natural communities (Estrada et al., 1987a). The trends observed in the evolution of the state variables of primary producers in microcosms confirm the cumulative effects of enhanced rateprocesses of copepods at an individual level under TABLE 8. – Effects of turbulence on the trophic efficiency (ratio consumers biomass/producers biomass) of copepod communities (Acartia grani) in laboratory microcosms at equivalent initial food conditions, copepod abundance and sex ratios. Day: days after starting the experiment. C: calm. T: turbulence. In parentheses: standard error of the mean. (Modified from Saiz et al., 1992). Day Trophic efficiency Calm Turbulence 0 4 8 12 16 0.031 0.012 0.132 0.280 3.210 0.029 0.010 0.095 0.600 1.070 0.731 (0.619) 0.361 (0.208) Mean turbulence. The higher values of integrated phytoplankton biomass are consistent with the reduction of consumers biomass, a general tendency observed in microcosms under turbulence (Oviatt, 1981; Alcaraz et al., 1988, 1989). The consequences from a functional point of view are the final reduction of the grazing pressure, and the lower trophic efficiency of the system (Table 8), which result in a reduction of the biomass of consumers (copepods) supported per unit of producers biomass (phytoplankton). Global effects of turbulence on pelagic systems The control exerted by mechanical (exosomatic) energy on plankton distribution (Mackas et al., 1985; Tett and Edwards, 1984), production (Margalef, 1974; Legendre, 1981) and selection of phytoplankton life forms (Margalef, 1978), is particularly evident in relation to hydrographic singularities that occur across a wide range of space and time. In the majority of examples in which the structure, spatial distribution, and relative proportion of the trophic components in pelagic systems appear related with the forcing induced by exosomatic energy, the characteristics of small-scale turbulence play an important role (Cushing, 1989; Kiørboe, 1993). The matter and energy originated from phytoplankton production circulates in pelagic systems across two main trophic webs. By the classical, herbivorous food webs, the production of relatively large phytoplankton is transferred to higher trophic levels mainly through herbivorous copepod grazing; by microbial food webs, phytoplankton production goes to microheterotrophs (bacteria), and enters the microbial loop (Azam et al., 1983; Le Fèvre and Frontier, 1988). The relative importance of either of the two transfer pathways has significant consequences for the ultimate fate of the biogenic carbon. The carbon circulating through the microbial loop returns to the atmosphere in about < 10-2 years, and constitutes the short-lived carbon pool. When biogenic carbon circulates via classical herbivorous food webs (mainly copepods), its turnover time ranges from > 10-2 to 102 years, which correspond to the long-lived or sequestered pools (Legendre et al., 1993). The selection of either of two transfer pathways is in part controlled by the coupling between the temporal scales of energy inputs (responsible for the phtyoplankton outbursts), and those correCOPEPODS UNDER TURBULENCE 191 sponding to the different trophic compartments (i.e., the response time of bacteria, bacterivores, phytoplankton and herbivorous copepods). In marine areas where the energy inputs are periodic, the cycles of stabilization-destabilization can induce phytoplankton pulses, either tuned or not with the time-response of the different groups of heterotrophs. This is the case observed by Holligan et al. (1984a, b) and Le Fèvre and Frontier (1988) in the vicinity of the English Channel, where the heterogeneity in the spatial distribution of the different trophic groups of plankton is highly persistent and related to the different frequencies at which mechanical energy inputs occur. At a thermally stratified zone on the shelf and a tidal front, the dominant periodicity of energy inputs corresponds to the alternation between neap and spring tides that allows short phytoplankton pulses every two weeks. Due to the lack of tuning between the frequency of phytoplankton pulses and the time-response of herbivorous zooplankton, these areas are cumulative biotopes. The biomass of primary producers is not grazed and a microhetrotrophic food web develops, although eventually, microheterotrophs can be grazed upon by large macrozooplankton. In the Shelf-Break zone, the periodicity corresponds to the M2 tide. The frequency of phytoplankton bursts is coupled with the response time of herbivorous copepods. The result is a quasi-permanent regime that leads to a classical food web dominated by herbivorous copepods (Le Fèvre and Frontier, 1988; Legendre et al., 1993). When the inputs of external energy are not periodic (i.e., weather induced), the spatial heterogeneity in the planktonic trophic groups is less persistent, and the changes in the trophic pathway are hardly reflected by the taxonomic structure of the planktonic communities. This is the case observed in the vicinity of the Catalan density front in the Western Mediterranean (Estrada and Margalef, 1988; Font et al., 1988), where the spatial heterogeneity of the different trophic groups is weak. In such circumstances, the time changes in the relative importance of both transfer pathways are better indicated by the relationships between rate processes of the different trophic groups, which respond almost immediately to biological (trophic) or physical (turbulence) stimulation (Alcaraz et al., 1994 a, b; Calbet et al., 1996), and are in agreement with the intermittent and fluctuating nature of turbulence. 192 M. ALCARAZ CONCLUSIONS Apart from the changes in the velocity components of planktonic organisms (and consequently on their rate of encounter) due to hydrodynamism, small scale turbulence enhances copepod rate processes similar to an increase in temperature (i.e., higher feeding, respiration, excretion, swimming behaviour, and development rates), and modifies organism size and even sex determination. The changes on copepod rate processes at the individual level translate, through cumulative processes, to changes in the extensive properties of whole plankton communities. Our knowledge about the functional response of copepod rate processes to changes in physical, chemical or biological conditions, and the corresponding interaction with other trophic components of the pelagic system, derives from laboratory experiments. Until recent years, the importance of turbulence had not been considered and, as a consequence, the underestimated activity rates used to produce plankton production models have been biased. The forcing induced by small-scale turbulence on the feed-back mechanisms that control the interaction between phytoplankton and herbivorous copepods is schematized in Fig. 11 (Saiz, 1991). However, the functional response of planktonic copepods to small-scale turbulence has been only partially studied. Uncertainities derive not only from the observed species-specific differences in the organismal reponse to turbulence. An important unresolved problem refers to the “quality” of the turbulent flow generated in laboratory experiments, which need to be compared with the characteristics of “true” field turbulence (Strickler et al., 1997). A second source of undetermination arises from the turbulence intensity used in laboratory studies. The energy dissipation rates of experimentally generated turbulence (ε) usually correspond to the highest values recorded in highly dynamic marine environments, which represent a reduced proportion of the overall marine turbulence (Peters and Redondo, 1997). Nevertheless, average values of ε do not adequately represent singular, extreme values as expected taking into account the intermittent nature of small-scale turbulence. Planktonic copepods occupy a key position in planktonic systems. Their size, swimming velocity and feeding behaviour could explain their evolutive success and the important role played in the matter and energy flow in aquatic systems. Copepods feed FIG. 11. – Diagram of the effects of turbulence on rate processes of zooplankton and qualitative and quantitative properties of phytoplankton at the individual level, and their consequences for plankton communities and ecosystem function. (Modified from Saiz, 1991). in a “viscous” world, at low Reynolds numbers (Re ≈ 1), but are preyed upon and develop escape responses in the “inertial” realm, under high Reynolds numbers (Re up to 1000: Naganuma, 1996), linking primary producers with carnivores (mainly fishes). For this reason, a better understanding of the changes induced by small-scale turbulence on the processes taking place in this border line between viscous and inertial forces would represent a significant step in the knowledge of pelagic systems. ACKNOWLEDGEMENTS This work was made possible by the organizers of the MAST-II Advanced Course “Ocean turbulence: A basic environmental property for plankton”, and financially supported by the CICYT grants AMB94-0853 and AMB94-0746. The author wishes to express his gratitude to C. Marrasé and unknown referees for their critical reading of the manuscript. COPEPODS UNDER TURBULENCE 193 REFERENCES Alcaraz, M. – 1977. Ecología, competencia y segregación en especies congenéricas de copépodos (Acartia). Ph. D. Thesis, Univ. Barcelona. Alcaraz, M., M. Estrada and C. Marrasé. – 1989. Interaction between turbulence and zooplankton in laboratory microcosms. In: Proceedings of the 21st. EMBS. Polish Acad. of Sci. pp. 191-204. Alcaraz, M., G.A. Paffenhöfer and J.R. Strickler. – 1980. Catching the algae: A first account of visual observation of filter-feeding calanoids. Am. Soc. Limnol. Oceanogr. Spec. Symp. 3: 241-248. Alcaraz, M., E. Saiz and A. Calbet. – 1994a. 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