Remote prey detection in Oithona similis: hydromechanical versus

Journal of Plankton Research Vol.22 no.6 pp.1155–1166, 2000

Remote prey detection in Oithona similis: hydromechanical versus chemical cues Camilla Svensen and Thomas Kiørboe1 The Norwegian College of Fishery Science, University of Tromsø, N-9037 Tromsø, Norway and 1Danish Institute for Fisheries Research, Charlottenlund Castle, DK-2920 Charlottenlund, Denmark Abstract. We quantified prey encounter rates and prey reaction distances in the ambush-feeding cyclopoid copepod Oithona similis by video recording freely swimming copepods at different concentrations of prey, the dinoflagellate Gymnodinium dominans. Prey encounter rate increased with prey concentration, and a maximal clearance rate of 0.42 ± 0.10 ml h–1 was estimated. The average distance (from the antennules) at which O.similis reacts to prey is 0.014 ± 0.007 cm. A simple prey encounter model was used to combine observed predator and prey velocities and prey reaction distance, and yielded a clearance rate similar to that estimated directly from prey encounter rates. The observed prey reaction distance was consistent with that estimated from a published model of hydromechanical prey perception. The possibility of remote chemodetection was examined by modeling the distribution of solutes leaking out of a swimming cell. The cell leaves a long slender chemical trail in its wake. However, since the ambush-feeding O.similis is essentially stationary when perceiving prey, it is the width rather than the length of the trail that matters. Owing to advection, the chemical signal vanishes almost instantaneously off the sides of the swimming flagellate, and solute concentrations are below any likely detection threshold within 40–50 µm from the flagellate. Our observations are thus inconsistent with remote chemodetection in O.similis. The considerations are generalized, and it is concluded that ambush-feeding copepods, unlike cruisers and suspension feeders, cannot utilize chemical signals for the detection of individual prey, but rely on either hydromechanical detection or direct interception of prey.

Introduction Small marine cyclopoid copepods are often numerically dominant in the marine pelagic environment and, hence, are potentially significant in pelagic material processing [e.g. (Gonzáles and Smetacek, 1994; Nielsen and Sabatini, 1996)]. Yet, the biology of most species is poorly studied and incompletely understood. Oithona similis, one of the most studied cyclopoids, can be characterized as an ambush feeder [e.g. (Kiørboe and Visser, 1999)]. Like other cyclopoids, it does not generate a feeding current (Paffenhöfer, 1993), but remains motionless in the water for most of the time (Hwang and Turner, 1995). It feeds mainly on motile prey (Drits and Semenova, 1984; Sabatini and Kiørboe, 1994) and on sinking fecal pellets (Gonzáles and Smetacek, 1994). Coprophagous feeding in O.similis can be very efficient in recycling fecal material within the euphotic zone (Gonzáles and Smetacek, 1994). Little is know about how O.similis, or other ambush-feeding copepods, perceive their prey. Owing to the presence of numerous long mechanoreceptory setae on the antennules of O.similis, Kiørboe and Visser proposed that O.similis perceives motile (or sinking) prey remotely by the hydrodynamic disturbances these generate in the ambient water (Kiørboe and Visser, 1999). Gonzáles and Smetacek, in contrast, suggested that O.similis utilize chemical cues to detect prey (Gonzáles and Smetacek, 1994). However, no detailed descriptions of feeding © Oxford University Press 2000

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behavior and prey response distances are available to help resolve the influence of these different cues. Here we report on prey searching behavior and prey reaction distances in O.similis preying on swimming dinoflagellates, Gymnodinium dominans. We make direct comparisons of observed reaction distances with predictions of a model of hydromechanical prey detection described by Kiørboe and Visser (Kiørboe and Visser, 1999). We also examine by simple models the possibility of O.similis utilizing chemical cues to detect prey, as suggested by Gonzáles and Smetacek (Gonzáles and Smetacek, 1994). We demonstrate good correspondence between predictions of the hydromechanical model and observations, and incompatibility between observations and chemical prey detection. Our results have more general application to prey detection mechanisms in ambush-feeding copepods. Method Zooplankton for the experiments were collected in December in the Øresund, Denmark. Collection temperature and salinity were 10°C and 17–20‰ S, respectively. In the laboratory, adult females of O.similis were separated in 5 l beakers with filtered seawater, and Heterocapsa triquetra and Dunaliella marina were provided as food. The copepods were kept in darkness and acclimated to the experimental conditions of 15°C and 20‰ S for at least 24 h. Prior to experiments, the copepods were kept in filtered seawater overnight and acclimated to the experimental food condition for at least 1 h. In the feeding experiments, we used the heterotrophic dinoflagellate G.dominans (equivalent spherical diameter 19 µm) as prey. Gymnodinium dominans was isolated from the Øresund by H.H.Jakobsen (Danish Institute for Fisheries Research) and was kept on a diet of Rhodomonas salina. Before experiments, G.dominans was acclimated to the experimental salinity and temperature conditions for 24 h. Oithonia similis feeding behavior was studied by video recording freely swimming females. From video recordings, we could quantify prey reaction distances and prey encounter rates. Oithona similis females were filmed twice in filtered seawater and at eight concentrations of G.dominans (17–350 cells ml–1). Concentrations of G.dominans were estimated from four 1-ml samples that were fixed with Lugol’s solution and counted under a dissecting microscope. All filming was conducted in a 1 l Plexiglas aquarium (10 10 10 cm3) with ~50 females. Filming equipment consisted of a CCD video camera (Mintron MTV 1802CB) equipped with a 105 mm Nikon macrolens. The camera was connected via a time–date generator (Panasonic, WJ-810) to a VCR (NV-FS 200 HQ) and a monitor. Illumination was provided from the back and from the side from infrared-light-emitting diodes (LED), and light was collimated through 10-cmdiameter convex lenses. The camera was placed 20–25 cm from the aquarium and mounted on a rack that could be regulated in height as well as be moved from side to side and back and forth. When filming, one animal at a time was kept in focus by moving the camera, thus keeping the magnification constant. Randomly chosen copepods were filmed continuously for 2–5 min, and the total filming time at each concentration of food was ~1 h. 1156

Cues for remote prey detection in O.similis

The videotapes were analyzed for the general behavior of O.similis females in filtered seawater and at an intermediate (~125 cells ml–1) and a high (~250 cells ml–1) concentration of G.dominans. General behavioral parameters were sinking speed, jump frequency, jump length and jump speed. A detailed description of the prey encounter behavior was also provided. Over the full range of prey concentrations, we recorded prey encounter rates, prey handling time and, whenever possible, measured the distances of reaction to attacked prey. Sinking speed, jump length and jump speed were calculated by marking the position of the tip of the head at appropriate time intervals. Because sinking of O.similis is so slow, we had to correct for the unavoidable convective flows in the aquarium by subtracting the velocity of neutrally buoyant pollen grains from the sinking speed of O.similis. Jump frequency included all jumps longer than one body length (~500 µm). Reaction distance was defined as the shortest distance between the prey and the antennules immediately prior to an attack. Periods when the copepods were close to the surface, bottom or walls of the aquarium were excluded from the analysis. The swimming speed of G.dominans was analyzed by marking trails of individual flagellates on a plastic sheet. Gymnodinium dominans swims in helices, and because our filming was in two dimensions, we selected flagellates that were swimming perpendicular to the camera axis. The swimming speed, vhelix, was then calculated as: vhelix = √vx2 + (2fA)2

(1)

where vx is the tangential swimming speed, i.e. the transportation rate along the helical axis (length, l, of a helical cycle divided by the duration, T, of a cycle, l/T), f is the cycle frequency (f = 1/T ) and A is the amplitude of the helix. The swimming speed, vhelix, is relevant for the computation of the fluid disturbance generated by the flagellate, while the transportation rate, vx, is relevant for the calculation of the encounter velocity. Results and discussion Prey swimming velocity Gymnodinium dominans swims in helices with an amplitude of 0.005 cm, at an average swimming velocity, vhelix, of 0.058 cm s–1, and an average transportation rate, vx, of 0.037 cm s–1 (Table I). Motility of O.similis Oithona similis females sink slowly, 0.009 cm s–1, interrupted by relatively infrequent jumps (5–8.4 jump min–1) of ~2 mm length (Table II). The jump motion is generated by a backward stroke of the antennules, as illustrated in Figure 1A. Both jumps frequency and jump length varied significantly with food concentration (ANOVA, P < 5%; Table II). It is unlikely that jumping significantly increases the volume searched for food in O.similis. For such a saltatory prey’s 1157


Table I. Parameters used to characterize swimming in G.dominans. Average ± SD. T is the duration of one helix, A is the helix amplitude, L is the length of one helix, F is frequency (1/T ), vx is the transportation rate (L/T ) and vhelix is the swimming speed calculated from equation (1). N is the number of observations T A L Helix duration Helix amplitude Helix length (s) (cm) (cm)

F Frequency (s–1)

vx Transportation rate (cm s–1)

vhelix Swimming velocity (cm s–1)

N

0.66 ± 0.18

1.63 ± 0.45

0.037 ± 0.006

0.058 ± 0.007

8

0.005 ± 0.001

0.024 ± 0.006

Table II. Behavioral characteristics of O.similis at various prey concentrations: sinking speed, jump frequency, jump length and jump speed (average ± SD). Numbers of observations are given in parentheses Cell concentration Sinking speed (cm s–1) (ml–1)

No. of jumps min–1 Length of jumps (cm)

Speed of jumps (cm s–1)

0 124 246

7.4 ± 2.3 (15) 5.0 ± 1.7 (15) 8.4 ± 2.5 (22)

1.4 ± 0.2 (10) 1.6 ± 0.1 (7) 1.3 ± 0.2 (10)

0.009 ± 0.002 (14)

0.18 ± 0.03 (10) 0.23 ± 0.04 (7) 0.17 ± 0.04 (10)

search strategy to be efficient, jump length should be of a similar magnitude to prey perception distance and jump frequency should be high (O’Brien et al., 1990). Neither appears to be the case (cf. the estimated prey reaction distance below). The distance covered by jumping far exceeds that covered by sinking and is, thus, sufficient to prevent net settling of the copepods. This may be the main effect of jumping in O.similis, which can thus be considered a true ambush feeder. Prey encounter and feeding behavior Oithona similis discovers prey particles by the antennules or telson (only rarely observed) and attacks the prey by jumping towards it, placing its mouthparts at the spot where the prey was discovered. This is followed by a period of rapid movements of the mouthparts, after which the copepod jumps away from the place of attack (occurred in 80% of the observations). The time period from the attack on prey until the copepod jumps away is referred to here as the handling time. The handling time of a copepod attacking G.dominans is 0.96 ± 0.58 s (average ± SD). This sequence of events is defined as an encounter event, even when the prey particle could not be seen. During the encounter events where the position of the prey particle was clearly identifiable, the distance between the antennules of O.similis and the prey immediately prior to attack (i.e. the reaction distance) was 0.014 ± 0.007 cm (average ± SD, n = 27). Reaction distances and examples of the orientation of the copepod before an attack are illustrated in Figure 1B. 1158


Fig. 1. (A) Schematic diagram illustrating the position and orientation of an O.similis female during a jump (positions 1–5). Most of the time the copepod is sinking slowly in the water, as in position 1. When jumping (positions 2–4), the antennules are swept backward, resulting in replacement and change of orientation of the copepod (position 5). (B) Schematic diagram of the position and orientation of O.similis and its prey G.dominans (small dots) immediately prior to attack in 14 different cases. Most often, the prey are close to one of the antennules of the copepod before an attack, but presumably the prey can also be detected by the mouthparts, as is possibly the case in numbers 6 and 9.

Encounter rate as a function of prey density With the adopted definition of an encounter event, we observed a few ‘apparent’ encounters even in filtered seawater (0.03 min–1, n = 17). Encounter rates in the presence of food were invariably higher (0.08–0.56 min–1, n = 14–23 at each prey 1159


Fig. 2. Encounter rate between O.similis and its prey (G.dominans) as a function of prey density. An apparent encounter rate in filtered seawater of 0.03 s–1 (n = 17) was subtracted from all observations. Holling’s disk equation was fitted to the observations. R2 = 0.88.

density), and observed encounter rates, corrected for encounter rate in filtered seawater, increased with increasing prey concentration in a saturating response (Figure 2). We fitted Holling’s disk equation [see e.g. (Saiz and Kiørboe, 1995)] to the observed encounter rates: E = C/(1 + bC)

(2)

where E is encounter rate, C is prey concentration, is the instantaneous rate of prey encounter (or maximum clearance rate at low prey concentration) and b is the inverse half-saturation concentration (Figure 2). How does the maximum clearance rate thus estimated, 0.42 ± 0.10 ml h–1 (mean and 95% confidence limit), compare with the clearance rate that can be estimated from the reaction distance? If we assume that all prey passing within 1 reaction distance (R) from the antennae are perceived, then the perception volume becomes a cylinder of the length of the antennae (d) and with radius R. The clearance rate () is then the velocity difference between predator and prey (v) multiplied by the cross-sectional area of the perceptive volume perpendicular to the arrival direction of the prey. Assuming random arrival direction of the prey () and integrating over all directions, this becomes: 1 /2 2 4 = — 2Rdvcosd + — R2vsind = — Rd + 4R2 v 0 –/2

(3)

The first integral corresponds to encounters over the length of the cylinder and the second integral is encounters at the ends of the cylinder. The velocity 1160


difference between predator and prey is due both to the transport velocity of the prey (vx) and the sinking velocity (vs) of the predator. Again assuming random relative directions, the average velocity difference can be estimated as (Evans, 1989): v = (vx2 + vs2)0.5

(4)

Inserting estimates of R (0.014 cm), d (0.1 cm), vx (0.037 cm s–1) and vs (0.009 cm s–1) in the above equations yields an estimated clearance rate of 0.35 ml h–1. One may argue that the effective encounter radius is larger than the reaction distance due to the spiraling movement of the prey, and that the amplitude of the helix (0.005 cm; Table I) should be added to R in the above equations. If we do so, the estimated clearance rate becomes 0.53 ml h–1. These two extreme estimates are both within the confidence limits of the directly estimated clearance rate. Thus, the encounter rate model [equation (3)] properly describes the observations and the two independent assessments of the reaction distance are consistent with one another. Hydromechanical prey detection in O.similis A swimming prey causes the ambient fluid to move. Because hydromechanical perception is based on the bending velocity of the setae (Yen et al., 1992), Kiørboe and Visser proposed that signal strength due to small prey simply equals the magnitude of the fluid velocity due to the motion of the prey (Kiørboe and Visser, 1999). This fluid velocity declines with increasing distance to the prey. Assuming that a threshold signal strength (u*) is required to elicit a behavioral response and assuming Stokes’ creeping flow around a moving prey of radius a, the reaction distance can be approximated (for R >> a) by (Kiørboe and Visser, 1999): R ≈ K vhelixa/u*

(5)

K is a parameter (dimensionless) that varies between 3/2 (directly in front of the prey) and 3/4 (directly off its equator) and is thus near 1. From reported clearance rates on various swimming protozoans and sinking fecal pellets, spanning about three orders in magnitude, and by employing a slightly simpler encounter rate model than equation (3), Kiørboe and Visser estimated a threshold signal strength for prey detection of u* = 0.004 cm s–1 in O.similis (Kiørboe and Visser, 1999). Inserting this value and estimates of a (9.5 10–4 cm) and vhelix (Table I) in equation (5) yields R ~ 0.014 cm, i.e. similar to that observed. Figure 3a graphically illustrates the 0.004 cm s–1 velocity isoline around a moving sphere of the size and velocity of G.dominans. The position of this isoline indicates the distance at which O.similis can detect a swimming G.dominans hydromechanically. Stokes’ creeping flow is only strictly valid for a sphere moving under the influence of a body force (such as a fecal pellet sinking due to gravity) that exerts only drag on the fluid. A self-propelled body (such as a swimming flagellate), on the other hand, which exerts both drag and thrust on the fluid, may be better modeled 1161


Fig. 3. Ambient fluid velocity generated by swimming G.dominans. The 0.004 cm s–1 isoline has been shown, corresponding to the detection threshold in O.similis. The position of the isoline thus corresponds to the reaction distance for various orientations of the prey relative to the predator. Fluid velocities are computed assuming Stokes’ creeping flow (a) or a dipole (b); see the text.

as a force dipole [cf. (Childress, 1981), p. 15]. The absolute velocity generated in the ambient fluid by a dipole can be written in polar (r, ) coordinates as [(Leal, 1992), p. 238]:

–3s(1 + 3 cos(2)) u = ————————— 2r 2 1162

(6)


where is the direction relative to the movement direction of the flagellate, r is the distance from the dipole center and s is the dipole strength. The latter can be approximated (from dimension analysis) by: s = vhelix a2

(7)

The reaction distance R = r(u = u*) can then be estimated by solving equations (6) and (7) for r at u = u*: R=

3v a (1 + 3 cos(2)) ——————————— 2u* helix

2

0.5

(8)

Directly in front of the moving flagellate ( = 0), R = 0.016 cm, and off its equator ( = /2), R = 0.011 cm, i.e. estimates similar to the reaction distance observed. Figure 3b depicts the 0.004 cm s–1 velocity isoline for a dipole, using the size and swimming velocity of G.dominans. The two models (creeping flow, dipole) thus yield reaction distances of the same magnitude, and both estimates are similar to that actually observed. We did not attempt the application of more elaborate models [cf. (Bundy et al., 1998)], but conclude that our observations are consistent with hydromechanical prey perception in O.similis. Chemical prey detection in O.similis Several species of copepods have been shown to be able to perceive and behaviorally respond to solute substances in the water [e.g. (Gill and Poulet, 1988)], and chemical detection of small prey has been postulated in copepods that generate a feeding current (Andrews, 1983; Moore et al., 1999). Gonzáles and Smetacek suggested that O.similis perceives falling fecal pellets by means of chemoreception (Gonzáles and Smetacek, 1994). Are our observations of detection distances consistent with remote chemodetection of small swimming prey in O.similis that does not generate a feeding current? And is chemoreception a feasible mechanism for the remote detection of sinking fecal pellets? To address these questions, we modeled the spatial distribution of solutes leaking out of a moving particle. The distribution of solutes is governed by the leakage rate of solutes from the prey cells (Q; mol s–1) and by both advection and diffusion. We will consider free amino acids, because it has been demonstrated that other copepods can perceive and respond to dissolved amino acids. Reported concentration thresholds for neurophysiological responses in copepods are down to ~10–9 M (Yen et al., 1998), but behavioral responses have been recorded only at 10–6–10–8 M (Gill and Poulet, 1988) or higher (Poulet and Ouellet, 1982) concentrations of amino acids. If we generously assume that G.dominans leaks 50% of its nitrogen content per day as amino acids, then Q can be estimated to be ~10–15 mol amino acids s–1 [assuming cell carbon content = 10–7 µg C µm–3; C:N = 6.6; 0.75 mol amino acid (mol N)–1]. Amino acids have diffusion coefficients (D) of ~10–5 cm2 s–1. Again assuming Stokes’ creeping flow, we solved the advection–diffusion equations numerically, largely as in Karp-Boss et al. [(Karp-Boss et al., 1996), their 1163


Fig. 4. Spatial distribution of free amino acids leaking out of a moving G.dominans cell. The computations have been made on the assumptions specified in the text, and approximately as described in Karp-Boss et al. (Karp-Boss et al., 1996). (A) and (B) are two different magnifications. The depicted isolines are 10–6 [not in (A)], 10–7, 10–8 and 10–9 M.

appendix 2], and computed the spatial distribution of amino acids around a moving G.dominans (Figures 4 and 5). A moving cell leaves a long slender chemical trail behind it. A non-swimming copepod like O.similis cannot, however, really take advantage of the length of the trail. What matters is rather the extension of the plume perpendicular to the prey’s direction of motion. Off the cell’s equator, the concentration falls off rapidly and is less than any likely detection threshold within 40–50 µm from the center of the cell (Figure 5). Owing to diffusion, the chemical trail widens out somewhat behind the moving prey, but only at a considerable distance from the prey is the trans-sectional radius of the trail similar to the detection distance observed here. For example, the maximum radius of the plume described by the 10–8 M concentration isoline is 0.014 cm, but this width is only reached ~0.3 cm behind the particle, i.e. long after the prey itself has passed by. Predator motility would help detect long slender chemical trails, but O.similis is essentially motionless when detecting a prey. Thus, chemical detection is inconsistent with the behavior of O.similis. Gonzáles and Smetacek had sinking copepod fecal pellets in mind when suggesting chemodetection in O.similis (Gonzáles and Smetacek, 1994). However, chemodetection of sinking fecal pellets is even less likely than chemodetection of small moving flagellates. The dimensionless Peclet number (Pe = 2au/D) describes 1164


Fig. 5. Concentration gradients of amino acids leaking out of a moving G.dominans cell. Computed as in Figure 4. Concentration gradients behind (downstream), in front of (upstream) and off the side (equator) of the swimming cell are shown.

the importance of advection relative to the importance of diffusion in distributing leaking chemicals. The higher the Peclet number, the steeper the concentration gradients off the side of the moving particle. Pe for the swimming dinoflagellate is 11, but it is 116 for a 50-µm-radius fecal pellet sinking at 100 m day–1. Thus, solute concentrations due to leakage from a fecal pellet vanish rapidly off the side of the pellet. Conclusions Generally, our considerations suggest that chemical detection of individual prey is unlikely in ambush-feeding zooplankters. Predator motility—in a general sense—is required to utilize chemical signals from individual prey. Copepods generating a feeding current may use chemical information for remote prey detection (Andrews, 1983), as may male copepods swimming in search for mates (Tsuda and Miller, 1998; Yen et al., 1998), also in Oithona spp. (Uchima and Hirano, 1988). It thus follows that prey capture in ambush feeders requires mechanosensory detection or direct prey interception. The latter is likely to be the case in many passive flux feeders (Jackson, 1993), including some copepods (Dagg, 1993). Gonzáles and Smetacek demonstrated that residing populations of O.similis may efficiently prevent vertical fecal pellet fluxes in the ocean, and that they provide an efficient ‘coprophagous filter’ (Gonzáles and Smetacek, 1994). The detection distances required for high ‘filter efficiency’ are substantial (Kiørboe and Visser, 1999) and, according to the results presented here, can be accomplished only by hydromechanical rather than chemical remote detection of sinking pellets. 1165


Acknowledgements This work was supported by grants from NoRFA to C.S. and from the Danish Natural Sciences Research Council to T.K. (# 9801393). Uffe Thygesen wrote the MatLab code to solve the diffusion–advection equations. Andy Visser and Stefan Mayer provided advice on hydrodynamical modeling. We thank them all. References Andrews,D.J. (1983) Deformation of the active spaces in the low Reynolds number feeding current of calanoid copepods. Can. J. Fish Aquat. Sci., 40, 1293–1302. Bundy,M.H., Gross,T.F., Vanderploeg,H.A. and Strickler,J.R. (1998) Perception of inert particles by calanoid copepods: behavioral observations and a numerical model. J. Plankton Res., 20, 2129–2152. Childress,S. (1981) Mechanics of Swimming and Flying. Cambridge University Press, Cambridge, 155 pp. Dagg,M. (1993) Sinking particles as a possible food source of nutrition for the large calanoid copepod Neocalanus cristatus in the subarctic Pacific ocean. Deep-Sea Res., 40, 1431–1445. Drits,A.V. and Semenova,T.N. (1984) Experimental investigations of the feeding of Oithona similis Claus. Oceanology (USSR), 24, 755–759 (English translation). Evans,G.T. (1989) The encounter speed of moving predator and prey. J. Plankton Res., 11, 415–417. Gill,C.W. and Poulet,S.A. (1988) Responses of copepods to dissolved free amino acids. Mar. Ecol. Prog. Ser., 43, 269–276. Gonzáles,H.E. and Smetacek,V. (1994) The possible role of the cyclopoid copepod Oithona in retarding vertical flux of zooplankton faecal material. Mar. Ecol. Prog. Ser., 113, 233–246. Hwang,J.S. and Turner,J.T. (1995) Behaviour of cyclopoid, harpacticoid, and calanoid copepods from coastal waters of Taiwan. Mar. Ecol., 16, 207–216. Jackson,G.A. (1993) Flux feeding as a possible mechanism for zooplankton grazing and its implication for vertical particle flux. Limnol. Oceanogr., 38, 1328–1331. Karp-Boss,L., Boss,E. and Jumars,P.A. (1996) Nutrient fluxes to planktonic osmotrophs in the presence of fluid motion. Oceanogr. Mar. Biol. Annu. Rev., 34, 71–107. Kiørboe,T. and Visser,A. (1999) Predator and prey perception in copepods due to hydromechanical signals. Mar. Ecol. Prog. Ser., 179, 81–95. Leal,L.G. (1992) Laminar Flow and Convective Transport Processes. Scaling Principles and Asymptotic Analysis. Butterworth-Heineman, Boston, 740 pp. Moore,P.A., Fields,D.M. and Yen,J. (1999) Physical constraints of chemoreception in foraging copepods. Limnol. Oceanogr., 44, 166–177. Nielsen,T.G. and Sabatini,M. (1996) Role of cyclopoid copepods Oithona spp. in North Sea plankton communities. Mar. Ecol. Prog. Ser., 139, 79–93. O’Brien,W.J., Browman,H.I. and Evans,B.I. (1990) Search strategies in foraging animals. Am. Sci., 78, 152–160. Paffenhöfer,G.A. (1993) On the ecology of marine cyclopoid copepods (Crustacea, Copepoda). J. Plankton Res., 15, 37–55. Poulet,S.A. and Ouellet,G. (1982) The role of amino acids in the chemosensory swarming and feeding of marine copepods. J. Plankton Res., 4, 341–361. Sabatini,M. and Kiørboe,T. (1994) Egg production, growth and development of the cyclopoid copepod Oithona similis. J. Plankton Res., 16, 1329–1351. Saiz,E. and Kiørboe,T. (1995) Predatory and suspension feeding of the copepod Acartia tonsa in turbulent environments. Mar. Ecol. Prog. Ser., 122, 147–158. Tsuda,A. and Miller,C.B. (1998) Mate-finding behaviour in Calanus marshallae Frost. Philos. Trans. R. Soc. London Ser. B, 353, 713–720. Uchima,M. and Hirano,R. (1998) Swimming behavior of the marine copepod Oithona davisae: internal control and search for environment. Mar. Biol., 99, 47–56. Yen,J., Lenz,P.H., Gassie,D.V. and Hartline,D.K. (1992) Mechanoreception in marine copepods: electrophysiological studies on the first antennae. Invertebr. Biol., 115, 191–205. Yen,J., Weissburgh,M.J. and Doal,M.H. (1998) The fluid physics of signal perception by mate-tracking copepods. Philos. Trans. R. Soc. London Ser. B, 353, 787–804. Received on June 8, 1999; accepted on December 17, 1999

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