Diel Vertical Movements and Feeding Activity of Zooplankton in St ...

Movements and Feeding Activity of Zoop in St. Georges Bay, N.S., Using Net Tows and a oped Passive Trap G . C. Harding, W. P. Vass, and B. T. Hargrave Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by 174.118.149.253 on 12/04/14 For personal use only.

Department of Fisheries and Oceans, Marine Ecology Laboratory, Bedford institute of Oceanography, P.O. Box 1006, Dartmouth, N.S. B2Y 4A2

and S. Pearre, Jr. Department of Ocednography, Dalhousie Clniversity, Halifax, N.5. B3H 3M2

Harding, G. C., W. P* Vass, 5. T. Hargrave, and 5. Pearre, jr. 1986. Diel vertical movements and feeding activity of zooplankton in St. Georges Bay, N.S., using net tows and a newly developed passive trap. Can. ). Fish. Aquat. Sci. 43: 952-967. Newly developed plankton traps, designed to passively collect vertically mobile plankters, sampled ascending plankton but failed to collect many species during descent. This discrepancy may be behavioral with passively sinking organisms reacting to the trap surface with an upward avoidance reaction. Simultaneous use of conventional net tows and semiautomatedtraps allowed us to interpret the vertical movements sf plankton more fully than by either method alone. Asynchronous vertical movement of the Pseudocabanus population is suspected because the percentage of trapped animals with food in their guts was usually higher in the downward moving fraction of the population. Migratory behaviors ranged from dusk and dawn ascent with midnight sinking to reverse migrations where the night level inhabited is deeper than the day depth. Noctural dispersal of herbivore and omnivore populations over depth probably reflects predator avoidance by presenting less dense aggregations to vertically mobile predators. Sightless predators reside in deeper waters than their prey during daylight presumably because they are larger and more vulnerable themselves to visual predation. Visual predators descend to greater depths than their prey at night. ,411 the migration patterns observed can be explained in evolutionary terms simply by competition for food and avoidance of predators. Les pieges 21 plancton rkcemment mis au point, consus pour recueillir passivement les organismes planctoniques a mobilite verticale, ont perrnis de prdever des echantillons de plancton ascendant, mais n'ont pas permis de recueillir nombres dlesp&ces durant la descente. Cette divergence pourrait Gtre de nature comportementale, les organismes L3 descente passive reagissant a la surface du piitge par un mouvement d'evitement vers [e haut. b'utilisation simultanee de filets conventionnels et de pieges semi-automatiques nous a permis d'interprkter les deplacements verticaux du plancton de f a ~ o nplus complete que par I'une ou I'autre methode seule. On presume que Be dkplacement vertical de la population de Pseudocalanus est asynchrone, car le pourcentage des animaux pris avec des aliments dans I'intestin etait gkneralement plus eleve dans la fraction descendante de la population. bes comportements migratoires variaient de la montee au cr6puscule et a I'aube, avec descente au milieu de la nuit, aarx migrations inverses lorsque le niveau d'habitat de nuit est plus profond que celui du jour. La dispersion nocturne des populations herbivores et omnivores en fonction de la profondeur reflPte probablement l'evitement de la predation en prksentant des agregats moins denses aux predateurs mobilitk verticale. Les prkdateurs aveugles se trouvent en eau plus profonde qkee leurs proies durant le jour probablement parce qu'ils scsnt plus gros et donc plus vuln6rables eux-m@mes2 la prkdation 2 vue. Les pr6dateurs a vue descendent L3 de plus grandes prsfsndeurs que leurs proies la nuit. Tous les modes de migration observes peuvent s'expliquer en termes d'evolution par la simple concurrence alimentaire et I16vitementdes pr6dateairt;.

a

Received Augur t 7, 7 985 Accepted December 18, 7 985

(J8-375)

ritten accounts s f the surface swarming of aquatic organisms date back to at least the beginning of the nineteenth century when Cuvier observed that daphnids occurred at the surface during the moming and evening on bright days (see Cushing 1951). Since Michael's (191 1) work on the vertical migration of chaetcpgnaths most investigators have used sequential water samples or horizontal net tows at various depths to study the die1 movement of plankters. However, indirect analyses of this type, using changes in population depth modes to denote movements, depends on synchronous movement by most members 952

of a population; otherwise it could lead to e m n e o u s conclusions about the strength and even existence of vertical migration (Pearre 1979). An asynchronous population which undergoes an extensive vertical migration but spends little time at either or both its depth extremes or in transit would yield seemingly static depth distributions from serial samplings. Obviously, this is because an individual's probability of capture is greatest at the depth or depths at which it spends most of its time. The plankton literature abounds with examples of "static9' populations with bimodal, skewed, or uniform depth distributions which may have been incorrectly used to infer either weak CUM.9 . Fish. Aquaf. Sci., VoI. 43, 1986

Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by 174.118.149.253 on 12/04/14 For personal use only.

or nonmigratory species or development stages (e.g. Russell 1925, % 926; Clarke 1934; Hure and Scotto di Carlo 1974; Lee and Williamson 1975; Sekiguchi 1975; Youngbluth % 976; Hopkins and Gulliksen 1978; Southward and Barrett 1983; Williams and Conway 1984). A timely paper by Bovbjerg et al. (1976) proposed using a passive collector, vertically orientated net traps, to allow a direct measure of vertical migration expressed as the number of individuals moving up or down through a known area over a predetermined time period. Some inference is still needed because movement may be local and random. However, the extent of any migration might be clarified by the deployment of several traps over a broad depth range. This technique has been long used to quantify aquatic insect emergence (Needham 1988) but, as far as we know, it has not been used to study marine plankton migrations. Recently, marine benthic investigators (Thomas and Jelley 1972; Alldredge and King 1977; Youngbluth 1982) have adopted and modified the freshwater emergence trap concept (Mundie I97 1 ; Morgan l 97 1) to study diel migrations of epibenthic organisms into the water column. We developed a clear, semiautoanated, opening closing trap for collecting both ascending and descending openwater plankton populations (Vass et al. 198 1). In the present report we describe the first results of a 24-h vertical migration m d feeding study on the neritic zooplankton population in St. Georges Bay, N . S . , using both the horizontal net tow and ascendant - descendant trap techniques.

Methods St. Georges Bay is a shallow marine ernbayment open on the north to Northumberland Strait and the southern Gulf of St. Lawrence. A 24-h field investigation of the die1 vertical movement of plankton was undertaken near the mouth of the Bay (45"50tN, 6BQ48'W)in -33 rn of water between 08:W August 19 and l0:W ADT August 20, 1980. The sky throughout the study was clear with a high altitude haze present. The wind was less than 10 knots from the northeast on the first day, dying out in the late afternoon, calm throughout the night, and then increasing to -5 knots from the south by 08:OQ the next morning. A half moon was present until shortly after midnight. Alternate low and high water levels occurred at 0 8 5 4 (0.8 rn, above chart datum), 15:29 ( 1.1 m), and 20: 14 (1.1 m) August 19 and 02:29 (1.3 m) and 10:04 (0.$ rn) August 20 with the extreme range being 0.5 rn (Canadian Hydrographic Service B 980). Temperature, salinity, plant pigments, and nutrients data were collected at 12:25 August 19 and 0Q:25 August 28 at 5-m depth intervals using Nansen bottles with reversing themometers. Salinity samples were later analyzed using an Auto-lab@ salinometer. Temperature and conductivity data were also available from an Aanderaa" thermistor chain moored in the Bay throughout the summer. Chlorophyll a and pheopigments were measured on a Turner fluororneter following the techniques of Holm-Hansen et a]. (1965). Nitrate, silicate, and phosphate samples were analyzed with standard colorimetric methods (Strickland and Parsons 1972). Light penetration was measured throughout the water column at 14:08 with a LI-COR3 model L1-185 B quantum meter and L1-192 SB underwater sensor. The ''C fixation method outlined by Strickland and Parsons (1972) was used to measure in situ phytoplankton primary production at 5-m depth intervals (see Marine Ecology Laboratory 1980). Incubations started at 09:30 Can. J . Fish. Aquat. Sci., Vol. 43, 1986

and ended B 3:30 August 19. Incident radiation was recorded on deck throughout this study with a L1-C0RU%kI-550 integrator, set for 10-anin intervals. Daily carbon fixation at each depth was extrapolated from the fraction of radiation received during the incubation period. Transparent traps were designed and built to collect vertically mobile plankters in the field. Detailed material, design, and construction specifications have been documented (Vass et al. 1981). Each trap unit consists of a down-facing and up-facing pyramid-shaped funnel (0. 16-m2 openings) to concentrate and direct ascending and descending plankters into separate 2.6-L collection chambers. These chambers are opened and then closed at depth by a de~uble-messengertripping mechanism, through the sliding action of a spring-loaded gate valve. In this study, four trap units were moored at 8, 34, 21, and 28 m depth (Fig. 1). The mooring was kept taut between a train wheel and subsurface float. During deployment the collection chambers are filled with GF/C-filtered seawater and lowered in the closed position to avoid surFace contamination. Self-opening flaps on the walls of the collecting funnels ensure flushing during deployment. The battery operated messenger-release timer is activated on deck before deployment. This timer is programmed to release a narrow messenger 30 min after activation and a broad messenger 4.5 h later. The first messenger strikes the trip bar closest to the mooring wire which allows the gate valve to slide to the open position and release a similar messenger beneath the first trap, This process continues until all four traps are opened. The traps are allowed to collect mobile plankters for 4 h after which the subsurface timer releases a broad naessenger. This strikes a second trip bar further from the wire which releases the gate valve to slide to a closed position. Similarly, this initiates the closing process for the other three traps. The entire assembly can be retrieved on deck, trapped plankton preserved in 5% buffered formalin solution, and redeployed within an hour. In all, four deployments were made during this study. The collection times of l 1:00- 15:00, 17:6)0-21 :MI, 23:OO-03:00, and 05:OO-09:00 ADT were chosen to coincide with day, dusk, night, and dawn light conditions. All trapped plankton were identified to species and developmental stage although only the more abundant forms can be used here to decipher vertical migrations. The value of having clear plankton traps was tested on two separate days the following year, August 18 and 20, by covering two of our four traps with black plastic. All four traps were deployed at 14 rn depth on separate moorings within a 5000-rn2 area in St. Georges Bay. The clear and dark traps were opened simultanecsusly ( k 3 min) and allowed to collect plankton for 4 h between 11:00 and 16:OO. Eight series of Clarke-Bumpus net (12-cm diameter, 333-pm mesh) tows of 4-5 min duration were taken in 1"BO to overlap with the opening and closing times of the plankton traps. A series comprised seven separate horizontal tows at 5-m depth intervals; each vertical series required about 1 h. The order of towing was always from shallowest ( 1 m) to deepest (30 m) depth. The tow depths were estimated from wire angle and length of wire out and verified at the end of each tow from a Benthos time-depth recorder (No. 1170E) trace. Even the deepest tows were within l raa of the desired depth. Each net was soaped and/or spray cleaned before use, thus eliminating cumulative clogging problems. Average filtration during a tow varied little over our sampling scheme, 5.37 t 0.76 m3 (F k SD) seawater. Time did not allow duplicate tows but it is


hoped that the tow durations were sufficiently long to even out some small scale patchiness. The most abundant forms were subsampled with a Motoda splitter because of large sample size, We calculated fiducial limits of subsampling (Iforwood and Driver 1976) to arrive at the Beast number of sample splits needed to distinguish significant changes in a species abundance over depth. Only common species are reported here. In interpreting population depth shifts, we found that some distributions were asymmetrical. We therefore decided to use pspuBation depth medians and quartiles, following the example of Pennak ( 1 943) and Bosch and Taylor (1 973). Excessive patchiness caused US to follow earlier workers by reporting depth-frequency distributions as percentages. The dominant species caught in both trap and net tows were visually assessed as to the presence or absence of food in their digestive tracts by clearing the organisms in glycerin. The guts of fish larvae were dissected and examined.

SUB

Physical and Biological Cepnditions during the Field Experiment

MESSENGERS

FIG. I . Deployment of mooring with four traps (see text).

Past studies have shown that the thermally homogeneous surface layer gradually deepens from 10 rn in June to >30 m by %ateOctober (Hargrave et al. 1985). During our 24-h field experiment the upper mixed layer was nearly isothermal ( % 8.7 - 17.3"C) and isohaline (29.4 - 29.50/,,) down to -25 rn depth (Fig. 2). The bottom layer was cooler (17.3- 13.6"C) and slightly more saline (-29.6%,) with a vertical extent of only 8 rn at our sampling location. Past studies indicate that this stratified condition is persistent and widespread in the Bay, altered only by the available depth of water and season. Dissolved nitrate (0.48 t 0.07 phlol L- ') and phosphate (0.54 f 0.03 pMol k-')concentrations were low throughout the upper mixed layer, both day and night (Fig. 2). Silicate concentrations (4.8 2 0.3 pMolvL-') were uniformly high in the upper layer as expected from our previous study (Hargrave et al. 1985). A strong gradient of all three nutrient concentrations existed below the thermocline, increasing towards the sediment surface (Fig. 2). The apparent day -night differences in temperature, salinity, and nutrient concentrations at 30 rn depth (Fig. 2) are an artifact caused by the tidal change in the water depth. The water column was very turbid due to previous strong northeast winds which resuspended sediments from the shallow margins of the Bay. Only 57% of the surface radiation reached I m depth, which approaches the most turbid coastal waters observed (Sverdnep et al. 1942). The mixed layer was deepended 8 m by the storm and exceeded the euphotic zone by about 5 m at the start of the field experiment. In 1977, carbon assimilation by phytoplankton increased gradually throughout the summer with maximum rates in August through September (Hargrave et al. 1985). The level of primary production in the present study is similar to the maximum rates observed in 1977, 455 mg C m-2.d-', and was highest between 5 and 15 m depth. There was no accumulation of phytoplankton stocks, as measured by plant pigments, over the day-night period, suggesting a rapid consumption by herbivores. Previous studies of the biological dynamics in St. Georges Bay ii~dicatea rapid, tight coupling between nutrient regeneration, phytoplankton production, and consumption by herbivores and in turn by carnivores (Hargrave et al. 1985). Can. J . Fislt. Aqusf. Sci., Vo1. 43, I986


I

M

I

I

I

0

0

500 1000 1500 p ~.rn-Z%-' LIGHT INTENSITY

TEMP.

1%

15

17

Pseuhcaianus minutus

PWAEOPW~TIN

PRODUCTION

I

- L-'

2

CHLOROPHYLL

2

-

29.4

29.6

SALINITY

(%,I

NITRATE

pmok b-'

19

0 I

,

I /

2 ,

l

-

0

I

LJml-L-'

~rnolL-'

PHOSPHATE

SILICATE

FIG.2. Vertical depth profiles of light, primary production, salinity, and temperature and chlorophyll a, phaeophytin, phosphate, nitrate, and silicate concentrations during a day (broken line, August 19) and night (solid line, August 20) sampling.

Zooplankton Distributions, Movements, and Feeding Periodicity The following is a descriptive account of the observed vertical movements and feeding periodicity of each of the common species in St. Georges Bay, discussed in context with previous studies. The order in which a species is presented depends on its migration pattern, starting with the complex dusk and predawn rises between midnight sinking (e.g. PseudocaPanus), through a series of intermediate patterns, to the so-called reverse migration where the night level inhabited is deeper than the day depth (e.g. Balaemonetes and Cancer).

Can. S. Fish. Aquat. Scl., Vof.43, 1986

The patchy distribution sf this species resulted in an order of magnitude change in abundance after the third series of horizontal tows (Fig. 3). Although this change coincided with the dusk ascent, we can find no evidence of deep transit from either the depth-frequency diagrams or trap collections which one would expect if we had missed sampling a significant proportion of the population close to the bottom during daylight. Adult females and stage V copepodids were concentrated in the upper 15 m but the range of this species extended to the bottom (Fig. 3). Adult males were located deeper in the water column and their population was more dispersed (Fig. 3). All three stages had a tendency to rise towards the surface at dusk, submerge by midnight, and rise again before dawn. The final descent to daytime depths started at least 2 h before dawn. This migration behavior, known as "midnight sinking," has been reported for many species of marine plankton and it is usually ascribed to a lack of orientation by the plankters during darkness (see Cushing 1951 ) but also due to satiation (Pearre 8973). In our case a bright half moon was present until after the midnight sampling; thus there would be a selective advantage to early descent, once satiated, to avoid visual predators. The trap results, in general, support our interpretations of the vertical migration of Pseudocatanus from population depth analysis (Fig. 3). The daytime upward component at 8 m depth appears to be overly high given that the traps were located outside a patch and there was no apparent change in the population's depth distribution over the same time. The dusk rise is nicely recorded by the traps. However, the predawn rise is inadequately represented in the trap collections, especially considering the large numbers of Pseudocalanus present in the water column. The postdawn descent of the population is well represented by the trapping results. Our observations on the gut contents of trap and net collected zooplankton species demonstrate that n-nany individuals had defecated within the traps because fewer of the trap-collected organisms had material in their digestive tracts (e.g. Table 1). Further discussion of feeding periodicity, therefore, is based on gut observations made on net-collected individuals (Table 2). In our 24-h study, female Pseudocalanus fed mainly at night although greater than 20% of the population was feeding at any time of the day (Table 2). Stage V Pseudocakanus fed equally well during dusk and nighttime with 84 and 88% of the population feeding during daytime and dawn periods, respectively. Ps~udscalan~s males had empty guts throughout this study, which suggests a solely reproductive function at this time of the year. Previous field studies have all shown that Pseudocalanm~s feeds mainly during the dusk and dawn periods (Wirnpenny 1938; Mackas and Bohrer 1976; Nicolajsen et al. 8983). Bohrer (1988) has described dusk and dawn surface migrations by captive female Pseudocalanus in a 10-rn tower tank when food was either absent or at low concentrations (1-2 nag Ch1 a mm-3). This population was dispersed deeper in the water column during the nighttime at these How food concentrations. Bohrer found the At chlorophyll a concentrations > 2 mg night rise was unirnodal, occurring in the first half of the night and followed by a gradual sinking of the population throughout the night. Chlorophyll a concentrations in the present study were Bow (1.0- 1.5 rng m-7 and uniform throughout the upper 25 m (Fig. 2). Thus, the observed migration pattern of Pseudoa

955


I

. -

I

I

I

I

Pseudacalanus minutus IZ

FIG.3. Depth-frequency diagrams and trap results (dark arrows) of Pseudsc.alanus minutus females, males, and stage V cc~ppcadidsfor eight and four sampling periods, respectively, between 10:30 August 19 and 09:30 August 20, 1988. lncident radiation recorded on deck is indicated in the upper panel; arrows indicate sunset and sunrise. The actual nunmber of individuals moving up or down into the traps at 8, 14, 21, and 28 rn depth is indicated next to each arrow. Trap deployment and retrieval time was set to coincide with the nmiddle of adjacent horizontal, net-tow series. The 25 and 75% population quartiles are connected by broken lines and the population median is indicated by a black dot. The number located inside each depth-frequency diagram (scale lower right) is the estimated number of individuals * rn "in the water column during this series of horizontal net tows. TABLE1. Comparison of die1 feeding patterns (96 with food in gut) obtained from observations of plankton net- versus trap-collected zooplankters ( N = sample size). -

Gear Temom longicormis, 9 Pseledocalanus mknutus, ? Centropages hnmn~us,9 Podon in termedius

Net Trap Net Trap Net Trap Net Trap

p

p

Day Dusk Night Dawn N N % N % I V 97 57 31 1 77 8 27 11

300 684 199 74 117 119 89 101

98 75 26 5 95 18 68 55

350 253 286 117 85 M 73 30

98 69 56 30 90 15 52 20

319 235 343 93 83 66 145 41

95 71 20 42 78 40 33 3

299 217 350 174 89 115 114 $3

Can. J. Fish. Aquhat. Sci.. Vol. $3, 1986

TABLE2. Die1 feeding patterns 6% with food in gut) of net-collected specimens (N Day (l0:45- 15:30) 9k

N

Dusk (l7:OO-21:30)

Night (23:OO-03:30)

N

96

%

=

sample size).

Dawn (05:OO-09:30)

N

96

N

Evadne Bivalve Iarvae Podon Pseuduc~nkzrau,~"

Q Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by 174.118.149.253 on 12/04/14 For personal use only.

V Temcprn

Q 6 Centropages

0

8 Tortanus

0 d CaEaszus IV, V Cancer zasea Scrgkttn Pakutpmonetes larvae Taurogolrbrus larvae "Pseucfoculanusmales did not feed, N

-

-

125.

calanus in St. Georges Bay is consistent with the findings of Bohrer at low chlorophyll levels. Lsn the Ray, Pseuhcahnus occupies different depths of the euphotic zone at different times of the day and appears to utilize phytoplankton from the entire productive zone even though feeding is at least partly restricted in time.

TABLE3. Upward movement of zooplankters (no. -4h ' .0. $ 6rn ', SD,1= 4) during daylight, between 10:00 and 16:00, into clear and darkened traps at 14 m depth, August I8 and 20, 1981, St. Georges Bay (ns = significant).

Temora longicornis

Psaudocalanrts rninutus

The abundance of Ternera was less variable (-5 times) than Pseledoca~an~~s, with no broad patch moving through the sampiing area. Adult populations were concentrated near 10 m during daylight; however, the males were dispersed deeper in the water column (Fig. 4). At dusk, adult T ~ Z @ migrated ~ Q towards the surface, their median population depths reaching -5 rn by 21:QO. Small female T m o m ( 16%. The sightless predators, such as Torfanus,Saga'ma, and perallUfrequent S, deeper waters during the day prehaps C C ~ C J ~ sumably because they are more vulnerable themselves to visual predation. Both Sagitta and Calanus migrate up briefly to feed at dusk; Tortanus, however, inhabits a broader depth range both day and night and appears to feed throughout the die1 cycle. Conversely, species which use vision to capture prey, such as larval cunner, Paiaemoreetes, and Cancer, frequent at least the lower limit of the herbivore zone by day and descend by nightfall. The cunner feeds only during daylight in nearsurface waters. These predators must gain some advantage from descending to greater depths at night other than fo!lowing their prey because their nighttime depth is below mast of the herbivore population. This behavior may serve to remove them from predation by jellyfish (Cyeanea) wear the surface at wight. In general, then, the die1 patterns of zooplankton depth distribution in St. Georges Bay probably reflect a "trade-ofT9 between finding sufficient food and avoidance of being consumed themselves.

It is a pleasure to thank Ray Sheldon who managed and greatly facilitated the research carried nut from the field station at Crystal Cliffs. We arc most grateful to Bob Conovcr for consultations throughout our endeavors and also for presenting an earlier version of this manuscript to the Second International Conference on Copepoda in August 1984, Ottawa, Ont. Ken Drinkwater kindly supplied thermistor chain data and Nick Brouse assisted with masurernents of phytoplankton production, plant pigments, and nutrients. Ursula Grigg did a very capable job of enumerating and identifying the species and stages in our samples. Andy Hennebeny ~analysedthese samples to decrease the sampling variance of the less abundant species. Special thanks go to Captain Neil Langille, Ralph Savoury, and Hughie Marriott of the M . V . Na~icuEafor their willingness to work continuously for 30 h under very cramped conditions. We thank John Pringle and our reviewers for being very helpful.

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