Limnol. Oceanogr., 30(3), 1985, 598-606
0 1985, by the American
Society of Limnology
and Oceanography,
Inc.
In situ twilight grazing rhythm during diel vertical migrations
of a scattering layer of Calanusjinmarchicusl
Yvan Simard, Guy Lacroix,
and Louis Legendre
GIROQ, Departement de biologie, UniversitC Laval, Quebec, Quebec GlK 7P4
Abstract
A scattering layer of Calanusjnmarchicus was sampled every 90 min during 48 h in the lower
St. Lawrence estuary. Grazing activity (phytoplankton pigments in the gut) and the percentage of
recently and nonrecently fed copepods (from observation of food in the gut) were monitored in
two strata (O-30 m and 30-100 m). Phytoplankton was restricted to the upper stratum. A bimodal
twilight grazing rhythm was observed: the first feeding period, in the upper stratum, begins after
sunset; it is followed by the “midnight sinking” in the deeper stratum (2-3 h), during which the
gut content is evacuated; after this, the animals return to the upper stratum for a second meal,
before the dawn descent. In both migrations, there was a dynamic interchange of individuals
between the two strata, which masked the fact that all the copepods migrated to the upper stratum
and that a dawn rise actually happened. The feeding time in the warmer surface water was very
short. Feeding ceased rapidly even if phytoplankton concentration was low. A large increase in the
number of migrants did not change the feeding patterns. Results support the hypothesis that the
behavior of C.jinmarchicus during the central phase of vertical migrations in late summer is closely
linked to an in situ grazing rhythm.
Though many studies have been devoted
to zooplankton/phytoplankton
interactions, a few but increasing number have
considered the effects of short term fluctuations in natural conditions. The importance
of such fluctuations was first pointed out
after observations of a drastic decline in
feeding rates when grazing experiments were
prolonged (e.g. Mullin
1963; McAllister
1970). There is now much evidence that
zooplankton does not always feed continuously. The most frequent feeding rhythm
is diurnal, in phase with the day and night
cycle and with vertical migrations (e.g. Haney 1973; Boyd et al. 1980; Dagg and Grill
1980; Dagg and Wyman 1983; Head et al.
1984), but more complicated
bimodal
rhythms characterized by two peaks of intense feeding activity (at dusk and dawn)
have been reported (e.g. Chisholm et al.
1975; Haney and Hall 1975; Mackas and
Bohrer 1976; Dagg and Grill 1980). Another
rhythm with two periods of feeding activity
LThis work was supported by GIROQ, thanks to the
Fonds F.C.A.C. (Quebec) and the Natural Sciencesand
Engineering Research Council of Canada, and by grants
from NSERC to L.L. and from Fisheries and Oceans
(Canada) to L.L. and G.L. Postgraduate scholarship
from the Fonds FCAC provided financial support to
Y.S. Contribution to the program of GIROQ.
(day and night) has also been observed (Pavlov 1969).
Since feeding rhythms are often associated with vertical migrations, they may reflect periodic contact of zooplankton with
the phytoplankton-rich
surface layer (Gauld
1953). These rhythms are difficult to study
in the laboratory because in situ conditions
are not easy to reproduce (e.g. vertical gradients in food, light, and temperature, periodic starvation, acclimation of grazers, etc.).
In an effort to understand the dynamics of
such rhythms and their relation to vertical
migrations, we made in situ measurements
of zooplankton grazing activity in an area
of a dense scattering layer of Calanus jnmarchicus in the St. Lawrence estuary.
We thank B. d’Anglejan for making the
acoustic equipment available, D. Archambault, C.-A. Boudreau, I. Lamontagne, and
A. Gagne for assistance in the field, and L.
Roy-Saint-Pierre for drafting the figures. We
also thank anonymous referees for their
comments.
Methods
Fieldwork--In
situ grazing of CV C. finmarchicus was measured for 48 h, from 16
to 18 September 198 1, at an anchor station
(110 m deep) located over a zooplankton
scattering layer in the lower St. Lawrence
598
In situ grazing rhythms
599
TEMPERATURE
(“C)
SALINITY
25
L!iL-Lz
1
I
1
(%o)
30
1 I I
L
J
s :mean
-:SD
Fig. 2. Envelope of the temperature profiles and
mean salinity profile during the 48-h sampling period.
Total number of profiles for each variable is 33.
Fig. 1. Sampling area, showing the anchor station
(A).
estuary (Fig. 1). After preliminary sampling,
the water column was divided into a 0-30m warmer stratum (Fig. 2) with phytoplankton (Fig. 3), and a 30-100-m colder stratum
without phytoplankton.
Every 90 min, a
temperature profile was recorded with a
Wallace Tierman bathythermometer,
water
samples (Nishkin bottles) were collected at
0, 2, 5, 15, and 50 m for chlorophyll
and
salinity determination, and zooplankton was
sampled vertically in the two strata with a
50-cm-mouth-diameter
opening-closing
standard net with 76-pm mesh size and
flowmeter. The zooplankton scattering layer was monitored with a Ross 805 echosounder equipped with a 197-kHz transducer.
Water samples were filtered onto GF/C
Whatman filters for on-board fluorometric
determination
of chlorophyll
a and its
pheopigments extracted in 100% methanol
(Holm-Hansen
and Riemann 1978; Riemann 1980). After collection, the zooplankton sample was washed with filtered seawater and a subsample passed through a
76-pm Nitex filter to assemble about 100
Calanus, which were then frozen for later
determination
of their chlorophyll content
(Mackas and Bohrer 1976). These manipulations were completed as rapidly as possible, always within 10 min.
The evacuation time of nut ninment con-
tent was measured for a zooplankton sample collected in the top 10 m at 2030 EDT
on 17 September 198 1. The catch was immediately transferred to a carboy containing 10 liters of twice-filtered
seawater and
placed in a cold darkroom at 5°C. Evacuation of the guts was followed by retrieving
zooplankton
samples from the carboy at
successive times during the following 3 h,
for later gut pigment analysis.
Laboratory
analyses- Salinity
of the
water samples was measured with a Hytech
6220 salinometer. Preliminary
tests were
conducted to shorten the pigment analysis
of the zooplankton samples and also to improve the replicability of the measurements.
Methanol (100%) was used as solvent rather
CHLOROPHYLL
0.0
0.2
a (mg
0.4
mm31
0.6
O-
z
I
c
2i
20-
40-
Fig. 3. Mean chlorophyll profile during the 48-h
sampling period. Total number of profiles is 33.
600
Simard et al.
than 90% acetone, because of its better extraction efficiency and shorter extraction
time (Holm-Hansen
and Riemann 1978).
Sorting was done in an isotonic saline solution (NaCl30”/00) instead of dry-sorting the
copepods packed together on the Nitex filter; thus the animals were washed a second
time to eliminate phytoplankton
cells or fecal debris adhering to them or fluids which
might have come from animal regurgitation
before freezing. This step enhanced the replicability of the measurements since the significant difference (Kruskal-Wallis
test; P <
0.01) found between wet- and dry- (+25%
higher) sorted animals did not occur when
dry-sorted copepods were washed 2-3 times
in the saline solution. No significant difference was found between samples ground
with a tissue homogenizer and unground
samples (Kruskal-Wallis
test; P > 0. lo), so
we eliminated the grinding step. The method used was therefore as follows: zooplankters were rapidly sorted in artificial salt
water, subsamples of about 20 individuals
were put in centrifugation tubes with 100%
methanol, allowed to extract overnight in a
dark refrigerator (the plateau of extraction
was reached after about 2 h), centrifuged,
and the fluorescence of the supernatent read
on a Turner
model
111 fluorometer
equipped with a high-sensitivity
sample
holder. Sorting was done under low light to
prevent photodegradation
of pigments;
simple experiments have shown that this
effect was not important. To minimize possible effects of photodegradation
or other
pigment loss during sorting, we picked up
copepods in a decreasing order of gut content as estimated visually, the fullest-gut copepods (with also the highest pigment content) being placed first in centrifugation
tubes. On the average, each sample was processed as five subsamples. The fluorometer
was calibrated with pure chlorophyll a and
the formulae of Strickland and Parsons
(1972) were used to compute the quantities
of extracted chlorophyll a and the chlorophyll equivalent of pheopigments. The fluorescence background of copepod tissues
was estimated to be 0.32 ng pigments ind-l
(the value of the asymptote reached at the
end of the evacuation experiment) and was
subtracted from each measurement. During
sorting, the animals were classified into two
categories, depending on their recent feeding activity as estimated visually: the animals which were actively feeding when they
were captured or had recently fed (food in
the anterior or posterior part of the gut); and
the animals which had not recently fed at
the moment of catch (empty gut or a very
small fecal pellet in the posterior end of the
gut).
Results
The surface layer (O-30 m) at the sampling station is isolated by a thermocline
from an intermediate cold water layer (3080 m), that overlies the warmer bottom
water (~80 m) (Fig. 2). This vertical temperature structure is typical of the lower St.
Lawrence estuary in late summer (Ingram
1979). The relative thickness of each layer
shows short term variations that are related
to differential advection in each layer and
high amplitude semidiurnal internal tides
(Forrester 1974; Ingram 1979). The mean
salinity profile (Fig. 2) is typical of a partially mixed estuary.
Phytoplankton chlorophyll a in the top 5
m was, on the average, 0.3-0.4 mg ma3 (from
0.04 to 0.97 mg mD3). Most of the phytoplankton was concentrated in the upper 5
m of the water column (Fig. 3), as were the
suspended pheopigments. Pigment changes
in the upper 5 m were approximately
in
phase with the tide, their concentration generally increasing during the flood and decreasing during the ebb (Fig. 4A, B).
The most abundant zooplankter in the
catches, both in terms of biomass and numbers, was C. finmarchicus, with more than
95% of the individuals in the overwintering
stage CV. Numbers during the 48-h series
showed large variations,
some of them
semidiurnal, with a general trend to increase
during the first 36 h (Fig. 5B). The difference
between maximum (40.1 x lo3 ind. mm2)
and minimum numbers (4.8 x 1O3ind. m-2)
was one order of magnitude.
The animals showed typical vertical migrations on both days. The scattering layer
gradually left its day depth in midafternoon,
to reach the top 10 m at about 1930 (Figs.
5C and 6). Not more than 30 min later, the
dense scattering layer gradually dispersed
601
In situ grazing rhythms
UPPER
I$
f:y
Fuy
STRATUM
i.yq
,
E
UPPER
STRATUM
F
LOWER
STRATUM
G
100
80 I
UPPER
STRATUM
1
1
01
LOWER
21
STRATUM
i&b+
0
12
16 Sep
12
17 Sep
TIME
I8
LOWER
STRATUM
D
Sep
(EDT)
12
0
I6 Sep
I2
I7 Sep
I8 Sep
TIMEfEDT)
Fig. 4. A. Tidal height during the 48-h sampling period. B. Mean chlorophyll concentration in the top O-5
m. C, D. Mean mass of phytoplankton pigments per zooplankter in the upper (O-30 m) and lower (30-100 m)
strata. ESH. Percentage of Calanus in the upper and lower strata, with full (dashed line) and empty (solid line)
guts, and 95% C.I. from binomial distribut&n.
for the rest of the night (Fig. 6). The maximum proportion of Calanus recorded in
the top stratum from net catches was 76%.
As the night went on, an increasing percentage of individuals was found in the lower stratum (Figs. 5D and 6). From copepod
numbers only, this period of “midnight
sinking” did not seem to end abruptly with
a dawn rise, since the proportion of copepods in the upper stratum showed a continuous decrease all during the night (Fig. 5D).
The descent was initiated at around 0530
(1 h before the sunrise), and 1 h later there
were no Calanus left in the upper stratum
(Figs. 5D and 6). However, a small patch,
seen for only 5 min on the echogram, was
sampled by the upper-stratum net at 09 17
on 17 September. This explains the small
peak recorded on Fig. 5C and D at this time.
The gut pigment content of copepods in
the top stratum increased rapidly during the
first 2-3 h after surfacing of the scattering
layer (Fig. 4C). A first maximum was reached
at about 2200, followed by a decrease for a
few hours, and then a new increase until the
dawn descent. The lower stratum copepods
also showed this bimodal pattern, the levels
of gut pigments being however, on the average, 59% of that in the upper stratum (Fig.
4D). The first maxima after dusk do not
correspond to chlorophyll peaks in the surface layer (Fig. 4B), since, on both days,
these chlorophyll
peaks were recorded at
18 15, at which time the scattering layer
crossed the 30-m depth (Fig. 6) and < 10%
of the Calanus were in the upper stratum
(Fig. 5D). The first maximum in the gut
content occurred in fact when chlorophyll
602
Simard et al.
1
UPPER
0
12
I6 Sep
C
STRATUM
I2
17 Sep
TIME
I2
0
18 Sep
(E DT)
Fig. 5. Variations in the numbers of Calanus during the 48-h sampling period. A. Tidal height. B. Numbers of Calanus in the whole water column (O-100 m)
and 3-h moving average. C. Numbers of Calanus in
the upper stratum (O-30 m). D. Percentage of Calanus
in the upper stratum relative to the whole water column
(C divided by B). Sunset, 19 10; sunrise, 0640.
concentrations passed through a minimum
(Fig. 4B). The predawn gut content maximum appeared once in phase with (on 17
September) and once with a 90-min lag after
(on 16 September) the chlorophyll
maximum (Fig. 4B-D). During the day, from
0900 to 1800, copepods did not have any
significant gut contents, either by visual examination (Fig. 4G, H) or measurements of
pigment fluorescence (Fig. 4D). These conditions changed drastically during the first
2 h of the night, when the proportion
of
copepods with empty guts fell to almost zero
(Fig. 4H). The fed copepods evacuated their
guts during the following 2-3 h, which resulted in increasing proportions with empty
guts in the upper and lower strata (Fig. 4F,
H). These copepods then migrated to the
surface for a second meal (Fig. 4C, D), which
corresponded to a decrease in the proportion of copepods with empty guts in both
strata (Fig. 4F, H). This dawn rise was more
evident from gut contents (Fig. 4D, G, H)
than from the proportion of copepods in the
upper stratum (Fig. 5D). Then, from about
0530 to 0900, copepods evacuated their guts
in the lower stratum. This agrees with the
evacuation time measured at 5°C (2-3 h:
Fig. 7). Visual observations during the evacuation experiment showed that food transfer from the anterior to the posterior part
of the gut took about 30 min, followed by
90 min for complete gut evacuation.
Discussion
The data set presented here corresponds
to measurements made on a high concentration of Calanus. The sampling and analysis techniques averaged most of the individual
variability
and of the vertical
variability
within each stratum. Sampling
over the whole water column ensured, however, that the scattering layer was always
completely collected and, therefore, that the
samples were representative of the whole
population. Since we did not use a multifrequency echosounder, we do not know if
larger zooplankters or small fishes contributed to the recorded echo. However, the
high frequency used, the high concentrations of Calanus in the water column, their
dominance in the catches, their high lipid
content, and the good agreement between
the vertical distribution
of the scattering
layer (Fig. 6) and that of the Calanus from
net catches (Fig. 5C, D) all support Calanus
as the dominant contributor
to the echo.
The large fluctuations in numbers and the
high concentrations
observed during the
sampling period (Fig. 5B) probably result
from the interaction between tidal currents
and the behavior of the scattering layer that
can generate coastal accumulations in the
area.
The maximum amount of pigment in the
guts of copepods during the sampling period
was, on the average, 2.5 ng ind? (Fig. 4C).
These are low values for a 300~pg dry-wt
copepod compared to other values with the
same method (e.g. Boyd et al. 1980; Kiorboe
603
In situ grazing rhythms
= 60
CL
W
n
80
120
18~30 20~00
2 I:30
23~00 00:3C
TIME (EDT1
)6:3C
-.
18-z&
. Fig.
_ 6 Echograms (197 kHz) showing the position of the zooplankton scattering layer and its vertical extension
m the water column during vertical migrations (16-l 7 September 1981). Each band represents a 2-min recording
period. Bottom depth 105-l 15 m. The darker zone in the O-20-m layer from 2300 to 0200 was generated during
the propagation of high-frequency internal waves and does not correspond to higher zooplankton catches (Fig.
5C).
et al. 1982; Nicolajsen et al. 1983; Dagg
1983; Dagg and Wyman 1983). There could
be several reasons for this. First, there could
have been some loss of pigments during the
freezing of samples; Nicolajsen et al. (1983)
noted a 33% loss of pigments in frozen samples. However, this loss is not general; Dagg
and Wyman (1983) did not find any noticeable effect of freezing. However, such a
loss is too small to explain the low gut contents observed. Second, the copepods may
have been partly carnivorous in response to
the low phytoplankton
concentration (Corner et al. 1974); however, there was no evidence of significant carnivorous activity from
visual examination of gut contents. Third,
over-wintering could have reduced feeding
activity. During over-wintering, Calanus has
low digestive enzyme activity (Tande and
Slagstad 1982; Hirche 198 1, 1983), associated with a reduction of midgut epithelium (Hallberg and Hirche 1980) that is indicative of low feeding activity.
In our
region, Calanus over-winters mainly at stage
CV (Lacroix and Filteau 1970) as in Bals-
fjorden (Tande 1982). At the time of sampling, our animals were essentially CV with
a high lipid content, which indicates that
the overwintering
population was already
building up.
0 : mean
:SD
T
01
t
0
I
I
60
TIME
120
(min 1
I
1
180
Fig. 7. Evacuation rate of gut contents of Calanus
finmarchicus at 5°C. Y = 2.70 exp(-0.022X).
604
Simard et al.
Estimates of daily phytoplankton
rations
can be calculated from the C:Chl ratio in
the area (slopes varying with season from
24 to 66: Levasseur and Therriault
pers.
comm.), a C:dry wt ratio of 0.4 (Curl 1962),
and alternative assumptions concerning the
pattern of feeding activity. These estimates
range from 0.1% of the body C, for a lowfeeding hypothesis (C:Chl = 24; 2 gut fillings
d-l), to 1.6%, for a high-feeding hypothesis
(C:Chl = 66; ingestion rate maximum from
dusk to the first peak in gut content, and
then equal to gut content times evacuation
rate measured at 5°C until dawn). Assuming
that respiration under regular metabolism
varies from 1.6% (OOC at depth) to 2.7%
body C d-l (8OC at the surface) (from Hirche
1983, table 1: 0.7 ,ul 0, mg dry wt-l h-l at
6°C; Qlo = 2, respiratory quotient = 1, dry
wt= 0.3 mg, C content = 0.12 mg), our
estimated rations do not meet the energy
requirement. Alternatively, if copepods were
overwintering,
their respiration
requirement could have been between 0.3% (OOC
at depth) and 0.6% body C d-l (8OC at the
surface) (from Hirche 1983, table 1: 0.15 ~1
O2 mg dry w-t-l h-l at 6°C; same assumptions as above). Since the energy required
for vertical migration is negligible (Vlymen
1970: 1 cm s-l swimming speed), the respiration of over-wintering copepods at the
observed temperatures could have been satisfied by the estimated daily ration without
significant use of their body reserves.
In situ rhythmic grazing-Gut
content
analysis (Fig. 4) clearly showed two night
peaks in mean gut pigments per copepod.
Since the environment studied is dominated by tidal advection processes, the first
possible explanation for these peaks is periodic advection of phytoplankton
or of copepods with a different feeding history.
However, continuous feeding on periodically advected phytoplankton
is not supported by our observations, since the dusk
peaks in gut pigments occurred during phytoplankton minima (Fig. 4B, C); on the other hand, the advection of copepods with a
different feeding history cannot account for
the observed synchronous feeding peaks in
both the upper and lower strata (Fig. 4C,
D), since the two strata did not have the
same velocity and direction as a conse-
quence of stratified tidal circulation. As the
copepods could not graze at depth because
of the very low chlorophyll (Fig. 3), the peaks
in gut content resulted from periodic feeding by Calanus on surface phytoplankton.
The grazing rhythm of the copepod population was, however, not a simple day and
night cycle, but followed a bimodal pattern
with peaks around dusk and dawn. The first
period of grazing activity took place during
the 2-3 h that followed the dusk contact of
zooplankton with the phytoplankton
layer.
During this period, the digestive state of all
the Calanus changed from empty to full (Fig.
4E-H), which resulted in a first peak of mean
gut pigment (Fig. 4C, D). Then, the mean
gut content decreased (Fig. 4C, D), as most
of the copepods evacuated their guts (Fig.
4E-H). After this, a second period of feeding
activity is evidenced by a decrease in the
proportion
of the population with empty
guts in the two strata (Fig. 4F, H) and simultaneous increase in the mean gut content (Fig. 4C, D).
Relation with vertical migrations-The
bimodal feeding pattern raises the question
of why feeding should stop in the middle of
the night and start again before dawn. Haney and Hall (1975) suggested that the rate
of change in light intensity around dusk and
dawn could enhance the feeding activity of
daphnids. This hypothesis does not fit our
observations since the second period of
feeding activity and the corresponding migration to the upper stratum (Fig. 4B-H)
began before the presumed light signal, nor
does it explain twilight feeding rhythms in
the absence of light or temperature stimuli
(Chisholm et al. 1975; Duval and Geen
1976). The hunger-satiation
hypothesis for
vertical migrations (Conover 1968; Rudjakov 1970; Pear-r-e 1973, 1979) better explains the observed rhythm. According to
this hypothesis, the hungry copepods (empty gut) migrated to the upper stratum at dusk
for a first meal, became sated, and sank back
to depth while digesting and defecating before a second migration to the upper stratum for a predawn meal. The observed satiation in the presence of low phytoplankton
concentrations may be related to overwintering and the corresponding reduction of
digestive ability (Hallberg and Hirche 1980).
In situ grazing rhythms
In addition, the interruption of feeding during the night may be a consequence of feeding periodicity and the replenishment rate
of the prestored digestive enzyme pool (see
Head et al. 1984).
Gut content dynamics in the two strata
can be used as a tracer of vertical movements of copepods in and out of the feeding
layer (Pearre 1979) to show that a large part
of the Calanus population
underwent a
double migration to the surface layer during
the night (Fig. 4C-H). On the basis of the
decrease in copepods with empty guts (Fig.
4H), at least 27% of the population took
part in the second migration before dawn
on the first day and 22% on the second day.
This second migration
probably
corresponds to the so-called dawn rise, and it was
detected neither by net catches (Fig. 5D) nor
by the echosounder (Fig. 6). Another fact
which would have been overlooked without
gut content analysis is that all of the Calanus
population underwent vertical migrations.
Even if the maximum catch in the top stratum was 76% of the animals (Fig. 5D), all
of the individuals
migrated to the phytoplankton layer since, 2 h after surfacing of
the scattering layer, the number of copepods
with empty guts in the lower stratum had
declined to zero (Fig. 4H). This is in good
agreement with the hypothesis of Pearre
(1973, 1979) for chaetognaths, and its extension to copepods by Mackas and Bohrer
(1976), that vertical migration is not synchronous among individuals and that there
is a rapid vertical interchange of copepods
over the water column. As pointed out by
Pearre (1979), numbers alone cannot adequately describe the actual path of vertical
migrations.
The dusk ascent and dawn descent were
probably set by underwater light (inaccurately defined by sunset or sunrise) acting
as a vertically moving barrier for copepods,
as demonstrated by Forward et al. (1984)
for crab larvae. Time spent feeding in the
warmer surface layer was short and probably controlled by food requirements, which
can fluctuate seasonally, and possibly also
by food concentration (Bohrer 1980). The
large increase in the number of migrants on
the second day (Fig. 5C) did not change the
patterns of feeding and vertical migration.
605
Since the depth of copepods changes rapidly
with their feeding activity, as was suggested
by Mackas and Bohrer (1976) and Dagg and
Wyman (1983), gut contents at a given depth
are not necessarily related to the corresponding food concentration and therefore
must be interpreted with caution. Vertical
displacements across the temperature gradient during the night affect the gut clearance rate (Kiorboe et al. 1982; Dagg and
Wyman 1983) and metabolic activity, both
of which should be considered in modeling
the bioenergetics of vertical migrations (Nival et al. 1974; Enright 1977).
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Submitted: 1 December 1983
Accepted: 14 December 1984