Deep-Sea Research II 48 (2001) 1063}1068
Diel changes in the near-surface biomass of zooplankton and
the carbon content of vertical migrants
Graeme C. Hays *, Roger P. Harris, Robert N. Head
School of Biological Sciences, University of Wales Swansea, Singleton Park, Swansea SA2 8PP, UK
Plymouth Marine Laboratory, Prospect Place, Plymouth PL1 3DH, UK
Received 28 August 1997; received in revised form 23 February 1998; accepted 5 August 1998
Abstract
Zooplankton biomass and the carbon content of vertical migrants were measured in the NE Atlantic
(36.53N, 19.23W) between 11 and 18 July 1996 as part of the Plankton Reactivity in the Marine Environment
(PRIME) programme. The increase in zooplankton biomass near the surface (0}100 m) at night compared to
during the day suggested that diel vertical migration was an important feature at this site. For three species of
vertically migrant copepods, Pleuromamma pisekii, P. gracilis and P. abdominalis, the carbon content of
individuals collected at dusk was signi"cantly less than for individuals collected at dawn, with this reduction
being 6.2, 7.3 and 14.8%, respectively. This dawn}dusk reduction in carbon content is consistent with the diel
pattern of feeding and fasting exhibited by vertical migrants and supports the suggestion that migrating
zooplankton will cause an active export of carbon from the surface layers. 2001 Elsevier Science Ltd. All
rights reserved.
It has been suggested that signi"cant loss of material from near the ocean surface may be
mediated by the diel vertical migration (DVM) of zooplankton, although quantifying this rate
directly is problematic (Longhurst and Harrison, 1989). For oceanic zooplankton, the amplitude of
DVM may be several hundreds of meters, with deep daytime fasting and shallower nighttime
feeding. While zooplankton are feeding at night, there will be a net #ow of material into their bodies
(through ingestion and assimilation) and, during the day there will be a net #ow of material out of
their bodies due to excretion, defecation and respiration (Atkinson et al., 1996; Dagg et al., 1989;
Dam et al., 1995; Longhurst and Harrison, 1988, 1989; Longhurst et al., 1989, 1990). We have
recently argued that it should be possible to quantify directly the vertical #uxes caused by DVM by
measuring the diel change in the elemental content of migrating species (Hays et al., 1997b). As
a consequence of the net #ow of material into migrating animals during the night and out of them
* Corresponding author. Fax: #44-1792-295447.
E-mail address: [email protected] (G.C. Hays).
0967-0645/01/$ - see front matter 2001 Elsevier Science Ltd. All rights reserved.
PII: S 0 9 6 7 - 0 6 4 5 ( 0 0 ) 0 0 1 0 9 - 0
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G.C. Hays et al. / Deep-Sea Research II 48 (2001) 1063}1068
during the day, their elemental content should decrease progressively during the day and reach
a minimum just prior to their onset of feeding around dusk, and should increase progressively
during the night to reach a maximum around dawn when they cease feeding. Thus, the di!erence
between the dusk minimum and dawn maximum should represent the amount of material exported
daily by each species. The vertical distance through which this material is exported will vary. For
example, material that is excreted, respired and defecated during the descent at dawn may only be
transported through a few 10s of metres, while material that is excreted, respired and defecated at
the daytime residence depth may be transported through several hundreds of metres.
The Plankton Reactivity in the Marine Environment (PRIME) cruise in the NE Atlantic in 1996
provided us with our "rst opportunity to implement this technique, and we have already reported
the diel change in the nitrogen content for vertical migrants on this cruise (Hays et al., 1997a). Here
we consider whether DVM may have induced important vertical carbon #uxes. We "rst examine
the diel patterns of near-surface size-fractionated zooplankton biomass to establish whether
vertical migration was an important feature within this ecosystem as a whole, and second we
quantify the carbon content of individual migrant species to see if the dawn-dusk changes predicted
from a diel pattern of feeding and fasting were evident.
Sampling took place between 11 and 18 July 1996 (days of the year 193}200) at 36.53N, 19.23W
close to a drogued drifting buoy that was deployed at the start of the time series. This sampling
period constituted the `southern time-series stationa on the PRIME cruise. The biomass of the
zooplankton community was assessed using standard JGOFS protocols (Anon, 1989) that have
routinely been used previously (e.g. Morales et al., 1991). In short, zooplankton were collected by
vertical tows from 100 m to the surface using a WP-2 net of 200 lm mesh size. Nets were deployed
around local midnight and local midday. Upon retrieval of the net, the contents were wet-sieved to
obtain three size fractions (200}500, 500}1000 and 1000}2000 lm). Each size fraction was then
made up to a volume of 1000 ml, and 3;50 ml sub-samples taken for subsequent analysis on
a Carlo Erba NA1500 elemental analyzer.
Zooplankton for elemental analysis were collected between 11 and 18 July 1996 using a 500 lm
WP-2 net hauled vertically between 200 m and the surface. The times of sunset and sunrise during
the study were 20:30 and 06:15 h, respectively (all times in the text are given as Greenwich Mean
Time). Sampling was focused around dusk (net deployments took place between 20:00 and 21:30 h)
and just prior to dawn (net deployments took place between 04:30 and 05:50 h) when the minima
and maxima in carbon levels were predicted. As soon as the net was retrieved, the catch was sorted,
animals were placed into tin capsules (Elemental Microanalysis Limited), and then frozen at
!203C for subsequent analysis on a Carlo Erba NA1500 elemental analyzer.
Throughout the sampling period, there was a strong diel signal in the zooplankton biomass, with
higher levels of biomass at night (Fig. 1a). The mean biomass was 2.05 mg C m\ at night and
1.42 mg C m\ during the day, a di!erence that was highly signi"cant (t-test, t "3.26, P(0.01).
This diel signal appeared most evident in the two largest size fractions (500}1000 and
1000}2000 lm) where the day}night increase was signi"cant (one-sided t-test, t "2.71, P(0.01
and t "2.67, P(0.01, respectively) and was less evident in the smallest size fraction
(200}500 lm) where the day}night increase was not signi"cant (one-sided t-test, t "0.073,
P"0.07) (Fig. 1b}d).
The number of samples and the number of animals for which carbon content was determined for
the di!erent species are detailed in Table 1. For three of the species, P. pisekii, P. gracilis and P.
G.C. Hays et al. / Deep-Sea Research II 48 (2001) 1063}1068
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Fig. 1. The temporal and diel pattern in zooplankton biomass (mg C m\). *"day and 䢇"night. (a) All size fractions
combined; (b) size fraction 200}500 lm; (c) size fraction 500}1000 lm; (d) size fraction 1000}2000 lm.
Table 1
The number of samples and number of individuals (more than 1 individual typically occurred in each sample to give
su$cient material for elemental analysis) and the mean carbon content (lg C ind\) for di!erent Pleuromamma spp
Species
No. samples
No. individuals
lg C ind\
SD
P.
P.
P.
P.
P.
25
27
6
32
7
324
379
56
148
10
23.0
19.8
17.7
99.9
255.6
1.8
2.0
2.2
18.1
21.2
pisekii
gracilis
borealis
abdominalis
robusta
abdominalis, we collected su$cient samples to examine whether there was a signi"cant dawn}dusk
di!erence in carbon content. For all three species, the carbon content at dusk was signi"cantly less
than the carbon content at dawn, with the decrease being 6.2, 7.3 and 14.8%, respectively (Fig. 2).
Zooplankton diel vertical migration is commonly observed in oceanic areas, and our results
show that DVM was a strong feature of the southern time-series station on the PRIME cruise. It is
well known that copepods of the genus Pleuromamma are an important component of the migrant
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G.C. Hays et al. / Deep-Sea Research II 48 (2001) 1063}1068
Fig. 2. The mean body carbon content (#1 SE) for individuals collected at dawn (solid bars) and at dusk (hatched bars)
for P. pisekii, P. gracilis and P. abdominalis. For all three species the mean carbon content at dawn was signi"cantly
greater than the mean content at dusk (one-sided t-test, t "2.1, P"0.02; t "2.0, P"0.03; t "2.4, P"0.01,
respectively) with the decrease in carbon content being 6.2, 7.3 and 14.8%, respectively.
community in the Atlantic (e.g. Roe, 1984; Longhurst et al., 1989), and certainly several species of
this genus were evident in our samples. We have previously characterised the extent of DVM
within zooplankton communities through an index termed the `Mean Community DVMa, which
is calculated as (mean night biomass!mean day biomass)/mean night biomass. At the PRIME
southern time-series station, the di!erence between the mean zooplankton biomass at night
(2.05 mg C m\) and during the day (1.42 mg C m\), gives a value for the mean community DVM
of 0.31. This "gure lies within the middle of the range we have previously reported for the NE
Atlantic (as far south as 453N) using historically collected data from the Continuous Plankton
Recorder survey (Hays, 1996). The implication is that the extent of DVM we observed on the
PRIME cruise is typical compared to other measurements in the NE Atlantic.
Examination of the diel change in the biomass of di!erent size-fractions revealed that DVM
occurred most strongly in larger animals. This is a widely reported observation (e.g. Rodriguez and
Mullin, 1986), which has been explained by the greater susceptibility of larger animals to visual
predators and hence their increased need to descend and spend the daytime at darker depths.
Given the strong DVM within the community as a whole, if migrants did export carbon from the
surface layers, their biogeochemical impact at the PRIME southern time-series station may have
been important. Longhurst et al. (1990) determined the respiration rate for migrating mesozooplankton (dominated by Pleuromamma) in the North Atlantic. During the daytime at a temperature
of 163C (i.e. similar to the temperature below the thermocline in our study) the respiration rate was
conservatively estimated at 2.3 lg C mg dry wt h\. This would give a loss of 32.8 lg C mg dry wt
during 14.25 h below the thermocline (the length of the day in our study), which, assuming that
carbon was 44% of the dry weight (Longhurst and Harrison, 1988), equals 7.5% of the body
carbon. The magnitude of the diel di!erence in zooplankton carbon content that we found (6.2, 7.3
and 14.8% for P. pisekii, P. gracilis and P. abdominalis, respectively) is broadly similar to this value
of 7.5% estimated from respiration rates and, therefore our results lend further support to the
existence of an active C-#ux.
A problem (discussed in Hays et al., 1997a) with the integrated tows that we used to collect
Pleuromamma spp. for elemental analysis, is that the exact depth of the animals is not known.
G.C. Hays et al. / Deep-Sea Research II 48 (2001) 1063}1068
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Potentially, therefore, in our dawn samples we may have collected animals from near the surface
with full guts and then defecation may have occurred prior to the animals' departure from the
surface. If this was the case, then our samples would overestimate the rate of the active C-#ux.
However, the long gut passage time for vertical migrants (Atkinson et al., 1996; Morales et al., 1993)
and the rapid vertical movements during migration (Enright, 1977) lead to the conclusion that
there will be relatively little emptying of their guts at their nighttime feeding depth. Nevertheless,
a better sampling strategy for future studies would clearly be to deploy appropriate nets that allow
collection of animals from discrete depth strata.
In conclusion, our observations suggest that diel vertical migration was an important feature of
the zooplankton community at the southern-time series station during the PRIME cruise and that
vertical migrants may have caused a signi"cant removal of carbon from the surface layers.
Important objectives must now be to quantify the active C-#ux for other species and to incorporate
this #ux into marine ecosystem models.
Acknowledgements
We thank the Chief Scientist on the PRIME cruise, Graham Savidge, for allowing us to sample
in the busy cruise schedule even though this work was not a funded part of the PRIME programme
and Ian Joint for his keen interest in our development of the technique for measuring the active
C-#ux. This is PRIME contribution number 50.
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