Feeding and diel vertical migration cycles of - Springer Link

Polar Biol (1995) 15:21-30

9 Springer-Verlag 1995

M.D.G. Lopez 9M.E. Huntley

Feeding and diel vertical migration cycles of Mefridia gerlachei (Giesbrecht) in coastal waters of the Antarctic Peninsula

Received: 18 January 1994/Accepted: 10 April 1994

Abstract Diel vertical migration and feeding cycles of adult female Metridia gerlachei in the upper 290 m of a 335-m water column were measured during a total of 65 h in two periods of early summer (Dec 20-21 and Dec 25-26, 1991). Samples collected in eight depth strata by 35 MOCNESS tows (333%tm mesh) were analyzed for abundance and mean individual gut pigment content. Most of the copepod population was concentrated in a 50-m depth interval at all times. Feeding began simultaneously with nocturnal ascent from a depth of 200-250 m at ,,~ 18:00 h (local time), when the relative change in ambient light intensity was greatest. Ingestion rate increased exponentially (ki = 0.988 h -1) at double the gut evacuation rate (ke = 0.488 h - 1 ) as the population moved upward at 22.3 26.5m h-1 through increasing concentrations of particulate chlorophyll-a. Although the bulk of the population did not move to depths shallower than 50 m, and began its downward migration at a rate of 20.8-31.7mh -1 in complete darkness, individual females continued to make brief excursions into chlorophyll-rich surface waters (4-8 gg1-1) during the first few hours of population descent. Ingestion rate diminished abruptly by one order of magnitude (ki = 0.068 h - 1) at dawn ( ,,~ 03:30 h). Within four more hours, the population had reached its daytime depth

M.D.G. Lopez 1 Marine Science Institute, University of the Philippines, Diliman, Quezon City 1101, Philippines M.E. Huntley ([~l) Marine Biology Research Division, Scripps Institution of Oceanography, 0202, La Jolla, CA 92093-0202, USA Present address:

1Department of Oceanography, School of Ocean and Earth Science & Technology, University of Hawaii at Manoa, Honolulu, HI 96822, USA

and gut pigment content remained constant at a minimum value until the next migration cycle. No feeding appeared to take place at depth during the day. Ingestion by M. gerlachei females removed < 4% of daily primary production, with only ~ 20% of this amount being removed from surface waters by active vertical transport.

Introduction

Although it has long been known that the feeding behavior of zooplankton is strongly linked to their diel vertical migration (Weismann 1877), the simultaneous and detailed quantification of both behaviors has proven difficult. It is not uncommon for a species to migrate a hundred or more meters within a few hours to feed near the surface (e.g. Bainbridge 1960; Banse 1964). Thus, to simultaneously quantify both feeding and migration requires repeated, depth-stratified sampling and a rapid means of assessing ingestion rate. Metridia gerlachei, a mesopelagic copepod found throughout the Southern Ocean (Baker 1954; Everson 1984; Mackintosh 1934), is a strong vertical migrator which remains below 200 m during the day and feeds near the surface at night (Hardy and Gunther 1935; Vervoort 1965). It feeds mainly on phytoplankton, but becomes more carnivorous when under pack ice (Hopkins and Torres 1989). Daily ingestion rates extrapolated from short-term incubations suggest that M. gerlachei may be able to meet its metabolic requirements on a diet of diatoms (Schnack 1983; Schnack et al. 1985). However, its ingestion rate decreases with decreasing food availability (Schnack 1983), and phytoplankton and total microbial concentrations below 100 m are relatively low (Lipski 1985; Karl et al. 1991; Tien et al. 1992). Therefore, estimates of the daily food intake of M. gerlachei must take account of the amount of time it actually spends in the surface layer.

22

Diel migration by Metridia 9erlachei has usually been inferred from comparisons of day and night vertical abundance profiles (e.g. Chojnacki and Wegl6nska 1984; Hopkins and Torres 1988; Huntley and Escritor 1992; Mackintosh 1934), which yield no information on timing. Rudyakov and Voronina (1974) observed that M. gerlachei rises in the early afternoon and sinks at midnight, and estimated migration velocities to be 30-56 m h - 1. Prior to the invention of automated, depth-stratified, net sampling systems such as the MOCNESS (Wiebe et al. 1976) or the Longhurst-Hardy Plankton Recorder (Longhurst and Williams 1976), depth-stratified samples of the water column often required several hours, with the result that either relatively few samples could be collected during the diel migration cycle of the plankter being studied, or only shallow layers could be sampled. The measurement of ingestion rate posed a similar problem. Until the advent of the gut-fluorescence method (Mackas and Bohrer 1976), the most common method for measuring feeding activity required bottle incubations; not only do such measurements require considerable time, but they may not reflect in situ rates of ingestion. In the study presented here, we used both multiple net sampling and gut fluorescence measurements to examine the diel feeding and vertical migration cycles of M. 9erlachei during early summer (Dec 20-26, 1991) at a coastal station in Gerlache Strait, near the Antarctic Peninsula. We report diel changes in the depth distribution of adult females in the upper 290 m of the 335-m water column, and associated changes in gut pigment content. Gut pigment evacuation rates were measured in the laboratory, enabling estimates of in situ rates of ingestion and evacuation. We then examine how these cycles might influence the metabolic budget of M. gerlachei females, and the redistribution of organic matter in the water column.

Materials and Methods Zooplankton collection Two series of stratified zooplankton tows were made using a 1-m 2 MOCNESS (Biological and Environmental Sampling Systems, Falmouth, Massachusetts) over a mean water depth of 335 m at RACER Station A (64~ 61~ The first series covered 42 h from 01:15 local time, 20 December to 19:05, 21 December 1991; the second series was collected over 23 h from 18:20, 25 December to 17:20, 26 December. Tows of approximately 45-rain duration were made every 1-2 hours, with generally higher frequency during periods of relatively low ambient light intensity, from 21:00 to 08:00 local time. A total of 35 tows were made during the 65 h of observations. To diminish the potential effect of advection on our ability to repeatedly sample the same population, we chose as our sampling site a station previously identified as the site of a long-lived (3month) eddy in springtime (Lopez et al. 1993). Each tow was made in a direction from the central station offset by 90 ~ from the previous

tow (i.e. NNE, SSE, SSW, NNW), transiting a distance of approximately 1 km. The cycle of tow directions was repeated every 4 h. The following depth intervals were sampled with 333 gm nets: 0=5, 5-15, 15-50, 50-90, 90-130, 130-170, 170=210 and 210=290 m. During the first sampling series, these strata were fished from depth to the surface, regardless of the time of day. The time required to fish through the eight strata was generally 20=30 rain; an additional 10-15 min were required to transit in the opposite direction with all nets closed. Thus, during the second sampling series (Dec 25-26) we opened nets during descent of the MOCNESS when Metridia 9erlachei was deepest in the water column, and during ascent of the MOCNESS when the copepods were closer to the surface. This approach allowed the least time for evacuation of gut pigment to occur during sampling. Depending on catch size, 10-50% of cod-end contents from the first sample series was immediately drained at low vacuum onto G F / D filters and frozen at - 80~ for pigment analysis. Remaining fractions were preserved in borate-buffered 10% formalin in seawater for enumeration. In the second series, 50=90% of catches from the modal depth were frozen for gut pigment analysis. Catches from all other depths in the second series were treated as in the first series.

Gut pigments Measurements of gut pigment content were made on shipboard within one week (generally within 1-2 days) after collection, following standard methods (e.g. Dagg and Walser 1987; Huntley and Escritor 1992). Adult female Metridia 9erlachei were picked from the frozen filters with the aid of a dissecting microscope in low, incandescent light. Individual filters required no more than 5 min for processing. Brief exposure to light during picking has no significant effect on gut pigment estimates (Simard et al. 1985). For each sampled depth, gut pigments were extracted from groups of 10 copepods immersed in 7 ml absolute methanol and refrigerated at 1-3~ for ~ 2 h in the dark. In samples from the second series, at least 10 groups of copepods were obtained from each modal depth and adjacent intervals. Due to the rarity of M. 9erlachei at other depths it was often not possible to collect as many as 10 groups of copepods, and at some depths we obtained a single sample containing < 10 females. Gut pigments were measured on a Turner Model 10 fluorometer.

Gut evacuation rate During the second sampling series we measured gut evacuation rate using females collected in a 10-min tow from the 15-50 m depth stratum at approximately 02: 00 local time, when Metridia gerlachei was near the peak of its nocturnal migration and feeding cycle. The catch, which consisted almost entirely of M. 9erlachei, was immediately placed in a container holding 20 liters of GF/C-filtered seawater and allowed to defecate for a period of 7 h. Samples were removed at 1-2 rain intervals during the first 10 rain, 5 min intervals for the following hour, and at 20-40 min intervals for the remainder of the experiment; these were immediately filtered onto G F / D filters and treated as were field samples (see above). Seven to 10 groups of 10 females each were analyzed for each time point.

Environmental parameters Prior to each MOCNESS tow, water for pigment determinations was collected with a 10-1 bottle rosette sampler at 2, 5, 10, 15, 20, 30, 50, 75, 100, 200 and > 300 m (near-bottom). Chlorophyll a and phaeopigment derivatives were measured after dark extraction in absolute methanol (Riemann 1980). Surface photosynthetically active radiation (PAR) was monitored with a 2n irradiance meter

23 (QSR-240, Biospherical Instruments Inc., San Diego). During each net tow, temperature and salinity data were collected using CTD sensors (Sea-Bird Electronics, Bellevue, Washington) carried aboard the MOCNESS.

ol so| g

Results

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Physical and biological environment Depth profiles of temperature and salinity were stable and consistent throughout the field study. Temperature decreased rapidly from a maximum of 0.5-1.5~ at the surface to - 0.25~ at 75 m, where it then declined less sharply to a minimum of - 0.65~ at 300 m (Fig. 1A). There was a slight difference between temperature profiles in the 75-150 m depth interval, depending on whether we towed to the west or the east; in the former direction temperatures were - 0.1 to - 0.2~ whereas to the east they were between - 0.3 and - 0.5~ Salinity increased rapidly from 33.85%o to 34.3%o in the upper 100 m, reflecting the input of fresh meltwater, and then more slowly to a maximum of 34.52%o at 300 m (Fig. 1B). A strong pycnocline, dominated by the influence of salinity, was present throughout the upper 100 m; even waters below this depth were not clearly isopycnal, suggesting little vertical mixing (Fig. 1C). Surface light intensity was greatest ( > 1,000x 1016 quanta c m - Z m i n -~) from approximately 07:00 to 16:00 h local time; apparent total darkness lasted for almost 4 h, from 23: 00 through 03: 00 (Fig. 2). The greatest concentrations of chlorophyll-a in the water column were in the upper 30 m, and showed no diel variability (Fig. 3). Maximum concentrations occurred in the 5-15 m depth range, generally 4-8 pg 1-x, but occasionally exceeding 10 lxgl-L Concentrations decreased by more than one order of magnitude, from 0.35 ggl-~ at 35 m to 0.03 g g l - ~ at 200 m, equivalent to a decrease from 17.5 to 1.5 pgC1- x ifa C:Chl ratio of 50 (Mitchell and Holm-Hansen 1991) is applied.

Diel vertical migration The abundance of adult female Metridia gerlachei in the upper 290m fluctuated between 170 and 8,628 individuals m - 2 (Table 1). However, there was no clear evidence of diel migration into the sampled strata from deeper water, as changes in abundance were unrelated to either the migration cycle or to changes in ambient light intensity. There were no systematic differences in total abundance throughout the time series, and thus the observed variance may be attributable to horizontal patchiness. The population migrated in unison, with 80% of its biomass generally remaining within a 50 m depth interval, except for the period near the peak of its nocturnal migration, when it was briefly spread over an 80-100 m

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Fig. 1 A - C Physical oceanographic measurements: (A) temperature, in ~ (B) salinity, in %o, and (C) sigma-t at R A C E R Station A in Gerlache Strait during the vertical migration study

depth interval (Fig. 4). During the daytime Metridia gerlachei were centered at g 220 m. The upward migration began when the rate of decrease in light intensity was maximal ( g 18:00h local time). The shallowest depth was attained within an hour or so after local midnight, in complete darkness. The downward migration began immediately thereafter, before any detectable change in light intensity, and ended at approximately 06:00 h, as the daily rate of increase in ambient light intensity reached a maximum (Fig. 2). Only

24 1400/

Table 1 Integrated abundance (no. m-2) of female Metridia gerlachei in the upper 290 m at Station A, Gerlache Strait. "Modal depth stratum" is the depth interval in which the greatest abundance occurred. The majority of the population usually occurred within a single 40-m depth stratum. The mean abundance was 2,030 females

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L O C A L TIME (h) Fig. 2 Daily cycle of ambient surface light intensity (1016 quanta cm-2 rain -a) at Station A, Dec 25 26, 1991, as a function of local time. Data courtesy of O. Holm-Hansen and A.F. Amos

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Fig. 3 Chlorophyll-a concentrations (pg 1- 1) at Station A during the vertical migration study. Contours, beginning at 0.2pg1-1 and separated by intervals of 1.0 gg 1- ~, were calculated with a kriging technique on a 1326-element grid using Surfer 4.0 (Golden Software, Boulder, Colorado). The time axis begins at 00:00 h (local midnight), Dec 20, and ends at 18 : 00 h Dec 26, 1991. The vertical dashed line at 42.5 h represents the 4-d separation between the two data sets. Small dots represent time-depth coordinates where data were collected. Data courtesy of M. Vernet and O. Holm-Hansen

a small fraction of the population (10-30%) was ever at depths where the chlorophyll-a concentration exceeded 0.2 pg 1 - 1 (Fig. 3), and even this lasted for a period of no more than 1-2 h (Fig. 4). The vertical displacement of the population median with respect to time (Fig. 4) suggests a migration velocity of 22.3-26.5 m h - ~ during ascent, and 20.8-31.7 m h - ~ during descent.

Gut evacuation rate The gut evacuation experiment was initiated at 02:00 h, when Metridia gerlachei was near the peak of its nocturnal migration and feeding cycles. Shipboard measurements of copepod gut content were fitted to the exponential model: Pt = P0 e-k~

Modal depth stratum (m)

% of Population in modal depth

Series 1, 20-21 December 1991:

04':o0

24:00

No. m-2

(1)

01:15 03:15 05:14 07:07 09:11 11:19 13:24 15:22 17:20 19:14 21:08 23:19 01:11 03:05 05:10 07:14 09:10 11:06 13:13 15:13 17:21 19:07

364 1489 3566 3015 1470 936 1095 904 227 293 1288 1351 911 1881 8628 3042 3445 1059 1333 5547 170 836

50 90 90-130 170 210 210-290 210-290 210-290 210 290 210 290 210-290 210-290 170-210 170-210 15 50 130 170 170-210 210-290 210-290 210-290 210-290 210-290 210-290 210-290

60 69 95 95 98 94 97 99 97 98 82 71 50 66 89 72 98 96 98 99 95 75

Series 2,25-26December 1991: 18:46 1429 210 290 21:00 3085 130-170 22:00 2642 90-170 23:01 1334 90-130 01:11 406 50-130 2:46 4861 90-130 3:16 2847 90-130 5:04 1385 170-210 7:02 4160 210-250 8:29 1566 210-250 9:41 2706 210 250 14:03 315 210-290 17:17 1445 210 290

98 65 79 53 47 79 44 46 73 85 66 97 55

where Pt is the gut pigment content (ng chlorophyll-a equivalents per individual) at time t, Po is the initial gut content, and ke is the gut evacuation rate constant (h-t). The experimental data yielded a gut evacuation rate constant of ke = 0.488 h - t (n = 143; r 2 = 0.93; Fig. 5), with Po = 13.89 ng individual-1. The corresponding gut retention time can be approximated as 1/ke = 2.05 h. Gut pigment content in situ The interval between the time of capture and the ti-lme at which specimens were fast-frozen for gut pigment analysis was in the range 4 4 2 min (X = 18.2 min). Thus, to estimate the actual gut pigment content at the time

25

100

200

2.~ 2 0 0

300

0

12

24

48

36

TIME (h)

60

72

Fig.4 Metridia gerlachei females: Depth contours of population percentiles, shown in intervals of 20%. The value shown represents the percentage of the population above the depth indicated, e.g. at 00:00 h 10% of the population occurred above 30 m, and 90% occurred above 120 m. Three migration cycles are clearly visible during the 3-d composite data set. Contouring procedure and symbols as in Fig. 3

100_

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Fig. 5 Metridia gerIachei females: Gut evacuation rate of specimens captured at 02:00 h, Dec 26, 1991 and allowed to void their guts in filtered seawater. Gut content values are corrected for pigment loss in the net (see equation 2)

of capture, we corrected all measurements on fieldcollected copepods by applying the known evacuation rate (ke = 0.488 h - 1), i.e. Pt

Pf -- -kot e

(2)

where Pf is the estimated gut content at time of capture, Pt is the measured gut content, and t is the time elapsed between the time the net was closed in a given depth stratum and the time at which specimens were frozen at 80~ This correction raised estimates of in situ gut pigment content by 3.3 to 40.1% in excess of the measured value. Changes in the gut pigment content of female Metridia gerlachei (Fig. 6) demonstrate that at the population level, feeding by Metridia gerlachei on phytoplankton was coupled to diel migratory behavior. Gut pigment content was greatest ( > 10ng indi-

300

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0

12

24

36

TIME (h)

48

60

72

Fig. 6 Metridia gerlachei females: Depth contours of individual gut pigment content, shown in intervals of 1 ng chlorophyll-a equivalents, as a function of local time (h) during the 3-d study. Gut content values are corrected for pigment loss in the net (see equation 2). Contouring procedure and symbols as in Fig. 3

vidual- i, Dec 20 and 26; > 4 ng individual- t, Dec 21) shortly after local midnight, decreased during early morning hours, and remained low ( ~ 1 ng individual- i) during the day. At the time the population was most shallow, the maximum gut pigment content always occurred in a relatively small proportion of individuals located above the population center. Later, after downward migration had begun, the depth of the greatest gut pigment content (Fig. 6) coincided with the population center (Fig. 4). For example, at ~ 01:00 h on Dec 20, when the population was most shallow, the greatest gut pigment content ( > 9 ng individual -1) occurred at a depth of 45 m, although only 30% of the population was above this depth. By 03 : 00 h, the location of greatest gut pigment content ( > 12 ng individual- 1) coincided with the depth of the downwardly migrating population at 120m. On Dec 21 the gut pigment content just after midnight was greatest ( > 4 ng individual- 1) at about 40 m depth, although most of the population was below this depth. By approximately 04:00 h, the location of greatest gut pigment content ( > 4 ng individual -I) again coincided with the depth at which the downwardly migrating population was centered ( ~ 170 m). Finally, on Dec 26, the greatest gut pigment content at the peak of the migration cycle ( > 11 ng individual -1) occurred at 45 m, although less than 10% of the population was above this depth. By approximately 04:00 h, the gut pigment content was greatest ( > 12 ng individual- 1) between 70-120 m, again coinciding with the depth at which the shallowest 50% of the population occurred. The greatest gut pigment contents always occurred well below the depth of the chlorophyll-a maximum (Fig. 3). The apparent rates of gut filling and evacuation are clearly evident by examining the gut pigment content of individuals located at the population's center of abundance (Fig. 7). The time-dependent increase in gut pigment contents of these individuals on Dec 25-26 was described by: P t = P 0 e kt

(3)

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Fig. 8 Metridia gerlachei: Total gut pigment in the female population (ng chl-a equivalents m-3), as a function of depth and local time of day (h). Contour intervals are 100 ng m-3. Contouring procedure and symbols as in Fig. 3

0.1] 16:00 20100 24100 04100 08100 12100 16:00 LOCAL TIME (h)

Fig. 7 Metridia gerlachei : Mean gut pigment content (ng chl-a equivalents) of individual females, sampled from the core of the population during ascent and descent on Dec 25-26, as a function of local time of day (h). Gut content values are corrected for pigment loss in the net (see equation 2). Results are shown of regression analyses performed on two subsets of the data. Also included are initial gut pigment values from females collected in the upper 50 m at 02:00 h, Dec 26, used in the experimental determination of gut evacuation rate

maxima occurred. On the three days of our study these values were 305, 634, and 654 ng chlorophyll-a equivalents m - 3, respectively.

Di~u~ion Diel vertical migration of the population

where P0 ( = 0.397 ng female- 1) is the initial gut pigment content at to = 18:21 h, and Pt is the gut pigment content at any time thereafter until 03: 34 h, when the nocturnal maximum was reached. Regression analysis provided an estimate of the pigment accumulation rate constant, k= = 0.423 h-1 (n = 201; r 2 = 0.89; Fig. 7). The apparent gut evacuation rate in situ was estimated from the time at which pigment content reached a maximum, at 03:34 h, until 09:41 h, by which time it had reached a constant daytime value. The rate of decrease in gut pigment content during the early morning hours was described by:

Pt =

P m a x e - kat

(4)

where Pt is the gut pigment content at time t in the 6-h interval beginning at to -- 03: 34 h, when the initial gut pigment content was maximal at Pma= -- 14.91 ng female -1, and ending at t = 09:41 h. The apparent rate of gut pigment loss during downward migration is estimated from the constant, kd -- 0.425 h - 1 (n = 110; r 2 = 0.85; Fig. 7), and is significantly different from the gut evacuation rate, ke, measured in the laboratory (p < 0.05). The total gut pigment content of the Metridia 9erlachei female population (ng m-3) was estimated from a weighted value, calculated by multiplying the individual gut pigment content (ng female-1) by the local abundance of females (females m-s). The maximum values on any given day (Fig. 8) provide an estimate of the amount of pigment actively transported from surface waters to depths between 120 and 190 m, where the pigment actively transported from surface waters to depths between 120 and 190m, where the pigment

The migration pattern of Metridia gerlachei through the upper 290 m in Gerlache Strait is similar to that observed in a single migration cycle by Rudyakov and Voronina (1974) in the Scotia Sea in early December, 1971. Both populations remained below 200 m during the day, rose to approximately 50 m, and started their descent before sunrise. In the Scotia Sea, the upward migration began at 17:00h at a rate of 30.142.6 m h-1; the downward migration was greatest between 04:24 to 05:30, when it attained a rate of 36.0-55.8 m h - 1. Similarly, we found the rate of ascent (22.3-26.5 m h -1) to be slightly less than the rate of descent (20.8-31.7mh-), though the absolute rates were less than those described by Rudyakov and Voronina (1974). The Scotia Sea population, which was sampled when nights were longer, remained near the surface for a longer period than in the Gerlache Strait, implying the importance of light in motivating vertical migration behavior. It appears that the upward migration was triggered by a maximum in the rate of change in light intensity, which was greatest at about 18:00 h (Fig. 2). This observation agrees with experimental findings on Daphnia magna, in which the relative change in light intensity stimulates phototaxis and subsequent vertical displacement (Ringelberg 1964, 1966). Our estimate of the population's descent velocity falls within estimates of passive sinking rates of adult M. gerlachei (Rudyakov 1973; Rudyakov and Voronina 1974). Thus, the return to deep water might simply be due to sinking after satiation, which reduces swimming activity in M. pacifica (Mackas and Burns 1986). Metridia gerIachei began its descent several hours before sunrise. In this respect

27

its behavior is similar to that of M. lucens, which in summer in the Gulf of Maine also ascends before sunset and begins its descent in complete darkness (Clarke 1933; Clarke 1934).

where P0 is the initial gut content just prior to the onset of feeding and ascent ( = 0.397 ng female- 1). The total amount of pigment ingested, Ia, after any time during the ascent and feeding period, t, can be found by integration of equation (8), which yields

Rates of in situ ingestion and evacuation Following Head (1986, 1988), the in situ ingestion rate, I, of zooplankton was estimated from i

dC

+ kC

(5)

where k is the evacuation rate constant, C is the gut pigment content, and ~

is the apparent rate of change

of gut pigment content during the time period of interest. We note two periods of the migration cycle during which the pigment ingestion rate must have differed significantly (Fig. 7). The first period began at approximately 18: 00 h local time, coinciding with the onset of upward migration (Fig. 4); gut pigment accumulated at a net rate of 0.423 Pt (ng h- 1), and reached a maximum at 03: 34 h. By this time the downward migration was already well under way, having begun more than two hours earlier (Fig. 4). The second period immediately followed the first, just as ambient light intensity began to increase (Fig. 2), with gut pigment showing net loss at a rate of - 0.425 Pt (ng h- 1). This is less than the evacuation rate in filtered seawater ( - 0.488 P0, implying that some ingestion must have continued during descent. Gut pigment concentrations reached the minimum daytime value by 09:41 h, by which time the population had attained its daytime depth of ~ 220 m (Fig. 4). We refer to ingestion rate during the two distinct periods of gut pigment accumulation as Ia (ingestion during ascent) and Id (ingestion during descent), respectively. For the ingestion rate during ascent, we rewrite Head's (1986) equation, using notation employed earlier, as I, = ka Pt + k e Pt

(6)

where Ia is the rate of ingestion, Pt is the gut content at time t, ka is the apparent rate of accumulation of gut pigment ( = 0.423 h-1), and ke is the experimentally determined gut evacuation rate constant ( = 0.488 h-l). From this it follows that the rate of ingestion during ascent is equal to I, = ki, a Pt

(7)

where k~,a is the ingestion rate constant during ascent, having a value of 0.911h -1 (i.e. ki,a = ka + k~ = 0.423 + 0.488). Substituting equation (3), the ingestion rate at any time during ascent can be determined from I a = ki, a Po ek~t

(8)

Ia = P0

ki,a c k t

~ + c}

(9)

where c = 0.577 is the constant of integration. Similarly, the ingestion rate during downward migration, Id, after feeding had been reduced significantly, can estimated from Id =

-- kd Pt + ke Pt = ki,d Pt = ki,d Pmax e-kdt

(10)

where kd is the apparent rate of gut pigment loss during downward migration (ka = 0.425 h-1), and Pm,x is the maximum gut pigment content achieved during the night ( = 14.91 ng female-1). The rate of ingestion during downward migration, ki,d, is one order of magnitude lower than the corresponding rate during upward migration (i.e. ki,d = 0.063 h-1), but is not negligible. The total amount of pigment ingested during downward migration, Id, can similarly be found by integration of equation (10), which yields ki d -

I d = P m a x ~ d - { - - e -kat --}-C}

(11)

where c = 1.425 is the constant of integration. During this study Metridia 9erlachei appeared to feed only on phytoplankton, and only at night. In the many samples observed under the microscope, guts were consistently translucent, clear, and devoid of matter during the day, from approximately 09:00h through 18:00 h, when the population was mostly below 200 m. This is consistent with independent observations that most individuals below 200 m have empty guts (Hopkins and Torres 1988). Gut pigment analysis corroborates the visual observation that no significant herbivorous feeding occurred. Although the species is thought to be an omnivore, and is capable of ingesting tintinnids (Hopkins 1985) and copepod eggs (Huntley and Escritor 1992) during austral spring and summer, it feeds predominantly on phytoplankton in many regions of the Southern Ocean (Hopkins and Torres 1989) - even during late summer when plant material is relatively scarce. Feeding on athecate protozoans is unlikely to be detected by gut content analysis, but these probably accounted for a minor fraction of total intake by M. 9erlaehei because microbial standing stocks at Station A in early spring consist predominantly of phytoplankton (Karl et al. 1991), and are one order of magnitude less abundant at 200 m than near the surface (Tien et al. 1992). It is therefore a fair assumption that the diet of M. 9erlachei in our study could be accounted for only by its grazing on phytoplankton.

28 The system of equations given above provides estimates of the ingestion rate at any time of day, as well as the total daily ingestion. It is more meaningful to discuss ingestion rates in terms of carbon, so we apply a C:Chl ratio in the range from 50 (Mitchell et al. 1991; Mitchell and Holm-Hansen 1991) to 130 (Sakshaug and Holm-Hansen 1986; Nelson et al. 1989); the former value is applicable to standing stocks dominated by phytoplankton, as in surface waters, whereas the latter value represents an upper limit for the ratio of total POC:Chl in oligotrophic or deep waters. During the period of ascent and active feeding, from 18:20 to 03:34 h, the instantaneous ingestion rate began at 18-47ng C female -1 h -~ and culminated at 886-2,300 ng C female-1 h - i ; the total ingestion during this period was 2.12-5.51 gg C female-1. During the period of reduced feeding and descent, from 03 : 34 h to 09:45h, the initial rate of ingestion was 47-122 ng C f e m a l e - l h -1 and ended at 1.2-3.1ng C female - i h - i; the total ingestion during this period was only 0.15-0.39/_tg C female -1. This brings the total daily ingestion rate to a range of 2.27-5.90 gg C female- 1 which, for a M. gerlachei female of mean body weight in the range from 81 ~tg C (Price et al. 1988) to 99 ~tg C (Schnack 1985; Schnack et al. 1985), represents a daily ration in the range 2.1-7.2% body carbon. Clearance rates, F, can be approximated from the predicted ingestion rate and the ambient concentration of chlorophyll-a. Assuming that the population migrated upward from 220 m at a mean rate of 24.4 m h - i (Fig. 4), we estimate that observed ingestion rates could be accounted for by a clearance rate in the range 12-41 ml f e m a l e - I h -1 (Table 2). After sunrise, the clearance rate would have been reduced by more than one order of magnitude, whatever the initial value. The basic conclusion we draw from these observations is that the rate of ingestion during the seven hours after the onset of upward migration was approximately one order of magnitude greater than it was after sunrise. Estimates of absolute ingestion rate are based on many more assumptions, and are at best only crude approximations. Nevertheless, it is worth considering how such assumptions might affect estimates of the ingestion rate and daily ration so that at least reason-

Table 2 Metridia gerlachei: Clearance rates estimated during nocturnal ascent at 24.4 m h- i. Assumptionsare that migration and ingestion begin at 18:21 h at a depth of 220 m. Gut content is calculated as Pt = 0.397 e~ 423t; ingestion rate during ascent is Ia = 0.911 P~. Chlorophyllconcentrations (C) are mean values at the depths indicated(courtesyof O. Holm-Hansenand M. Vernet). Clearance rate is F = I/C

able upper and lower bounds can be determined. The principal factor affecting these estimates would be degradation or disappearance of gut pigment (Conover et al. 1986; Head 1988; Lopez et al. 1988). Pigment loss is frequently assumed to be constant at ~ 33% (e.g. Helling and Baars 1985; Downs 1989; Dam and Peterson 1993). If this is true, then our estimates of ingestion and daily ration would increase to as much as 8.8 ~tg C and 10.8% body carbon day -I, respectively; clearance rates would increase to 19-61 ml female- I h - i. In the laboratory and particularly after starvation, pigment loss may increase to more than 90% (Conover et al. 1986), increasing ingestion rate and daily ration to 59/ag C and 72% body carbon day -I, respectively; clearance rates would rise to 120-410 ml female- 1 h - i The results of feeding rate measurements on female Metridia gerlachei using bottle incubation methods in spring suggests daily rations in the range 6.4-35.2% body carbon d-1 (Schnack 1985; Schnack et al. 1985). Schnack's estimates of clearance rate (7.4-29.9 ml female- 1h - i; in Conover and Huntley 1991) approximately agree with the range of lower limits we estimated (13-43 ml female- 1 h - i). Thus, pigment degradation could not have been very great, as a loss of even 33 % of ingested pigment would suggest unsupportably high clearance rates, i.e. > 30 ml female-i h-1. We conclude that daily ration was probably < 10%. Regardless of how much pigment might have been lost, the amount of degradation over a period of several days at the same location is likely to be quite constant. For example, Head and Harris (1992) found that in situ rates of pigment degradation in Calanus spp., although high, were not so variable (74-82%) in three experiments initiated between April 6-9 at the same location. We therefore conclude that the relative magnitudes of ingestion rate throughout our data set are accurate.

Grazing impact on the carbon budget in Gerlache Strait Conservative estimates of the ingestion of particulate carbon by the female Metridia gerIachei population suggest that it was significantly less than primary

Depth (m)

Local time at depth

Gut content ng female-1

Ingestion rate (ng female- i h -~)

A m b i e n t Clearance Chl-a rate (gg1-1) (ml female- 1 h-l)

220 200 100 75 50 30

18:21 19:10 23:16 00:18 01:19 02:08

0.40 0.56 3.18 4.90 7.56 10.70

0.36 0.51 2.90 4.47 6.89 9.75

0.03 0.03 0.08 0.13 0.17 0.35

12.1 17.1 36.2 34.4 40.5 27.8

29

production. Applying the estimates of individual ingestion rate (2.27-5.90 I-tg C female- 1 d - 1) to the average abundance (2,030 females m-3; Table 1) suggests a daily ingestion of 4.6M2.0 mg C m - 2 d-1. This represents only 0.7-2.7% of the total primary production at Station A on Dec 25 and 26, which was measured at 437 and 680 mg C m - 2 d - 1 (Holm-Hansen and Vernet 1992). Allowing for 33% pigment degradation would increase the estimate to 1.0-4.1% of daily primary production, which is still a small number. The active vertical transport of particulate carbon from surface waters by Metridia gerlachei (Fig. 8) has a similarly negligible effect on the particulate carbon budget. The removal of particulate carbon amounts to ~ 25 ~tg chlorophyll-a m - 2 or, at most, 3.25 mg C m-2; this would be equivalent to less than 1% of daily primary production. Diel feeding rhythm and its relation to the migration cycle

Metridia gerlachei displays a pronounced rhythmicity in both its feeding and migration activity, but the rhythms are not entirely synchronous. Here we summarize important features of these diel behaviors, and discuss possible causes. Upward migration and feeding activity begin at the same time of day (Figs. 4 and 7), apparently initiated by the maximum rate of decrease in ambient light intensity (Fig. 2), in agreement with the mechanism suggested for Daphnia magna (Ringelberg 1964, 1966). The initially high clearance rate remains constant as the population ascends, but the exponential increase in particulate chlorophyll at shallower depths (Fig. 3) requires an exponential increase in ingestion rate (Fig. 7). Although the population begins its downward migration through decreasing food concentrations just after local midnight (Fig. 4), there continues to be an increase in individual gut pigment (Figs. 6 and 7). This discrepancy is probably due to individuals that make brief excursions toward the surface, where they eat rapidly before swimming down to join the bulk of the population, which continues its descent. Furthermore, the small numbers of females always present in surface waters consistently had higher gut pigment content than those at depth. Such behavior would explain why - after the start of the nocturnal descent - individual gut pigment content was consistently greatest above the depth where M. gerlachei was most abundant (compare Figs. 4 and 6). This explanation is remniscent of Pearre's (1979) demonstration that, although all individuals in a population may perform vertical migrations, such migrations might not be observable as vertical movements of the population as a whole. Similar behavior has been inferred for the copepod Centropages typicus (Mackas and Bohrer 1976) and the chaetogna'th Sagitta eIegans (Pearre 1973), based on the gut contents of individuals caught in deep water.

Ingestion continues to increase for several hours after the downward migration began, and decreases by more than one order of magnitude just before 04:00 h (Fig. 7). Perhaps the copepods have become satiated by this time, or the distance between the surface and the population center is too great to allow for additional individual foraging expeditions. A more plausible explanation is that morning sunlight, which begins to increase rapidly at this time (Fig. 2), triggers a virtual cessation of feeding. The diminution in ingestion is not caused by the lack of available food because, when the population was at the same depth ( ~ 150 m) only 6-7 hours earlier (Fig. 4), individuals were accumulating gut pigment at a high rate (Fig. 7). Whatever the cause, the total ingestion rate for the seven hours after sunrise was one order of magnitude less than the ingestion for the seven hours preceding sunrise. Why the entire population of Metridia gerlachei does not enter the upper 50 m of the water column is not obvious, nor is it clear why the population should begin its downward migration so long before sunrise. Is this behavior an evolutionary adaptation to predation pressure in the surface waters? If so, then why are females of Calanoides acutus, another dominant copepod in local waters, centered at 44 m throughout the day and night in the Gerlache Strait at the same time of year (Lopez et al. 1993), where their presence, and similar size to M. gerlachei, suggests an equivalent susceptibility to predation pressure? Addressing similar questions with respect to the diel vertical migration and feeding of three other common Southern Ocean copepod species, Atkinson et al. (1992) suggested that these behaviors might be related to the vertical distribution of preferred food types or to predator avoidance. We do not have the information required to address these possibilities, and can only concur that greater attention should be focused on the distributions of both predators and prey if we are to understand how different species impact budgets of materials in the water column. Acknowledgements We thank E. Brinton, R. Gartman, S. Kaupp, J. Lovette, W. Nordhausen, and E. Venrick for their assistance in collecting and analyzing zooplankton samples: O Holm-Hansen, M. Vernet and A. F. Amos for chlorophyll and PAR data; and the crew of the R/V Polar Duke for their impeccably professional performance. This research was supported by grant number NSF-DPP 88-17779 from the US National Science Foundation and grant number N00014-92-J-1618 from the US Office of Naval Research.

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