Journal of Marine Systems 15 Ž1998. 503–509
Diel vertical migration and feeding in adult female Calanus
pacificus, Metridia lucens and Pseudocalanus newmani during a
spring bloom in Dabob Bay, a fjord in Washington USA
M.J. Dagg
a
a,)
, B.W. Frost
b,1
, J. Newton
c,2
Louisiana UniÕersities Marine Consortium, 8124 Highway 56, ChauÕin, LA 70344, USA
b
School of Oceanography, UniÕersity of Washington, Seattle, WA 98195, USA
c
Washington State Dep. of Ecology, 300 Desmond Dr., Olympia, WA 98504, USA
Accepted 26 September 1997
Abstract
Diel vertical migration and feeding on phytoplankton by adult female Calanus pacificus, Metridia lucens and
Pseudocalanus newmani were simultaneously measured near the end of a phytoplankton bloom. Almost the entire Calanus
population migrated out of the deep layer Ž108–50 m. at night but only about 30% came to the surface Ž25–0 m.. Feeding
occurred only at night and was equally high in the surface and intermediate layers, in spite of much higher food
concentrations in the surface. Like Calanus, the entire Metridia population was found in the deep layer during the day but
unlike Calanus, 20–50% remained in the deep layer at night and most migratory Metridia were collected from the surface
layer. Metridia feeding at night was highest in the surface layer but significant feeding also occurred in both the
intermediate and deep layers. Migratory behavior of Pseudocalanus was weak, with the proportion of the population in the
surface layer increasing from slightly - 10% during the day to approx 30% at night. Feeding occurred in both surface and
intermediate layers throughout the 24 h but was greater in both layers at night. The different migratory patterns are discussed
in the context of our current understanding of the contributions of predator avoidance and feeding to diel vertical migration.
q 1998 Elsevier Science B.V. All rights reserved.
Keywords: Copepoda; zooplankton; vertical migration; feeding
1. Introduction
There is strong evidence that predator risk is a
stimulus to diel vertical migration in zooplankton
Že.g. Bollens et al., 1992; Forward and Hettler, 1992.
)
Corresponding author. Fax: q1-504-8512874. E-mail:
[email protected]
1
Fax: q1-206-5436073. E-mail: [email protected]
2
F ax:
q 1 -3 6 0 -4 0 7 6 8 8 4 .
E -m a il:
[email protected]
and it has become widely accepted that migration to
dimly lit areas during daylight is made to avoid
visually orienting predators Žsee review by Haney,
1988.. However, the need to obtain food must also
contribute to migratory behavior or else phytoplankton-ingesting zooplankton would not return to the
surface layer. There is evidence that food and feeding affect the upward portion of the migratory cycle
Že.g. Forward and Hettler, 1992; Dagg et al., 1997..
As a consequence of differences in size, swimming behavior, pigmentation and physiological needs
0924-7963r98r$19.00 q 1998 Elsevier Science B.V. All rights reserved.
PII S 0 9 2 4 - 7 9 6 3 Ž 9 7 . 0 0 0 9 3 - 6
504
M.J. Dagg et al.r Journal of Marine Systems 15 (1998) 503–509
it is reasonable to expect adult females of Calanus
pacificus, Metridia lucens and Pseudocalanus newmani to respond differently to their predator and
food environments. Each presents a unique image to
potential predators. For example, differences in the
migratory behavior of similarly sized stages of C.
pacificus and M. lucens have been attributed to
differences in their susceptibilities to visually orienting predators ŽBollens et al., 1992; Osgood and
Frost, 1994a,b., and the reverse migration made by
the smallest of the three species, P. newmani, has
been attributed to predation pressure from normally
migrating invertebrate predators ŽOhman, 1990; Frost
and Bollens, 1992.. Less is known about the significance of food and feeding behavior to diel migration
but copepods must balance the risk of predator-induced mortality with the biological necessity of energetic gains from food ŽDagg, 1985; Gliwicz, 1986.,
and food availability should contribute to observed
patterns of diel vertical migration.
In this study, we provide a detailed description of
the relationship between diel vertical migration and
feeding on phytoplankton by adult female C. pacificus, M. lucens and P. newmani during a late-winter
phytoplankton bloom.
2. Methods and materials
The study was done in March 1991 at a station in
the northern part of Dabob Bay Ž47847.8X N,
122848.3X W., a fjord in Washington State, USA.
Water depth was 110 m.
From March 5 to 28, CTD casts were made at
approximately 6 h intervals. During each cast, water
was collected from discrete depths with Niskin bottles. An aliquot of the water from each bottle was
analyzed by fluorometry for chlorophyll concentration, after extraction of pigments with 90% acetone
ŽLorenzen, 1966..
Phytoplankton production was measured daily between March 5 and 28 by in situ 14 C incubations.
Water was collected from 100, 50, 30, 15, 7 and 1%
surface irradiance depths at 04:30 h, prior to first
light, and aliquots of 125 ml were inoculated with 3
mCi of NaH 14 CO 3 . For each depth, one dark and
two light bottles were suspended in situ and incubated for 24 h, from dawn to dawn. After retrieval,
aliquots from each bottle were filtered ŽGFrF.,
placed in scintillation vials containing Ecolume fluor,
and counted for 14 C activity.
On March 23r24, zooplankton samples were collected with a vertically hauled 1 m closing net Ž216
mm mesh. deployed at frequent intervals throughout
the night and less frequently during the day. During
each interval, samples were collected from three
depth strata: 108–50, 50–25 and 25–0 m. Each
series required about 30–40 min. Immediately after
each net haul came on board, a portion of the
cod-end contents was immersed in liquid nitrogen.
The remainder of the sample was preserved in a 10%
formalin-seawater solution.
In the laboratory, triplicate samples of 5 C. pacificus, 5 M. lucens and 10 P. newmani were sorted
under a dissecting microscope with light passed
through a red filter, and placed in a DMSO:acetone
mixture for pigment extraction ŽShoef and Lium,
1976.. Pigment content of copepods was calculated
by summing the chlorophyll and pheopigment contents ŽDagg et al., 1989.. Unused portions of frozen
samples were added to the appropriate formalin preserved samples. Formalin preserved samples were
split with a Folsom splitter and copepods were enumerated.
3. Results
There was a phytoplankton bloom prior to our
zooplankton sampling on March 23r24 ŽFig. 1..
Chlorophyll stocks during the bloom peak, from
March 15 to 20, were typically between 300 and 400
mg my2 and maximum concentrations were ) 20
mg my3 in subsurface waters at approximately 10 m.
As the bloom progressed, the phytoplankton-rich
layer broadened and deepened, indicating some sinking was occurring ŽFig. 1.. On March 23r24, stocks
were between 140 and 250 mg my2 and concentrations in the upper 25 m were typically between 2 and
10 mg my3 . Moderately high concentrations of phytoplankton were observed at intermediate depths,
with concentrations between 0.5 and 3 mg my3 at
25–45 m, and ) 1 mg my3 at 60 m. On March
23r24, average stock in the 25–50 m stratum was
38.2 mg chlorophyll my2 , 25% of the total stock in
the upper 50 m. During this entire late-winter bloom,
thermal stratification was weak or non-existent.
M.J. Dagg et al.r Journal of Marine Systems 15 (1998) 503–509
505
Fig. 1. The phytoplankton bloom of March 6–28, 1991, as indicated by extracted chlorophyll. This bloom was dominated by the chain
forming diatom, Thalassiosira pacifica. Dates of detailed zooplankton sampling are indicated by the arrow.
Integrated phytoplankton production between
March 22 and 25 averaged 1632 mg C my2 dy1 ,
equivalent to 36.3 mg chlor my2 dy1 , assuming a
C:chl ratio of 45 ŽDowns and Lorenzen, 1985.. The
productivity maximum was between 3 and 6 m and
virtually no production occurred below 15 m.
The migratory behavior and gut pigment content
of each copepod during March 23r24 are shown in
Figs. 2–4.
3.1. Calanus pacificus (Fig. 2)
One hundred percent of the population was in the
deep layer during daylight h. Essentially all females
had migrated out of the deep layer by 20:00 h.
During the night, a maximum of 10% of the popula-
tion was found in the deep layer at 00:40 h. In the
early morning, there was a rapid descent and by
07:05 h virtually all the population was again in the
deep layer. At night, a significant portion of the
population migrated into the surface layer but, with
one exception, the larger portion Ž50–69%. was
found in the intermediate layer. The exception was in
the early morning at 03:30 h, immediately prior to
descent back into the deep layer, when almost 80%
of the population was in the upper 25 m.
In the intermediate layer, gut pigment levels were
low Žmean s 8.1 ng copepody1 . during the early
ascent phase Ž17:40 h. but increased to a high level
Ž30.9 ng copepody1 . during the next hour. Thereafter, gut pigment levels in this layer remained high
throughout the night, averaging 30.2 ng copepody1
506
M.J. Dagg et al.r Journal of Marine Systems 15 (1998) 503–509
3.2. Metridia lucens (Fig. 3)
One hundred percent of the population was in the
deep layer during the pre-sunset sampling intervals.
Over the next 3 h, a large fraction of the population
migrated out of the deep layer and into the surface
layer; at 20:00 h the population was split between
the surface layer Ž; 80%., and the deep layer Ž;
20%., with no animals in the intermediate layer. As
the night progressed, the proportion in the surface
layer decreased, a fairly constant fraction of the
population remained in the intermediate layer, and
the proportion in the deep layer increased; the entire
population seemed to drift deeper. Prior to the predawn descent, the population again split entirely
between the deep and surface layers Ž; 50:50.. By
06:00 h, the entire population was in the deep layer.
Gut pigment levels were highest in the surface
layer. High concentrations Ž8–10 ng copepody1 .
coincided with or slightly preceded the two periods
Fig. 2. Calanus pacificus females. Diel vertical migration Žtop.
and gut pigment contents Žbottom. in the 108–50 m
Žv
v ., 50–25 m ŽI— — —I. and 25–0 m Ž`- -`. depth strata. The abundance of C. pacificus females in the
water column, determined by summing the abundance in each
stratum, ranged between 3758 and 10,850 my2 , with an average
of 6958 my2 .
Ž n s 21, sd s 11.4.. Gut pigment levels in the surface layer were also high throughout the night. The
mean of 26.2 ng copepody1 Ž n s 18, sd s 14.6. was
not significantly different from the mean in the
intermediate layer. In contrast to individuals collected in the intermediate layer during initial ascent,
copepods in the surface layer contained high levels
of pigment when they first appeared at 19:00 h,
suggesting they were feeding in the intermediate
layer while transiting through to the surface layer.
There were no discernable patterns in gut fullness
during the night in either the intermediate or surface
layers. Gut pigment levels in the deep layer were
lowest in the afternoon, prior to population ascent,
and remained low during the early evening, when
almost all the population was in the upper two strata.
Highest levels of gut pigment were observed in the
deep layer at the onset of the descent phase Ž04:45
h., suggesting that descending copepods carried a
portion of their gut contents into the deep layer.
Fig. 3. Metridia lucens females. Diel vertical migration Žtop. and
gut pigment contents Žbottom. in the 108–50 m Žv
v .,
50–25 m ŽI— — —I., and 25–0 m Ž`- - -`. depth strata.
The abundance of M. lucens females in the water column,
determined by summing the abundance in each stratum, ranged
between 510 and 1401 my2 , with and average of 961 my2 .
M.J. Dagg et al.r Journal of Marine Systems 15 (1998) 503–509
of highest copepod concentration in the surface layer,
suggesting highest feeding activity just after
sunsetrascent and just before dawnrdescent. Low
levels of gut pigment Ž2–4 ng copepody1 . were
present in the intermediate and deep layers during all
sampling periods, suggesting a low but continuous
rate of ingestion of pigment containing particles.
3.3. Pseudocalanus newmani (Fig. 4)
The largest portion of the population, approximately half, was in the intermediate layer at all
times. The proportion of the population in the surface layer mirrored the proportion in the deep layer;
as the proportion in the surface layer increased at
night, it decreased in the deep layer. The simplest
explanation for this pattern is a weak diel migration
of the entire population, a population spread vertically over a broad depth range centered in the intermediate layer.
Fig. 4. Pseudocalanus newmani females. Diel vertical migration
Žtop. and gut pigment contents Žbottom. in the 108–50 m
Žv
v ., 50–25 m ŽI— — —I., and 25–0 m Ž`- -`. depth strata. The abundance of P. newmani females in the
water column, determined by summing the abundance in each
stratum, ranged between 27,725 and 63,992 my2 , with an average
of 39,249 my2 .
507
Gut pigment levels in P. newmani females from
intermediate and surface layers appeared higher Ž1–2
ng copepody1 . than in copepods from the deep layer
Žapproximately 0.5 ng copepody1 . but deep data are
sparse. There were no clear differences between gut
pigment levels in the surface and intermediate layers.
Levels in both layers appeared to be higher at night
but some pigment was observed at all times, indicating some feeding occurred throughout the day.
4. Discussion
After at least 2 decades of accumulated evidence,
it should be accepted that downward diel migration
of copepods during daytime is a response to visually
orienting predators. It would therefore seem that
these three copepods are responding in similar but
not identical ways to predators during this study. C.
pacificus and M. lucens both completely avoid the
upper 50 m during daylight hours although the early
morning descent of M. lucens is more rapid than
that of C. pacificus. This was also observed in late
summer ŽDagg et al., 1989., when some C. pacificus
remained in the surface waters for as long as 2 h
after dawn but M. lucens did not. P. newmani, the
smallest of the three copepods, did not migrate as
deeply as the other two copepods during daylight,
and was approximately equally divided between the
intermediate layer Ž25–50 m., and the deep layer
Ž108–50 m..
Nocturnal ascent was observed in all three copepods but patterns were not identical. In C. pacificus,
upward migration out of the deep layer was almost
complete at night but, with one exception, more
individuals were in the intermediate layer than in the
surface layer. This did not appear to affect their
feeding on phytoplankton because gut pigment levels
were not significantly different in the two layers.
This is more fully discussed in Dagg et al. Ž1997..
M. lucens also showed a strong nocturnal migration out of the deep layer, with a maximum of 80%
of the population in the upper 50 m during early
evening. In contrast to C. pacificus, migrating M.
lucens did not stop in the intermediate layer but
moved right up into the surface layer in the early
evening. Individuals in the surface and intermediate
508
M.J. Dagg et al.r Journal of Marine Systems 15 (1998) 503–509
layers drifted deeper through the night, until the
pre-descent sampling when again there was a movement of migrants into the surface layer. Phytoplankton ingestion was high only in the surface layer and
peaked in the early evening and early morning,
during periods of strong surface-directed migration.
Some ingestion of pigment containing particles in
intermediate and deep layers occurred at all times.
The proportion of the P. newmani population in
the deep layer decreased from a maximum of about
50% during the day to a minimum of about 10%
during the night, indicating an upward migration.
The proportion of the population that left the deep
layer at night was approximately equal to the increase in the surface layer, suggesting a gradual
upward shift in the entire population although it is
possible that the deep water organisms were migrating to the surface while the bulk of the population
remained stationary in the intermediate layer. Phytoplankton ingestion was similar in the surface and
intermediate layers, was elevated at night, and appeared higher than in deep layer.
Without a good characterization of the predator
field for each copepod, it is not possible to directly
attribute differences in the daytime distributions of
these three copepods to predation risk. However, the
relatively shallow daytime distribution of P. newmani is consistent with its smaller size, and consequently with a reduced vulnerability to visually orienting predators ŽOhman, 1990..
Other differences are not easily explained on the
basis of size. In spite of its smaller size, the morning
descent from the surface by M. lucens is more rapid
than it is for the larger C. pacificus. This was also
observed in Dagg et al. Ž1989., and is discussed but
not explained in Bollens and Frost Ž1989..
The effects of feeding on the ascent phase of diel
vertical migration and on the nighttime distribution
of migrants is becoming increasingly recognized Že.g.
Forward and Hettler, 1992; Dagg et al., 1997..
Species that feed by particle filtration and are therefore predominantly herbivorous during blooms,
should respond in some fashion to the distribution of
phytoplankton. During this cruise, which occurred at
the end of a large phytoplankton bloom, phytoplankton concentrations were highest in the upper 25 m
but still significant in the 25–50 m layer. For C.
pacificus and P. newmani, more than half the popu-
lation of each species typically remained in the
intermediate layer and did not migrate to the surface
layer at night. In both copepods, feeding was as
strong in the intermediate layer as in the surface
layer, in spite of higher phytoplankton concentrations
in the surface. For these two copepods it appears the
upward migration, motivated by hunger, can be interrupted anywhere in the water column that suitable
feeding conditions are encountered, and that individuals vary in their perception of suitable feeding
conditions. In contrast, M. lucens feeding on phytoplankton was strongest in the surface layer and mainly
associated with the two times of night when copepods had actively migrated into the surface layer. M.
lucens is typically considered more omnivorous than
C. pacificus or P. newmani ŽArashkevich, 1969.. In
M. lucens, gut pigment patterns may be good indicators of the time, depth and strength of feeding but
foods other than phytoplankton, such as copepod
eggs or protozoans, may be the important stimuli for
upward vertical movement.
Copepods are complex organisms. They must balance the risk of predator-induced mortality with the
biological necessity of energetic gains from food
ŽDagg, 1985; Gliwicz, 1986.. Because each species
integrates these and perhaps other factors in a unique
way, species differences in diel migratory behavior
under identical conditions should be expected.
Acknowledgements
This work was supported by NSF Grant OCE
8917672 to MJD and NSF Grant OCE-8917671 to
BWF.
References
Arashkevich, Y.G., 1969. The food and feeding of copepods in
the northwestern Pacific. Oceanology 9, 695–709.
Bollens, S.M., Frost, B.W., 1989. Zooplanktivorous fish and
variable diel vertical migration in the marine planktonic copepod Calanus pacificus. Limnol. Oceanogr. 34, 1072–1083.
Bollens, S.M., Frost, B.W., Thoreson, D.S., Watts, S.J., 1992.
Diel vertical migration in zooplankton: a field test of the
predator avoidance hypothesis. Hydrobiologia 234, 33–39.
Dagg, M.J., 1985. The effects of food limitation on diel migratory
behavior in marine zooplankton. Arch. Hydrobiol. Beih.
Ergebn. Limnol. 21, 247–255.
M.J. Dagg et al.r Journal of Marine Systems 15 (1998) 503–509
Dagg, M.J., Frost, B.W., Walser, W.E. Jr., 1989. Copepod diel
migration, feeding and the vertical flux of pheopigments.
Limnol. Oceanogr. 34, 1062–1071.
Dagg, M.J., Frost, B.W., Newton, J.A., 1997. Vertical migration
and feeding behavior of Calanus pacificus females during a
phytoplankton bloom in Dabob Bay. USA. Limnol. Oceanogr.
42, 974–980.
Downs, J.N., Lorenzen, C.J., 1985. Carbon:pheopigment ratios of
zooplankton fecal pellets as an index of herbivorous feeding.
Limnol. Oceanogr. 30, 1024–1036.
Forward, R.B. Jr., Hettler, W.F. Jr., 1992. Effects of feeding and
predator exposure on photoresponses during diel vertical migration of brine shrimp larvae. Limnol. Oceanogr. 37, 1261–
1270.
Frost, B.W., Bollens, S.M., 1992. Variability of diel vertical
migration in the marine planktonic copepod Pseudocalanus
newmani in relation to its predators. Can. J. Fish. Aquat. Sci.
49, 1137–1141.
Gliwicz, M.Z., 1986. Predation and the evolution of vertical
migration in zooplankton. Nature 320, 746–748.
509
Haney, J.F., 1988. Diel patterns of zooplankton behavior. Bull.
Mar. Sci. 43, 583–603.
Lorenzen, C.J., 1966. A method for the continuous measurement
of in vivo chlorophyll concentration. Deep-Sea Res. 13, 223–
227.
Ohman, M.D., 1990. The demographic benefits of diel vertical
migration by zooplankton. Ecol. Monogr. 60, 257–281.
Osgood, K.E., Frost, B.W., 1994a. Ontogenetic diel vertical migration behaviors of the marine planktonic copepods Calanus
pacificus and Metridia lucens. Mar. Ecol. Prog. Ser. 104,
13–25.
Osgood, K.E., Frost, B.W., 1994b. Comparative life histories of
three species of planktonic calanoid copepods in Dabob Bay,
Washington. Mar. Biol. 118, 627–636.
Shoef, W.T., Lium, B.W., 1976. Improved extraction of chlorophyll a and b from algae using dimethylsulfoxide. Limnol.
Oceanogr. 21, 926–928.