Swimming Against the Flow: A Mechanism of Zooplankton Aggregation

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Science  06 May 2005:
Vol. 308, Issue 5723, pp. 860-862
DOI: 10.1126/science.1107834


Zooplankton reside in a constantly flowing environment. However, information about their response to ambient flow has remained elusive, because of the difficulties of following the individual motions of these minute, nearly transparent animals in the ocean. Using a three-dimensional acoustic imaging system, we tracked >375,000 zooplankters at two coastal sites in the Red Sea. Resolution of their motion from that of the water showed that the animals effectively maintained their depth by swimming against upwelling and downwelling currents moving at rates of up to tens of body lengths per second, causing their accumulation at frontal zones. This mechanism explains how oceanic fronts become major feeding grounds for predators and targets for fishermen.

Buoyant phytoplankton and nonliving flotsam accumulate at the sea surface along convergent fronts because they remain afloat while the water submerges (1, 2). Accumulations at fronts have also been reported for zooplankton (3, 4); however, their aggregations often occur below the surface and at both convergent (downwelling) and divergent (upwelling) zones (5). Hardy (6) was the first to suggest that such patchiness must be caused by some dynamic principles involving zooplankton behavior and water movement. A common, yet untested explanation for subsurface accumulations at frontal zones is that the animals actively swim against vertical currents in an attempt to maintain their depth (5, 710). Models (7, 8) show that complete depth retention by zooplankton should generate increasingly dense accumulations, whereas partial retention, due to fatigue or inability to match the velocity of the current, should lead to ephemeral patches. Copepods can form fine-scale aggregations in layers where the turbulence velocity is substantially weaker than their typical swimming speed (11). Although diel vertical migrations are well known among zooplankton in response to seasonal cues, their behavioral response to ambient currents has not been demonstrated in the ocean, largely because of the lack of a technology that can track in situ the motions of these small, nearly transparent organisms in a large volume of water.

We tested the hypothesis that zooplankton swim against vertical currents by acoustically tracking animals while simultaneously measuring currents at two coastal sites in the northern Gulf of Aqaba, Red Sea (table S1). The sites experience persistent (hours-long) periods of upwelling and downwelling driven by differential heating and cooling across the gradually sloping bottom (12, 13) and by the interaction between mesoscale currents and coastal topography. The three-dimensional trajectories of individual zooplankters as small as 1 mm in length were measured with FishTV-1.6 (FTV-1.6), a new, high-frequency (1.6-MHz), multi-beam sonar (14), within volumes of water up to 3.8 m in length and 0.1 to 0.4 m in width (Fig. 1) (15). The sonar's transducer, attached to a large submerged tripod (Fig. 1), was varied in depth and orientation among deployments (table S1). Three experiments using FTV-1.6 accomplished 274 tracking sessions, most of them acquiring >10 min of uninterrupted bioacoustic data at a rate of three “frames” per second, yielding a total of 375,171 tracks. The sessions were performed day and night under conditions of upwelling and downwelling currents (table S1).

Fig. 1.

(A) Schematic drawing of the underwater setup, showing the ∼6-m-high (adjustable) tripod on which the FTV-1.6 transducer and the current meter [Acoustic Doppler Velocimeter (ADV)] were mounted. (B) The volume insonified by the sonar [dotted lines, up to 0.33 m3, indicated by the yellow rays in (A)] with an example of seven zooplankton tracks (solid lines). During the first two experiments, the transducer was oriented horizontally as shown in (A). In the third experiment, the transducer was rotated 90° downward and insonified a volume within 2.2 to 3 m from the transducer (0.6 to 1.4 m above the bottom). The ADV was deployed on a separate tripod, 15 m away, and measured currents 1 m above the bottom. During the first experiment, before the availability of the ADV, currents were measured by video tracking of fluorescein dye (15).

Vertical and horizontal currents at the depth of the insonified volume were measured nearby (<15 m) during each tracking session (Fig. 1) (15). The average vertical flow during the three experiments, approximately 1 cm/s, was 10 to 15% of the prevailing horizontal currents.

Net tows near the insonified volume indicated that during the day, zooplankton assemblages consisted mostly of pelagic species typical of the open waters of the Red Sea (16). At night, the emergence of demersal zooplankton doubled the zooplankton density (17). At all times, copepods were the dominant group (50 to 85% by number). Additional common taxa included mollusks, chaetognaths, and tunicates; and during the night, decapod larvae and other crustaceans. More than 70% of the targets recorded by FTV-1.6 had weak reflectivity (<–80 dB referenced to 1 μPa at 1 m range), in agreement with the dominance in the net samples of small (<5 mm) zooplankton from the aforementioned taxa.

Comparison of the tracks obtained from the sonar with the currents revealed that under both downwelling and upwelling conditions, the zooplankton swam against the vertical currents (Fig. 2 and Table 1). Complete depth retention, with a regression coefficient of –1.0 between the zooplankton's vertical swimming velocity (Vz, relative to water) and the vertical current (Vw), was found in the first and second experiments; and nearly complete retention (Vz = –0.82 Vw) was found in the third experiment (Table 1). These results indicated that under strong vertical velocities, the small zooplankton recorded with FTV-1.6 swam vertically at velocities of >10 body lengths/s. In contrast, the animals' mean horizontal displacement (Hz) was indistinguishable from that of the current (Hw), with a regression coefficient of 1.0 (Hz = Hw) in the first and second experiments, indicating that the animals were passively drifting with horizontal currents; and nearly so (Hz = 0.73 Hw) in the third experiment (Fig. 2).

Fig. 2.

Zooplankton motion versus water velocity along vertical (left panels) and horizontal (right panels) directions during the first (A and B), second (C and D), and third (E and F) experiments. Zooplankton vertical motions are presented as swimming velocities (relative to water), and horizontal motions are absolute (relative to Earth). Each data point indicates the average value of a tracking session (5 to 14 min, 200 to >20,000 measurements). The 95% confidence intervals around each point (not shown) are typically much smaller than the size of the symbol. Dotted lines indicate negative (y = –x, left panels) and positive (y = x, right panels) linear relationships between the parameters. The regression lines between the plotted variables, for which the R2 values are shown, were highly significant (P < 0.001) in all six panels. Solid lines in (E) and (F) indicate the regression lines in the two cases where their slope was different from that of the dotted line. The video dye method of measuring currents during the first experiment (B) allowed the calculation of horizontal speed (scalar), not velocity (15).

Table 1.

Results of the three zooplankton-tracking experiments. Mean (±SD) vertical velocities of currents, zooplankton displacement (relative to Earth), and results of the regression analysis between the zooplankton's vertical swimming velocity (Vz, relative to water) and the vertical current velocity (Vw) under conditions of upwelling, downwelling, and both in each of the three experiments are shown. n, number of tracking sessions. P value, significance level of the regression coefficient (A) as follows: **P < 0.001, ***P < 0.00001. SE, standard error of the regression coefficient. In 3 of the 65 sessions of the second experiment, the vertical current was nearly zero.

Experiment Water current (cm/s) Zooplankton displacement (cm/s) n Regression [Vz = AVw]
A (SE) R2P value
   1 1.37 (±1.7) -0.05 (±0.2) 13 -1.0 (0.03) 0.99 ***
   2 0.56 (±0.42) -0.11 (±0.54) 9 -1.33 (0.24) 0.79 **
   3 0.69 (±0.77) 0.01 (±0.55) 56 -1.11 (0.07) 0.82 ***
   1 -1.5 (±1.2) -0.14 (±0.54) 11 -0.98 (0.09) 0.92 ***
   2 -0.89 (±0.66) -0.05 (±0.4) 53 -1.0 (0.05) 0.87 ***
   3 -1.16 (±0.87) -0.3 (±0.67) 129 -0.75 (0.04) 0.75 ***

Planktonic organisms that maintain their depth are expected to accumulate where vertical currents persist (7, 8). Because shallow downwelling and upwelling zones at the study sites were confined to near-shore waters (12, 13), a greater abundance of zooplankton was expected near the coast (movie S1). To test this prediction, we examined the distribution of zooplankton across the sandy shore of Ras Burka (experiment 1, table S1). The reef site could not be used for this test because of intense predation on zooplankton by reef fishes and invertebrates (18). Three sets of zooplankton sampling were conducted, each consisting of four net tows at different distances from shore (15). Two sets were done during periods of downwelling, and one was done when there was no discernible vertical current. Zooplankton density was approximately three times greater near the downwelling front than in the offshore waters (Fig. 3); no obvious cross-shore pattern was observed when vertical currents were negligible. The cross-shore pattern during downwelling agreed with that predicted by a simulation model (7, 8) using local bathymetry and observed downwelling velocities as input parameters. The simulation indicated that it would take 0.5 to 2.7 hours for depth-keeping animals to triple their density near the shore in the presence of downwelling of 3.6 and 0.4 cm/s, respectively (Fig. 3). Downwelling typically persists for several hours at our study sites (12, 13).

Fig. 3.

Observed (circles) and predicted (lines) zooplankton densities at 3 to 4 m depth across the shore at Ras Burka during downwelling of 0.4 cm/s (A) and 3.6 cm/s (B) on 5 and 6 December 1998, respectively. (C) The corresponding cross-shore profile of bottom depth (thick line), the stream lines generated by equations 2 and 3 in (7) (thin lines), and the vertical velocity at different distances from shore (vertical bars under the bottom axis). The stream lines are plotted evenly spaced on the stream function, so that more condensed stream lines indicate faster flow. Simulated density and vertical velocity are in arbitrary units relative to those farthest from shore. The simulation indicates that under the downwelling velocities measured at our deployment site [square in (C)] during the zooplankton net tows [tow positions are indicated by triangles in (C)], it would take 2.7 and 0.5 hours for depth-keeping animals to generate the cross-shore patterns plotted in (A) and (B), respectively. No obvious cross-shore pattern was observed when vertical currents were negligible (not shown in the figure). See movie S1 for an animated simulation of the accumulation mechanism.

The mechanism used by the zooplankton to sense their depth is currently unknown. Because depth retention was observed at all times, including moonless nights, light is unlikely to be the universal cue eliciting this behavior, although at the shallow depths at which we worked, crustaceans can sense light intensity even at night (19). One possibility is that the animals are sensing pressure. Although pressure sensors have not been identified in copepods, frontal organs of unknown function are found in these organisms (20), and some copepods as well as other crustaceans respond behaviorally to small changes in pressure (2124). Those findings were interpreted as indicating a “biological barostat” by which the animals might maintain constant depth (25). The fact that a cellular-level mechanism for pressure sensing is found in many invertebrates (26) makes pressure an intriguing possibility as a cue for directional swimming and depth maintenance in zooplankton.

The adaptive benefits of depth retention are not well understood. Ultimately, such behavior is necessary to avoid a passive drift into unfavorable depths. Depth preference during ontogenetic development is an effective mechanism for directed horizontal transport in some types of flow (27). Depth-keeping could also be an effective strategy to remain within thin layers of high food concentrations (28), especially if such layers disperse when advected vertically. In addition, because depth-keeping in vertical flows leads to patch formation (7, Fig. 3), this behavior enhances the probability of finding a mate in an otherwise sparsely populated ocean.

The formation of zooplankton patches at fronts has far-reaching implications for their predators. The survival and growth of many zooplankton predators, from invertebrates to whales, depends on their success in finding rich patches of prey (2932); the ambient abundances of zooplankton outside these patches are often too low to maintain the observed rates of predator growth and reproduction (31). If depth retention is pervasive, it could be a key mechanism for the formation of zooplankton patches that predators can dependably locate by tracking well-defined cues (such as a sharp temperature gradient across a front) or foraging in regions of persistent fronts (33). The numerous observations of dense aggregations of zooplankton and their predators at sites of vertical currents (5), including mid-ocean fronts (3), shelf breaks (9), submarine canyons (33), and banks (34), indicate that the phenomenon is widespread. Fishermen also frequent fronts (35). Hence, the zooplankton's ability to swim against the flow appears to have a major effect on the ability of pelagic predators to thrive in an otherwise food-impoverished ocean.

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Materials and Methods

Table S1


Movie S1

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