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Aurelia labiata medusae (Scyphozoa) in Roscoe Bay avoid tidal dispersion by vertical migration
Journal of Sea Research 57 (2007) 281 – 287 www.elsevier.com/locate/seares
Aurelia labiata medusae (Scyphozoa) in Roscoe Bay avoid tidal dispersion by vertical migration David J. Albert Roscoe Bay Marine Laboratory, 4534 W 3rd Avenue, Vancouver, B.C., Canada V6R 1N2 Received 10 January 2006; accepted 14 November 2006 Available online 17 November 2006
Abstract Aurelia labiata reside year around in Roscoe Bay on the west coast of Canada in spite of tides that exchange as much as 10% to 30% of the bay's water twice daily. Large numbers of medusae drift eastward over a gravel bar and out of the bay on ebb tides, only to return on flood tides. Drogues released into the tidal stream at the middle of an ebb tide drifted about 700 m out of the bay and into an adjacent large body of water. With the aid of a viewing box and lift net it was observed that after drifting out of the bay on an ebb tide, medusae remained within 300 m of the bay because they swam into still or counter current water below the turbulent ebb stream. When the tide turned to flood, medusae rose into the still water, became embedded in the nonturbulent flood stream, and drifted back into the bay. Vertical migration appears to enable the dense population of medusae to stay in a single location. This enhances reproductive success by keeping males and females in close proximity and increases survival by keeping the population in a favourable location. © 2006 Elsevier B.V. All rights reserved. Keywords: Northeast Pacific; Zooplankton; Coelenterates; Scyphomedusae; Aurelia labiata
1. Introduction Dense aggregations of Aurelia aurita and Aurelia labiata, commonly known as Moon Jellies, are found in bays and inlets, as well as open coastal oceans (for reviews see Arai, 1997; Lucas, 2001). These aggregations have substantial adaptive significance. The close proximity of males and females facilitates reproduction (Hamner et al., 1994). Dense aggregations also make predation by gelatinous predators more difficult (Purcell et al., 2000). Phacellophora camtschatica and Cyanea capillata scyphomedusae are able to prey upon A. labiata along the fringes, but not within, dense aggregations (Purcell et al., 2000). Finally, medusae may be E-mail address: [email protected]. 1385-1101/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2006.11.002
attracted to and congregate in habitat that contains food resources (Arai, 1992) and is suitable for the survival of planulae and juvenile medusae (Sullivan et al., 1994; Purcell et al., 2000). If dense aggregations of medusae stay in such habitat, the survival of planulae and juvenile medusae should be enhanced (Purcell, 2003). Dense aggregations of medusae are ecologically significant. Aurelia are known to consume fish larvae (for reviews, see Purcell and Arai, 2001; Purcell, 2003). Purcell (2003) has calculated that consumption by individual medusae may be in the 100s or 1000s daily. Large aggregations may impact reproduction of fish species and may also reduce the availability of food for other species. Increasing attention is being directed to understanding how dense aggregations of Aurelia labiata stay in
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one place rather than being dispersed by tides and currents. Hamner et al. (1994) have shown that A. aurita (more likely A. labiata) in Saanich Inlet accumulate and remain in dense aggregations along the southern and eastern shores of the inlet by using sunlight-stimulated horizontal migration. Dense elliptical aggregations in Tokyo Bay (Toyokawa et al., 1997) and Prince William Sound, Alaska (Purcell et al., 2000), appear to persist because medusae swim in directions aligned with the currents of convection cells in the water column. Roscoe Bay, a small bay on the Pacific Coast of Canada, has a dense resident population of A. labiata medusae (Fig. 1; Albert, 2005) that has remained relatively constant in size over the last two years in spite of tidal flushing that on average exchanges more than one-quarter of the bay's water twice daily (Canadian Hydrographic Service, 2005). Casual observations indicated that directional swimming was rare and there was no evidence of swimming guided by convection cells. The present report attempts to elucidate the mechanism by which A. labiata are able to remain in Roscoe Bay. It begins by providing evidence that many medusae actually are unable to resist the tidal flow and are swept out of the bay on ebb tides. A series of observations will indicate that medusae drifting out of the bay on ebb tides entered still and counter current layers of water beneath the ebb stream. These medusae subsequently rose into still water at the end of the ebb tide, became embedded in the flood stream, and returned to the bay.
2. Materials and methods 2.1. Establishing the location of medusae The location of medusae in the bay and narrow channel east of the gravel bar was assesssed by counting the number of medusae visible through a viewing box at 14 stops along the length of the bay and down the middle of the narrow channel east of the bay (Fig. 1, L transect). Counts along transects across counting stops 12, 13, and 14, established more precisely where medusae were in the channel outside of the bay (Fig. 1). There were three viewing points along transects across counting stops 12 and 13, and five viewing points along the transect across stop 14. Counting took 60 to 80 min. Counting usually, but not always, started in the west end of the bay. Counting direction did not alter the pattern of results obtained. The floating viewing box had a Plexiglas bottom (117 cm × 56 cm) and wood sides 46 cm high. To minimise reflections, the box was painted black on the inside and covered with a black cloth. When moving from one stop to another, we put styrofoam pontoons under each side so that the viewing box could be pulled briskly with a small rowboat (2.1 m long). Medusae were counted rapidly at each stop to minimise the influence of those entering or leaving the visual field. To increase assessment stability, the count entered for each stop was the average of several counts, with the viewing box moved slightly between counts. Medusae were counted in the morning or evening, or both. 2.2. Lift net assessment of the number of medusae in the channel A conical lift net (0.70 m dia.; 0.75 m deep, 4 × 4 mm mesh) was used to supplement and confirm visual observations of medusae at transects 1 and 3 in the narrow channel east of the bay. The lift net was lowered to the ocean floor, left for 4 min, and then slowly raised to the surface. Medusae were counted in the net, or in small groups as they were spilled from the net.
Fig. 1. A chart of Roscoe Bay ([124° 46′ W; 50° 09′ 36″ N] modified from Canadian Hydrographic Service Chart 3538 [1996]). The L transect down the centre of the bay had 14 stops (marked by bars) where medusae were counted. Vertical lines through stops 12, 13, and 14, mark the transects across these stops used to assess the position of medusae across the width of the channel. The gravel bar (G) dries at lower low water. North is at the top. The vertical line just east of Marylebone Pt is 124° 45′ W. A large deep water channel (Waddington Channel; 1800 m wide) is east of Marylebone Point. Depth contours in the bay and immediately east of the gravel bar are at 5 m intervals at lower low water (LLW).
2.3. Current flow and stratification Drogues were used to evaluate how far ebb currents might carry medusae out of the bay if medusae remained in the ebb stream. Each drogue was constructed of two plastic buckets (0.30 m high; 0.25 m dia) hung one above the other, 1.3 m apart. Each bucket had four plastic vanes (0.30 × 0.36 m) bolted vertically to the sides, 90 degrees apart. A float at the surface and a 2 kg
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weight at the bottom kept the drogue vertical in the water. Since medusae were within 1 to 3 m of the surface as they drifted eastward over the gravel bar, the drogues were set to span the distance from 0.5 to 2.5 m. Current stratification was assessed using a rope with plastic surveyor's flagging (25 mm wide and 1 m long) at 1 m intervals and a 4 kg weight at the bottom. The orientation of the flagging indicated the direction of current flow. 2.4. Accumulation of medusae east of the gravel bar A 36 × 50 × 0.6 cm thick piece of white plastic had pieces of styrofoam attached so that it floated horizontally when lowered to either 2 or 4 m below the surface. The plastic plate was lowered gently through the flowing water. When being lowered through still or counter current water, it was aligned vertically so as not to disturb medusae in those layers. Using the viewing box, medusae were counted over the piece of white plastic at 2 m and then at 4 m. Ten counts were made at each depth and total counting time at each depth was about 6 min. Since medusae seen when the plate was at 4 m included those seen at 2 m, the mean 2–m observation was subtracted from the mean 4–m observation to obtain an estimate of the number of medusae between 2 and 4 m. 2.5. Statistical analysis StatView software was used for the statistical analysis (SAS Institute, 1992-1998). 3. Results 3.1. Location of medusae at low and high tide The number of medusae visible through the viewing box at stops along the L transect on seven pairs of high and low tides is shown in Fig. 2. Assessments were from a high and low on the same day, or from a high or low in the evening of one day to the high or low in the morning of the next day (2003: September 3/4, 4/5, 24/24, 25/25; 2004: August 27/28, October 12/13, and November 9/10). High tides had a mean (± SEM [Standard Error of the Mean]) of 4.8 ± 0.4 m and low tides a mean of 1.5 ± 0.1 m. At low tides, medusae were in the bay and at stops 12 and 13 in the channel but not at stop 14 (Fig. 2). At high tides medusae were in the bay but virtually absent from the narrow channel east of the bay (Kruskal-Wallis OneWay Analysis of Variance by Ranks [K-W]: H = 34 [df = 5], p < .0001; Mann-Whitney U test [M-W] com-
Fig. 2. The mean number of medusae visible through the viewing box at stops along the L transect (Fig. 1) at high and low tides. The data points are the average (±SEM) of seven successive higher high and lower low tide pairs. Large numbers of medusae were visible in the channel east of the gravel bar during the low but not the high tide.
paring high and low tides: stop 12: U′ = 49, p < .001; stop 13: U′ = 42, p < .001; stop 14: U′ = 31.5, p > .10). The location of medusae across the width of the channel was also observed at lower low tides at transects through stops 12, 13, and 14. At stop 12, medusae were found all across the channel. At stop 13, they were in the centre of the channel but not at viewing points on either side. At the transect through stop 14, they were absent at all five designated viewing points across the channel. Lift net observations (2004: Oct 12, Nov 10); mean low 2.1 m, mean high 4.4 m) were used to confirm the results shown in Fig. 2. Observations were limited to transects through stops 12 and 14 because of the time required to make these observations and because observations at these stops provided the data essential to confirming the visual observations shown in Fig. 2. At low tide, medusae were found along the transect through stop 12 but not at any point along the transect through stop 14 (Table 1; [K-W] H = 21.4 [df = 3], p < .001; [M-W] U′ = 36, p < .005). At high tide, substantial numbers of medusae were not found any of these locations (Table 1). The differences in the numbers of medusae found at stop 12 at low and high tide are significant (U′ = 54, P < .001). These results confirm the observations with the viewing box (Fig. 2). 3.2. Tidal current and the movement of drogues On an ebb tide similar to that used to observe the location of medusae at low tides (Fig. 2; Aug 29/04), two drogues were released near stop 12 in the middle of
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Table 1 Mean number of medusae (±sem) retrieved by lift net near stop 12 at low and high tide Counting stop
Low Tide
High Tide
++
1
0.2 ± 0.0++ N = 9⁎ 0.0 ± 0.0 N=6
31.3 ± 1.4 ° N=6 0.0 ± 0.0° N = 12
3
⁎N = number of lifts of net. Significantly different,++p < .0001; °p < .005.
an ebb tide dropping 3.6 m. A drogue released a few metres to the south of stop 12 drifted along the south shore of the channel, reached the edge of Waddington Channel at 75 min after its release and a point about 200 m northeast of the narrow channel leading into Roscoe Bay at 120 min. A second drogue, released at stop 12 at the same time as the first, followed the set of the current, drifting along the south shore to a point south of stop 13, then toward the north shore, and finally to the south shore at the edge of Waddington Channel. At 105 min after its release, it was retrieved from Waddington Channel at about the same position where the first drogue was retrieved. These results indicate that if medusae leaving the bay stayed in the tidal stream, they would drift well beyond stop 14. 3.3. Observations during an ebb tide At counting stop 8 (Fig. 1), the top 5 m of the water column flowed eastward during the middle of a large ebb tide (drop of 3 m or more). There was a null layer beginning at about 6 m. At the west end of the bay (stop 5; Fig. 1), movement in the water column was erratic and only weakly toward the east throughout the top 5 m of the water column. At stop 12, about 100 m east of the gravel bar, the top 4 to 5 m of the water column flowed eastward. The water column was still or in gentle counter current below the ebb stream. At stop 12, medusae in the ebb stream were buffeted about by the current. Downward swimming was seen most unambiguously by looking at the bottom of the ebb
stream and observing medusae swim from the ebb stream into the still water below. Medusae typically continued swimming down after entering the still or counter current water. These observations were made a few metres south of the center of stop 12 on May 2004. Beginning at 1500 hr and at every 30 min thereafter until 1730 hr, an observer, using the viewing box, counted the number of medusae over a piece of white plastic at 2 m depth and then at 4 m (see Materials and methods). The tide turned to ebb at 1130 hr from a high of 3.2 m and reached a low of 1.6 m at 1800 hr. At 1500 hr, a small number of medusae were at 2 m and above in the water column (Table 2). Substantially more were between 2 and 4 m. While medusae in the 02 m layer were streaming eastward, medusae in the 24 m layer were intermittantly still or in a gentle counter current drifting westward. As the time of the low tide approached (1800 hr), there was a large increase in the number of medusae between 2 and 4 m (Table 2; 2 m and above: [K-W] H = 51, df = 5, p < .0001; 2-4 m, H = 47, df = 5, p < .0001). Comparison between successive time intervals shows that the number of medusae between 2 and 4 m, but not between 0 and 2 m, increased significantly at each observation interval from 1530 hr onward ([M-W] all U's > 14, all p's < .01). Observations were terminated at 1730 hr because the density of medusae in the 2-4 m layer was so great that an estimate of their numbers was no longer possible. Most medusae remained in the counter current or still water for the duration of the ebb tide. The occasional medusae that swam up into the ebb stream were immediately buffeted by the current and usually swam back into the still layer. Medusae in the weak counter currents were typically oriented vertically and were not swimming in the direction of the current. 3.4. Observations during a flood tide During the middle of a large flood tide (rise of 3 m or more) at about 100 m west of the gravel bar (between
Table 2 Mean number of medusae (±SEM) in each of two depth zones above a 36 × 50 cm white plate a few metres south of stop 12 as the time of low tide (1800 hr) approached Depth (m) 0–2⁎ 2–4
Time (hr) 1500
1530
1600
1630
1700
1730
2.5 ± 0.2 14.7 ± 0.5
1.2 ± 0.1 12.0 ± 0.4
2.4 ± 0.1+ 14.7 ± 0.1+
5.2 ± 0.1+ 16.1 ± 0.4+
14.3 ± 0.3++ 29.2 ± 0.8++
8.6 ± 0.1++ 48.4 ± 0.5++
⁎N = 10 medusae counts at each depth and time interval. Significantly different from previous observation period, +p < .01;++p < .001.
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stops 9 and 10), the top 2 m of the water column flowed westward. The water column below that was mostly still. The depth of the moving layer diminished to about 1 m at the middle of the bay (stop 6, Fig. 1). East of the gravel bar, the top 4 to 5 m of the water column moved westward. Below the flood stream, the water column was still or in a gentle eastward counter current. Observations of medusae in the channel during a flood tide were made at stop 12 on 28 August 2004 and on 28 May 2005 as the tide turned from a low of 0.6 m and moved to a high of 4.6 and 4.7 m, respectively. Observations using a viewing box and a rope with plastic ribbon to assess current stratification were made at 10–min intervals. About 30 min before the tide change, water 2 m deep became still that had previously been moving eastward. Within 30 min after the tide turned, the top 3 m of the water column began moving slowly westward. By 75 min following the tide change, the top 4 m of the water column was moving westward and a counter current had formed at 5 m. During the ebb tide, medusae had accumulated in the counter current layer 2 to 4 m deep, as described above. Within 15 min after the tide change, small numbers of medusae began to rise into still water above the 2 m level. Medusae remained at this level as the water began to move slowly toward the bay. The depth of the westward flow increased over the next hour, enveloping more medusae. Within 75 min following the tide change, medusae that had accumulated just east of the gravel bar during the ebb tide had all moved toward the bay, and large numbers of medusae that had accumulated farther east were now drifting past stop 12 in a nonturbulent flow at about 10 m min − 1 . Substantial numbers of medusae continued to move past for an additional 90 min. Similar observations were made at stop 13 the following day. The only difference was that by 1 hr following the tide change, no more medusae were moving past. 3.5. Dissociation of vertical migration in the bay and channel Vertical migrations in the bay and the narrow channel east of the bay were not identical. Medusae in the channel were consistently deep in the water column during the ebb tide and rose in the water column during the flood tide. It has not been possible to identify the conditions associated with vertical migration in the bay except that medusae tended to descend following sunrise and to be at the surface in the evening. Because flood tides tended to occur in the afternoon during the
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late spring, summer, and autumn, medusae in the bay appeared to be rising during the flood tide. However, exceptions regularly occurred. In April, May, June, and September 2004, notes in log books indicated differences in the vertical position of medusae in the water column in the bay and channel on 9 tides over the 15 days an observer was in the bay. 4. Discussion The existence of a dense, resident population of Aurelia labiata in Roscoe Bay appears dependent on both fluid dynamics and the behaviour of medusae. The turbulence of the ebb stream appeared to stimulate medusae to swim down in the water column after drifting over the gravel bar and out of the bay. Downward swimming was seen most unambiguously by observing medusae at the lower boundry of the ebb stream swim into the still water below. Medusae continued to swim downward after entering the still or counter current water. Swimming down in turbulent water may be an escape behaviour stimulated by chaotic movement. Shanks and Graham (1987) have reported that diving can be stimulated by using touch to move medusae (Stomolopus meleagris L Agassiz). Consistent with this line of reasoning, swimming down was sometimes seen on the west side of the gravel bar when the flood stream was turbulent (Albert, unpubl. obs.). Further, the few medusae that swam up from still water into the moving ebb stream were immediately buffeted by the current and usually swam back into the still layer. Most medusae appeared to stay in the still or counter current layer for the duration of the ebb tide. Remaining in the deep still layer would seem to be dependent on the ability to sense turbulence in the water above. The ability to sense moving water is consistent with the observation that Stomolopus meleagris L Agassiz medusae can sense wave direction and orient in relation to wave movement (Shanks and Graham, 1987; Graham et al., 2001). Visual observations rather than haul nets were used to establish the location of medusae in the bay and water column (Fig. 2; Table 1). Visual observations have also been the method of choice in recent studies of large, opaque scyphomedusae by Hamner and Schneider (1986), Shanks and Graham (1987), Hamner et al. (1994), Purcell et al. (2000), and Albert (2005). Because Aurelia are readily visible, visual observations allowed unobtrusive assessment of where medusae were located and the direction in which they were moving. In the present study, visual observations (Fig.
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2) were validated with lift-net observations (Table 1). Because of the effect of visual perspective (i.e., when looking deeper in the water column, medusae appear smaller and the area surveyed is larger), numbers obtained with the viewing box cannot be directly converted to number of medusae m− 2. Lift net data indicate densities of about 80 m− 2 around the time of a low tide east of the gravel bar at counting stop 12 (Table 1). Visual observations of medusae accumulating above a plastic plate indicate densities of 250 m− 2 near the time of the low tide a few metres south of counting stop 12 as medusae densities reached their maximum (Table 2). The observations of medusae above a plastic plate will not be enhanced by visual perspective. Medusae densities obtained with these two procedures represent the high end of the range of medusae densities in Roscoe Bay during the present observation period. Two features of stratified fluid flow appear significant in vertical migration by medusae. Fluid flow over a barrier created a counter current below the ebb stream that moved medusae back toward the gravel bar during the ebb tide. In addition, the bottom layers of the ebb stream should follow the contour of the gravel bar downward on the lee side (Baines, 1995; Farmer and Armi, 1999; Afanasyev and Peltier, 2001; Armi and Farmer, 2002). Accordingly, current flow may have carried large numbers of medusae down in the water column and positioned them close to still and counter current layers below the ebb stream. The water columns in Roscoe Bay, the narrow channel east of the bay, and Waddington Channel were stratified by temperature and salinity (frequently 23 [0.1 m] to 28 [10 m] parts per thousand (ppt) but sometimes 18 to 28 ppt) throughout the year except winter (Ricker, 1989; Albert, 2005; Albert, unpubl. obs.). The present results are the first to demonstrate that vertical migration is a mechanism enabling scyphomedusae to remain in a location subjected to tidal currents. The most closely related previous observations were made in the Wadden Sea. Kopacz (1994) observed that some ctenophores (Pleurobrachia pileus) and hydrozoans (e.g., Rathkea octopunctata; Eucheilota maculata) were high in the water column at high tide and low in the water column at low tide in a part of the Wadden Sea exposed to current flow. In a shallow area (location unspecified), Kopacz (1994) found only that the zooplankton were present at high tide and absent at low tide. Unfortunately, the vertical pattern of currents in the water column, the existence of counter currents, and the distribution of currents in different parts of the bay were not assessed. Accordingly, there is no basis for understanding how the overall distribution of zooplank-
ton in the Wadden Sea is affected by tidal currents. In addition, the population of gelatinous zooplankton was not stable. Hence, there is no basis for concluding that these zooplankton avoided tidal dispersion. Finally, there is no evidence that Aurelia would move in the same way as these ctenophores and hydrozoans. To the contrary, Van der Veer and Oorthuysen (1985), specifically comment that the “movement of Aurelia aurita from the inner parts of the Wadden Sea towards the North Sea is the opposite of that observed in another coelenterate, the ctenophore Pleurobrachia pilus …” (p. 41). It may seem paradoxical that in Roscoe Bay medusae swam down and out of the ebb stream leaving the bay but remained in the flood stream to drift back into the bay. However, medusae were in a non-turbulent flow as they drifted away from the bay toward the gravel bar on the ebb tide and as they drifted toward the bay on the flood tide. Major turbulence only occurred in water that had passed over the gravel bar and into the narrow channel east of the bay. Medusae regularly swam down only in that turbulent water. Consistent with the reasoning that vertical migration protects Roscoe Bay's population of A. labiata from tidal dispersion, the population of A. labiata has been relatively stable over the last two years (Fig. 4 in Albert, 2005). However, two new generations of juvenile medusae, each comprising about 30% of the adult population, have been produced during this interval (Albert, 2005) and no major mortality incidents have been observed (Albert, 2005). Accordingly, medusae are being lost to the bay, but there is no basis for speculating on how much of the loss is due to leakage out of the bay and how much to predation and mortality. Three different behaviours have now been demonstrated to participate in maintaining dense aggregations of A. labiata: vertical migration, horizontal migration (Hamner et al., 1994), and current guided swimming (convection currents: Toyokawa et al., 1997; Purcell et al., 2000; Strand and Hamner, Theodosia Inlet, Canada, pers. comm.). While knowledge of these behaviours is limited, each appears to be independent of tidal entrainment. Each requires an active and persistent behaviour. The behaviour in each situation is capable of adjustments as it unfolds as opposed to being independent of stimulus control once it is initiated. Horizontal migration has the interesting characteristic of being terminated by arriving at a particular location even though the stimulus activating the behaviour (sunlight) is still present. An understanding of the sensory capabilities of medusae that allow them to display these behaviours is incomplete. It may be significant
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that all of these observations have been on species of Aurelia in the Pacific Ocean. The ability of A. labiata to form and to remain in dense aggregations appears to be an important adaptation. Reproductive success is facilitated by having males and females in close proximity to one another (Hamner et al., 1994). Also, as Purcell et al. (2000) have pointed out, the presence of dense aggregations may indicate that this is an area where planulae and juvenile medusae have a relatively high survival rate. Not all medusae appear to emit the behaviours required to remain in the bay. Cyanea capillata, which prey on A. labiata (Hansson, 1997; Purcell et al., 2000), did not appear to be successful in staying in Roscoe Bay. One or two C. capillata appeared in the bay intermittantly but did not remain for more than a few days or a few weeks (Albert, unpubl. obs.). Aequorea victoria medusae also did not appear to be successful in staying in the bay. There were no dense aggregations of A. victoria and these medusae were frequently visible at counting stop 14 (Fig. 1) and further east where A. labiata were almost never seen. To summarise, A. labiata in Roscoe Bay appear to depend on vertical migration to avoid tidal dispersion. Medusae that drift over a gravel bar and out of the bay on ebb tides escape the ebb flow by descending several meters and entering still or counter current water. Medusae in the counter current below the ebb stream actually drift back toward the bay during the ebb tide. Medusae rise in the water column as the ebb abates, are caught up in the deepening flood flow, and are swept back into the bay. Vertical migration appears to enhance survival by keeping medusae in an environment that facilitates reproduction, decreases loss due to predation, and increases the survival of juveniles. Acknowledgements I am indebted to Dr. R. de Wreede (University of British Columbia), Chad Widmer (Monterey Bay Aquarium), and two annoymous reviewers for helpful suggestions and encouragement. References Afanasyev, Y.D., Peltier, W.R., 2001. On breaking internal waves over the sill in Knight Inlet. Proc. R. Soc. Lond., A 457, 2799–2825. Albert, D.J., 2005. Reproduction and longevity of Aurelia labiata in Roscoe Bay, a small bay on the Pacific Coast of Canada. J. Mar. Biol. Assoc. UK 85, 575–581. Arai, M.N., 1992. Attraction of Aurelia and Aequorea to prey. Hydrobiologia 216/217, 363–366.
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Arai, M.N., 1997. A Functional Biology of Scyphozoa. Chapman and Hall, London. Armi, L., Farmer, D., 2002. Stratified flow over topography: bifurcation fronts and transition to the uncontrolled state. Proc. R. Soc. Lond., A 458, 513–538. Baines, P.G., 1995. Topographic Effects in Stratified Flows. Cambridge University Press, Cambridge. Canadian Hydrographic Service, 2005. Canadian Tide and Current Tables. Juan de Fuca Strait and Strait of Georgia. Fisheries and Oceans Canada, Ottawa, Canada. Farmer, D., Armi, L., 1999. Stratified flow over topography: the role of small-scale entrainment and mixing in flow establishment. Proc. R. Soc. Lond., A 455, 3221–3258. Graham, W.M., Pages, F., Hamner, W.M., 2001. A physical context for gelatinous zooplankton aggregations: a review. Hydrobiologia 451, 199–212. Hamner, W.M., Schneider, D., 1986. Regularly spaced rows of medusae in the Bering Sea: Role of Langmuir circulation. Limnol. Oceanogr. 31, 171–177. Hamner, W.M., Hamner, P.P., Strand, S.W., 1994. Sun-compass migration of Aurelia aurita (Scyphozoa): population retention and reproduction in Saanich Inlet, British Columbia. Mar. Biol. 119, 347–356. Hansson, L.J., 1997. Capture and digestion of the scyphozoan jellyfish Aurelia aurita by Cyanea capillata and prey response to predator contact. J. Plankton Res. 19, 195–208. Kopacz, U., 1994. Evidence for tidally-induced vertical migration of some gelatinous zooplankton in the Wadden Sea area near Sylt. Helgol. Meeresunters. 48, 333–342. Lucas, C.H., 2001. Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia 451, 229–245. Purcell, J.E., 2003. Predation on zooplankton by large jellyfish, Aurelia labiata, Cyanea capillata and Aequorea aequorea, in Prince William Sound, Alaska. Mar. Ecol., Prog. Ser. 246, 137–152. Purcell, J.E., Arai, M.N., 2001. Interactions of pelagic cnidarians and ctenophores with fish: a review. Hyrobiologia 451, 27–44. Purcell, J.E., Brown, E.D., Stokesbury, K.D.E., Haldorson, L.H., Shirley, T.C., 2000. Aggregations of the jellyfish Aurelia labiata: abundance, distribution, association with age–0 walleye pollock, and behaviors promoting aggregation in Prince William Sound, Alaska, USA. Mar. Ecol., Prog. Ser. 195, 145–158. Ricker, K.E., 1989. Biophysical suitability of the Sunshine Coast and Johnstone Strait/Desolation Sound area for salmonid farming in net cages. Main Report. Ministry of Agriculture and Fisheries, Aquaculture and Commercial Fisheries Branch, Province of British Columbia, Canada. Shanks, A.E., Graham, W.M., 1987. Orientated swimming in the jellyfish Stomolopus meleagris L. Agassiz (Scyphozoan: Rhizostomida). J. Exp. Mar. Biol. Ecol. 108, 159–169. Sullivan, B.K., Garcia, J.R., Klein-MacPhee, G., 1994. Prey selection by the scyphomedusan predator Aurelia aurita. Mar. Biol. 121, 335–341. Toyokawa, M., Inagaki, T., Terazaki, M., 1997. Distribution of Aurelia aurita (Linnaeus, 1758) in Tokyo Bay; observations with echosounder and plankton net. Proc 6th International Conference on Coelenterate Biology, 1995. Natuurhistorisch Museum, Leiden, pp. 483–490. Van der Veer, H.W., Oorthuysen, W., 1985. Abundance, growth and food demand of the scyphomedusa Aurelia aurita in the western Wadden Sea. Neth. J. Sea Res. 19, 38–44.
Aurelia labiata medusae (Scyphozoa) in Roscoe Bay avoid tidal dispersion by vertical migration David J. Albert Roscoe Bay Marine Laboratory, 4534 W 3rd Avenue, Vancouver, B.C., Canada V6R 1N2 Received 10 January 2006; accepted 14 November 2006 Available online 17 November 2006
Abstract Aurelia labiata reside year around in Roscoe Bay on the west coast of Canada in spite of tides that exchange as much as 10% to 30% of the bay's water twice daily. Large numbers of medusae drift eastward over a gravel bar and out of the bay on ebb tides, only to return on flood tides. Drogues released into the tidal stream at the middle of an ebb tide drifted about 700 m out of the bay and into an adjacent large body of water. With the aid of a viewing box and lift net it was observed that after drifting out of the bay on an ebb tide, medusae remained within 300 m of the bay because they swam into still or counter current water below the turbulent ebb stream. When the tide turned to flood, medusae rose into the still water, became embedded in the nonturbulent flood stream, and drifted back into the bay. Vertical migration appears to enable the dense population of medusae to stay in a single location. This enhances reproductive success by keeping males and females in close proximity and increases survival by keeping the population in a favourable location. © 2006 Elsevier B.V. All rights reserved. Keywords: Northeast Pacific; Zooplankton; Coelenterates; Scyphomedusae; Aurelia labiata
1. Introduction Dense aggregations of Aurelia aurita and Aurelia labiata, commonly known as Moon Jellies, are found in bays and inlets, as well as open coastal oceans (for reviews see Arai, 1997; Lucas, 2001). These aggregations have substantial adaptive significance. The close proximity of males and females facilitates reproduction (Hamner et al., 1994). Dense aggregations also make predation by gelatinous predators more difficult (Purcell et al., 2000). Phacellophora camtschatica and Cyanea capillata scyphomedusae are able to prey upon A. labiata along the fringes, but not within, dense aggregations (Purcell et al., 2000). Finally, medusae may be E-mail address: [email protected]. 1385-1101/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2006.11.002
attracted to and congregate in habitat that contains food resources (Arai, 1992) and is suitable for the survival of planulae and juvenile medusae (Sullivan et al., 1994; Purcell et al., 2000). If dense aggregations of medusae stay in such habitat, the survival of planulae and juvenile medusae should be enhanced (Purcell, 2003). Dense aggregations of medusae are ecologically significant. Aurelia are known to consume fish larvae (for reviews, see Purcell and Arai, 2001; Purcell, 2003). Purcell (2003) has calculated that consumption by individual medusae may be in the 100s or 1000s daily. Large aggregations may impact reproduction of fish species and may also reduce the availability of food for other species. Increasing attention is being directed to understanding how dense aggregations of Aurelia labiata stay in
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one place rather than being dispersed by tides and currents. Hamner et al. (1994) have shown that A. aurita (more likely A. labiata) in Saanich Inlet accumulate and remain in dense aggregations along the southern and eastern shores of the inlet by using sunlight-stimulated horizontal migration. Dense elliptical aggregations in Tokyo Bay (Toyokawa et al., 1997) and Prince William Sound, Alaska (Purcell et al., 2000), appear to persist because medusae swim in directions aligned with the currents of convection cells in the water column. Roscoe Bay, a small bay on the Pacific Coast of Canada, has a dense resident population of A. labiata medusae (Fig. 1; Albert, 2005) that has remained relatively constant in size over the last two years in spite of tidal flushing that on average exchanges more than one-quarter of the bay's water twice daily (Canadian Hydrographic Service, 2005). Casual observations indicated that directional swimming was rare and there was no evidence of swimming guided by convection cells. The present report attempts to elucidate the mechanism by which A. labiata are able to remain in Roscoe Bay. It begins by providing evidence that many medusae actually are unable to resist the tidal flow and are swept out of the bay on ebb tides. A series of observations will indicate that medusae drifting out of the bay on ebb tides entered still and counter current layers of water beneath the ebb stream. These medusae subsequently rose into still water at the end of the ebb tide, became embedded in the flood stream, and returned to the bay.
2. Materials and methods 2.1. Establishing the location of medusae The location of medusae in the bay and narrow channel east of the gravel bar was assesssed by counting the number of medusae visible through a viewing box at 14 stops along the length of the bay and down the middle of the narrow channel east of the bay (Fig. 1, L transect). Counts along transects across counting stops 12, 13, and 14, established more precisely where medusae were in the channel outside of the bay (Fig. 1). There were three viewing points along transects across counting stops 12 and 13, and five viewing points along the transect across stop 14. Counting took 60 to 80 min. Counting usually, but not always, started in the west end of the bay. Counting direction did not alter the pattern of results obtained. The floating viewing box had a Plexiglas bottom (117 cm × 56 cm) and wood sides 46 cm high. To minimise reflections, the box was painted black on the inside and covered with a black cloth. When moving from one stop to another, we put styrofoam pontoons under each side so that the viewing box could be pulled briskly with a small rowboat (2.1 m long). Medusae were counted rapidly at each stop to minimise the influence of those entering or leaving the visual field. To increase assessment stability, the count entered for each stop was the average of several counts, with the viewing box moved slightly between counts. Medusae were counted in the morning or evening, or both. 2.2. Lift net assessment of the number of medusae in the channel A conical lift net (0.70 m dia.; 0.75 m deep, 4 × 4 mm mesh) was used to supplement and confirm visual observations of medusae at transects 1 and 3 in the narrow channel east of the bay. The lift net was lowered to the ocean floor, left for 4 min, and then slowly raised to the surface. Medusae were counted in the net, or in small groups as they were spilled from the net.
Fig. 1. A chart of Roscoe Bay ([124° 46′ W; 50° 09′ 36″ N] modified from Canadian Hydrographic Service Chart 3538 [1996]). The L transect down the centre of the bay had 14 stops (marked by bars) where medusae were counted. Vertical lines through stops 12, 13, and 14, mark the transects across these stops used to assess the position of medusae across the width of the channel. The gravel bar (G) dries at lower low water. North is at the top. The vertical line just east of Marylebone Pt is 124° 45′ W. A large deep water channel (Waddington Channel; 1800 m wide) is east of Marylebone Point. Depth contours in the bay and immediately east of the gravel bar are at 5 m intervals at lower low water (LLW).
2.3. Current flow and stratification Drogues were used to evaluate how far ebb currents might carry medusae out of the bay if medusae remained in the ebb stream. Each drogue was constructed of two plastic buckets (0.30 m high; 0.25 m dia) hung one above the other, 1.3 m apart. Each bucket had four plastic vanes (0.30 × 0.36 m) bolted vertically to the sides, 90 degrees apart. A float at the surface and a 2 kg
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weight at the bottom kept the drogue vertical in the water. Since medusae were within 1 to 3 m of the surface as they drifted eastward over the gravel bar, the drogues were set to span the distance from 0.5 to 2.5 m. Current stratification was assessed using a rope with plastic surveyor's flagging (25 mm wide and 1 m long) at 1 m intervals and a 4 kg weight at the bottom. The orientation of the flagging indicated the direction of current flow. 2.4. Accumulation of medusae east of the gravel bar A 36 × 50 × 0.6 cm thick piece of white plastic had pieces of styrofoam attached so that it floated horizontally when lowered to either 2 or 4 m below the surface. The plastic plate was lowered gently through the flowing water. When being lowered through still or counter current water, it was aligned vertically so as not to disturb medusae in those layers. Using the viewing box, medusae were counted over the piece of white plastic at 2 m and then at 4 m. Ten counts were made at each depth and total counting time at each depth was about 6 min. Since medusae seen when the plate was at 4 m included those seen at 2 m, the mean 2–m observation was subtracted from the mean 4–m observation to obtain an estimate of the number of medusae between 2 and 4 m. 2.5. Statistical analysis StatView software was used for the statistical analysis (SAS Institute, 1992-1998). 3. Results 3.1. Location of medusae at low and high tide The number of medusae visible through the viewing box at stops along the L transect on seven pairs of high and low tides is shown in Fig. 2. Assessments were from a high and low on the same day, or from a high or low in the evening of one day to the high or low in the morning of the next day (2003: September 3/4, 4/5, 24/24, 25/25; 2004: August 27/28, October 12/13, and November 9/10). High tides had a mean (± SEM [Standard Error of the Mean]) of 4.8 ± 0.4 m and low tides a mean of 1.5 ± 0.1 m. At low tides, medusae were in the bay and at stops 12 and 13 in the channel but not at stop 14 (Fig. 2). At high tides medusae were in the bay but virtually absent from the narrow channel east of the bay (Kruskal-Wallis OneWay Analysis of Variance by Ranks [K-W]: H = 34 [df = 5], p < .0001; Mann-Whitney U test [M-W] com-
Fig. 2. The mean number of medusae visible through the viewing box at stops along the L transect (Fig. 1) at high and low tides. The data points are the average (±SEM) of seven successive higher high and lower low tide pairs. Large numbers of medusae were visible in the channel east of the gravel bar during the low but not the high tide.
paring high and low tides: stop 12: U′ = 49, p < .001; stop 13: U′ = 42, p < .001; stop 14: U′ = 31.5, p > .10). The location of medusae across the width of the channel was also observed at lower low tides at transects through stops 12, 13, and 14. At stop 12, medusae were found all across the channel. At stop 13, they were in the centre of the channel but not at viewing points on either side. At the transect through stop 14, they were absent at all five designated viewing points across the channel. Lift net observations (2004: Oct 12, Nov 10); mean low 2.1 m, mean high 4.4 m) were used to confirm the results shown in Fig. 2. Observations were limited to transects through stops 12 and 14 because of the time required to make these observations and because observations at these stops provided the data essential to confirming the visual observations shown in Fig. 2. At low tide, medusae were found along the transect through stop 12 but not at any point along the transect through stop 14 (Table 1; [K-W] H = 21.4 [df = 3], p < .001; [M-W] U′ = 36, p < .005). At high tide, substantial numbers of medusae were not found any of these locations (Table 1). The differences in the numbers of medusae found at stop 12 at low and high tide are significant (U′ = 54, P < .001). These results confirm the observations with the viewing box (Fig. 2). 3.2. Tidal current and the movement of drogues On an ebb tide similar to that used to observe the location of medusae at low tides (Fig. 2; Aug 29/04), two drogues were released near stop 12 in the middle of
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Table 1 Mean number of medusae (±sem) retrieved by lift net near stop 12 at low and high tide Counting stop
Low Tide
High Tide
++
1
0.2 ± 0.0++ N = 9⁎ 0.0 ± 0.0 N=6
31.3 ± 1.4 ° N=6 0.0 ± 0.0° N = 12
3
⁎N = number of lifts of net. Significantly different,++p < .0001; °p < .005.
an ebb tide dropping 3.6 m. A drogue released a few metres to the south of stop 12 drifted along the south shore of the channel, reached the edge of Waddington Channel at 75 min after its release and a point about 200 m northeast of the narrow channel leading into Roscoe Bay at 120 min. A second drogue, released at stop 12 at the same time as the first, followed the set of the current, drifting along the south shore to a point south of stop 13, then toward the north shore, and finally to the south shore at the edge of Waddington Channel. At 105 min after its release, it was retrieved from Waddington Channel at about the same position where the first drogue was retrieved. These results indicate that if medusae leaving the bay stayed in the tidal stream, they would drift well beyond stop 14. 3.3. Observations during an ebb tide At counting stop 8 (Fig. 1), the top 5 m of the water column flowed eastward during the middle of a large ebb tide (drop of 3 m or more). There was a null layer beginning at about 6 m. At the west end of the bay (stop 5; Fig. 1), movement in the water column was erratic and only weakly toward the east throughout the top 5 m of the water column. At stop 12, about 100 m east of the gravel bar, the top 4 to 5 m of the water column flowed eastward. The water column was still or in gentle counter current below the ebb stream. At stop 12, medusae in the ebb stream were buffeted about by the current. Downward swimming was seen most unambiguously by looking at the bottom of the ebb
stream and observing medusae swim from the ebb stream into the still water below. Medusae typically continued swimming down after entering the still or counter current water. These observations were made a few metres south of the center of stop 12 on May 2004. Beginning at 1500 hr and at every 30 min thereafter until 1730 hr, an observer, using the viewing box, counted the number of medusae over a piece of white plastic at 2 m depth and then at 4 m (see Materials and methods). The tide turned to ebb at 1130 hr from a high of 3.2 m and reached a low of 1.6 m at 1800 hr. At 1500 hr, a small number of medusae were at 2 m and above in the water column (Table 2). Substantially more were between 2 and 4 m. While medusae in the 02 m layer were streaming eastward, medusae in the 24 m layer were intermittantly still or in a gentle counter current drifting westward. As the time of the low tide approached (1800 hr), there was a large increase in the number of medusae between 2 and 4 m (Table 2; 2 m and above: [K-W] H = 51, df = 5, p < .0001; 2-4 m, H = 47, df = 5, p < .0001). Comparison between successive time intervals shows that the number of medusae between 2 and 4 m, but not between 0 and 2 m, increased significantly at each observation interval from 1530 hr onward ([M-W] all U's > 14, all p's < .01). Observations were terminated at 1730 hr because the density of medusae in the 2-4 m layer was so great that an estimate of their numbers was no longer possible. Most medusae remained in the counter current or still water for the duration of the ebb tide. The occasional medusae that swam up into the ebb stream were immediately buffeted by the current and usually swam back into the still layer. Medusae in the weak counter currents were typically oriented vertically and were not swimming in the direction of the current. 3.4. Observations during a flood tide During the middle of a large flood tide (rise of 3 m or more) at about 100 m west of the gravel bar (between
Table 2 Mean number of medusae (±SEM) in each of two depth zones above a 36 × 50 cm white plate a few metres south of stop 12 as the time of low tide (1800 hr) approached Depth (m) 0–2⁎ 2–4
Time (hr) 1500
1530
1600
1630
1700
1730
2.5 ± 0.2 14.7 ± 0.5
1.2 ± 0.1 12.0 ± 0.4
2.4 ± 0.1+ 14.7 ± 0.1+
5.2 ± 0.1+ 16.1 ± 0.4+
14.3 ± 0.3++ 29.2 ± 0.8++
8.6 ± 0.1++ 48.4 ± 0.5++
⁎N = 10 medusae counts at each depth and time interval. Significantly different from previous observation period, +p < .01;++p < .001.
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stops 9 and 10), the top 2 m of the water column flowed westward. The water column below that was mostly still. The depth of the moving layer diminished to about 1 m at the middle of the bay (stop 6, Fig. 1). East of the gravel bar, the top 4 to 5 m of the water column moved westward. Below the flood stream, the water column was still or in a gentle eastward counter current. Observations of medusae in the channel during a flood tide were made at stop 12 on 28 August 2004 and on 28 May 2005 as the tide turned from a low of 0.6 m and moved to a high of 4.6 and 4.7 m, respectively. Observations using a viewing box and a rope with plastic ribbon to assess current stratification were made at 10–min intervals. About 30 min before the tide change, water 2 m deep became still that had previously been moving eastward. Within 30 min after the tide turned, the top 3 m of the water column began moving slowly westward. By 75 min following the tide change, the top 4 m of the water column was moving westward and a counter current had formed at 5 m. During the ebb tide, medusae had accumulated in the counter current layer 2 to 4 m deep, as described above. Within 15 min after the tide change, small numbers of medusae began to rise into still water above the 2 m level. Medusae remained at this level as the water began to move slowly toward the bay. The depth of the westward flow increased over the next hour, enveloping more medusae. Within 75 min following the tide change, medusae that had accumulated just east of the gravel bar during the ebb tide had all moved toward the bay, and large numbers of medusae that had accumulated farther east were now drifting past stop 12 in a nonturbulent flow at about 10 m min − 1 . Substantial numbers of medusae continued to move past for an additional 90 min. Similar observations were made at stop 13 the following day. The only difference was that by 1 hr following the tide change, no more medusae were moving past. 3.5. Dissociation of vertical migration in the bay and channel Vertical migrations in the bay and the narrow channel east of the bay were not identical. Medusae in the channel were consistently deep in the water column during the ebb tide and rose in the water column during the flood tide. It has not been possible to identify the conditions associated with vertical migration in the bay except that medusae tended to descend following sunrise and to be at the surface in the evening. Because flood tides tended to occur in the afternoon during the
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late spring, summer, and autumn, medusae in the bay appeared to be rising during the flood tide. However, exceptions regularly occurred. In April, May, June, and September 2004, notes in log books indicated differences in the vertical position of medusae in the water column in the bay and channel on 9 tides over the 15 days an observer was in the bay. 4. Discussion The existence of a dense, resident population of Aurelia labiata in Roscoe Bay appears dependent on both fluid dynamics and the behaviour of medusae. The turbulence of the ebb stream appeared to stimulate medusae to swim down in the water column after drifting over the gravel bar and out of the bay. Downward swimming was seen most unambiguously by observing medusae at the lower boundry of the ebb stream swim into the still water below. Medusae continued to swim downward after entering the still or counter current water. Swimming down in turbulent water may be an escape behaviour stimulated by chaotic movement. Shanks and Graham (1987) have reported that diving can be stimulated by using touch to move medusae (Stomolopus meleagris L Agassiz). Consistent with this line of reasoning, swimming down was sometimes seen on the west side of the gravel bar when the flood stream was turbulent (Albert, unpubl. obs.). Further, the few medusae that swam up from still water into the moving ebb stream were immediately buffeted by the current and usually swam back into the still layer. Most medusae appeared to stay in the still or counter current layer for the duration of the ebb tide. Remaining in the deep still layer would seem to be dependent on the ability to sense turbulence in the water above. The ability to sense moving water is consistent with the observation that Stomolopus meleagris L Agassiz medusae can sense wave direction and orient in relation to wave movement (Shanks and Graham, 1987; Graham et al., 2001). Visual observations rather than haul nets were used to establish the location of medusae in the bay and water column (Fig. 2; Table 1). Visual observations have also been the method of choice in recent studies of large, opaque scyphomedusae by Hamner and Schneider (1986), Shanks and Graham (1987), Hamner et al. (1994), Purcell et al. (2000), and Albert (2005). Because Aurelia are readily visible, visual observations allowed unobtrusive assessment of where medusae were located and the direction in which they were moving. In the present study, visual observations (Fig.
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2) were validated with lift-net observations (Table 1). Because of the effect of visual perspective (i.e., when looking deeper in the water column, medusae appear smaller and the area surveyed is larger), numbers obtained with the viewing box cannot be directly converted to number of medusae m− 2. Lift net data indicate densities of about 80 m− 2 around the time of a low tide east of the gravel bar at counting stop 12 (Table 1). Visual observations of medusae accumulating above a plastic plate indicate densities of 250 m− 2 near the time of the low tide a few metres south of counting stop 12 as medusae densities reached their maximum (Table 2). The observations of medusae above a plastic plate will not be enhanced by visual perspective. Medusae densities obtained with these two procedures represent the high end of the range of medusae densities in Roscoe Bay during the present observation period. Two features of stratified fluid flow appear significant in vertical migration by medusae. Fluid flow over a barrier created a counter current below the ebb stream that moved medusae back toward the gravel bar during the ebb tide. In addition, the bottom layers of the ebb stream should follow the contour of the gravel bar downward on the lee side (Baines, 1995; Farmer and Armi, 1999; Afanasyev and Peltier, 2001; Armi and Farmer, 2002). Accordingly, current flow may have carried large numbers of medusae down in the water column and positioned them close to still and counter current layers below the ebb stream. The water columns in Roscoe Bay, the narrow channel east of the bay, and Waddington Channel were stratified by temperature and salinity (frequently 23 [0.1 m] to 28 [10 m] parts per thousand (ppt) but sometimes 18 to 28 ppt) throughout the year except winter (Ricker, 1989; Albert, 2005; Albert, unpubl. obs.). The present results are the first to demonstrate that vertical migration is a mechanism enabling scyphomedusae to remain in a location subjected to tidal currents. The most closely related previous observations were made in the Wadden Sea. Kopacz (1994) observed that some ctenophores (Pleurobrachia pileus) and hydrozoans (e.g., Rathkea octopunctata; Eucheilota maculata) were high in the water column at high tide and low in the water column at low tide in a part of the Wadden Sea exposed to current flow. In a shallow area (location unspecified), Kopacz (1994) found only that the zooplankton were present at high tide and absent at low tide. Unfortunately, the vertical pattern of currents in the water column, the existence of counter currents, and the distribution of currents in different parts of the bay were not assessed. Accordingly, there is no basis for understanding how the overall distribution of zooplank-
ton in the Wadden Sea is affected by tidal currents. In addition, the population of gelatinous zooplankton was not stable. Hence, there is no basis for concluding that these zooplankton avoided tidal dispersion. Finally, there is no evidence that Aurelia would move in the same way as these ctenophores and hydrozoans. To the contrary, Van der Veer and Oorthuysen (1985), specifically comment that the “movement of Aurelia aurita from the inner parts of the Wadden Sea towards the North Sea is the opposite of that observed in another coelenterate, the ctenophore Pleurobrachia pilus …” (p. 41). It may seem paradoxical that in Roscoe Bay medusae swam down and out of the ebb stream leaving the bay but remained in the flood stream to drift back into the bay. However, medusae were in a non-turbulent flow as they drifted away from the bay toward the gravel bar on the ebb tide and as they drifted toward the bay on the flood tide. Major turbulence only occurred in water that had passed over the gravel bar and into the narrow channel east of the bay. Medusae regularly swam down only in that turbulent water. Consistent with the reasoning that vertical migration protects Roscoe Bay's population of A. labiata from tidal dispersion, the population of A. labiata has been relatively stable over the last two years (Fig. 4 in Albert, 2005). However, two new generations of juvenile medusae, each comprising about 30% of the adult population, have been produced during this interval (Albert, 2005) and no major mortality incidents have been observed (Albert, 2005). Accordingly, medusae are being lost to the bay, but there is no basis for speculating on how much of the loss is due to leakage out of the bay and how much to predation and mortality. Three different behaviours have now been demonstrated to participate in maintaining dense aggregations of A. labiata: vertical migration, horizontal migration (Hamner et al., 1994), and current guided swimming (convection currents: Toyokawa et al., 1997; Purcell et al., 2000; Strand and Hamner, Theodosia Inlet, Canada, pers. comm.). While knowledge of these behaviours is limited, each appears to be independent of tidal entrainment. Each requires an active and persistent behaviour. The behaviour in each situation is capable of adjustments as it unfolds as opposed to being independent of stimulus control once it is initiated. Horizontal migration has the interesting characteristic of being terminated by arriving at a particular location even though the stimulus activating the behaviour (sunlight) is still present. An understanding of the sensory capabilities of medusae that allow them to display these behaviours is incomplete. It may be significant
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that all of these observations have been on species of Aurelia in the Pacific Ocean. The ability of A. labiata to form and to remain in dense aggregations appears to be an important adaptation. Reproductive success is facilitated by having males and females in close proximity to one another (Hamner et al., 1994). Also, as Purcell et al. (2000) have pointed out, the presence of dense aggregations may indicate that this is an area where planulae and juvenile medusae have a relatively high survival rate. Not all medusae appear to emit the behaviours required to remain in the bay. Cyanea capillata, which prey on A. labiata (Hansson, 1997; Purcell et al., 2000), did not appear to be successful in staying in Roscoe Bay. One or two C. capillata appeared in the bay intermittantly but did not remain for more than a few days or a few weeks (Albert, unpubl. obs.). Aequorea victoria medusae also did not appear to be successful in staying in the bay. There were no dense aggregations of A. victoria and these medusae were frequently visible at counting stop 14 (Fig. 1) and further east where A. labiata were almost never seen. To summarise, A. labiata in Roscoe Bay appear to depend on vertical migration to avoid tidal dispersion. Medusae that drift over a gravel bar and out of the bay on ebb tides escape the ebb flow by descending several meters and entering still or counter current water. Medusae in the counter current below the ebb stream actually drift back toward the bay during the ebb tide. Medusae rise in the water column as the ebb abates, are caught up in the deepening flood flow, and are swept back into the bay. Vertical migration appears to enhance survival by keeping medusae in an environment that facilitates reproduction, decreases loss due to predation, and increases the survival of juveniles. Acknowledgements I am indebted to Dr. R. de Wreede (University of British Columbia), Chad Widmer (Monterey Bay Aquarium), and two annoymous reviewers for helpful suggestions and encouragement. References Afanasyev, Y.D., Peltier, W.R., 2001. On breaking internal waves over the sill in Knight Inlet. Proc. R. Soc. Lond., A 457, 2799–2825. Albert, D.J., 2005. Reproduction and longevity of Aurelia labiata in Roscoe Bay, a small bay on the Pacific Coast of Canada. J. Mar. Biol. Assoc. UK 85, 575–581. Arai, M.N., 1992. Attraction of Aurelia and Aequorea to prey. Hydrobiologia 216/217, 363–366.
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