Journal of Plankton Research Vol.21 no.9 pp.1799–1808, 1999
SHORT COMMUNICATION
Carbon and nitrogen fluxes in the oceans: the contribution by
zooplankton migrants to active transport in the North Atlantic
during the Joint Global Ocean Flux Study
Carmen E.Morales
Estación de Biología Marina, Departamento Oceanografía, Universidad de
Concepción, Casilla 44, Dichato, VIII Región, Chile
Abstract. The role of vertical migrant zooplankton, with both seasonal/ontogenetic and daily strategies, in the active transport of carbon and nitrogen out of the surface layer in the North Atlantic is
analysed. The data used were obtained mainly during the Joint Global Ocean Flux Study
(JGOFS)–North Atlantic Bloom Experiment (NABE) (1989–1990) in the North Atlantic and from
published information on the biochemical composition of the dominant genera/species. The resulting
estimates of active transport are compared with the values of sedimentation rates at the
JGOFS–NABE stations and other sites in the North Atlantic. The estimates obtained support
previous findings indicating that active transport, especially by interzonal diel migrants, should be
taken into account in the estimation of total carbon and nitrogen export flux. The contribution of
seasonal migrants to carbon export flux, however, has been considerably underestimated before,
although it appears to be significantly lower compared to that of diel migrants. Biomass estimates and
biochemical composition, together with mortality and metabolic rates, should be investigated in
further detail for some of the dominant species in oceanic areas in order to evaluate active transport
more precisely.
The sequestration of carbon (C) in the oceans via the biological pump (Longhurst
and Harrison, 1989; Shaffer, 1993) was initially conceived and modelled basically
in terms of photosynthetic capacity, the structure and dynamics of epipelagic
assemblages, the supply of allochthonous nutrients into the photic zone, and the
sedimentation of organic matter from the photic zone or export flux (Legendre
and Le Fevre, 1989; Longhurst, 1989). During the 1990s, a series of multidisciplinary studies has focused on the assessment of C and nitrogen (N) fluxes in different regions of the world oceans, with emphasis on the magnitude of the export
flux from the surface layer [i.e. the Joint Global Ocean Flux Study (JGOFS)
programme]. These studies have incorporated many other oceanographic variables and appropriate methods have been developed (e.g. Najjar et al., 1992;
Aksnes and Wassman, 1993; Ducklow and Harris, 1993).
It is only more recently that active transport by vertical migrants has been
incorporated into export flux via the biological pump. Longhurst and Harrison
(1989) suggested that active transport leads to a net export only if (i) the migrants
cross a barrier to vertical mixing (e.g. the pycnocline or nutricline) and (ii) the C
or N consumed above this barrier is released below it (diel migrants) or there is
a net biomass transfer below this barrier, during the resting phase (seasonal
migrants). The migrants moving across such a barrier are known as interzonal
migrants (Longhurst and Harrison, 1988; Flint et al., 1991), in contrast to the
zonal migrations (within a uniform layer) of many other zooplankton species
© Oxford University Press 1999
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C.E.Morales
(Longhurst and Harrison, 1989; Ohman, 1990). The idea of interzonal transport
of organic matter by migrants is not recent, but it has usually been considered to
be minimal (Tseytlin, 1982).
Longhurst et al. (1989, 1990) suggested that the active transport of C and N by
diel migrants, mostly in tropical and subtropical oceanic areas, is a significant
proportion of the total export flux (mean of ~20% compared to the sedimentation
rates or gravitational flux). Seasonal migrants, on the other hand, have been
suggested to contribute insignificantly to the export flux (<1% of the sedimentation rates) when actively migrating out of the surface layer after the spring bloom
at high latitudes in the North Atlantic area (Longhurst and Williams, 1992). The
more recent studies related to the role of active transport in export flux, including
zooplankton and nekton interzonal migrants, have shown that there are several
processes by which this can be achieved: mortality at depth (Longhurst and
Williams, 1992; Zhang and Dam, 1997), excretion at depth (Longhurst et al., 1989;
Dam et al., 1993, 1995a; Le Borgne and Rodier, 1997), respiration at depth
(Longhurst et al., 1990; Le Borgne and Rodier, 1997; Zhang and Dam, 1997) and
defaecation at depth (Morales et al., 1993; Atkinson et al., 1996).
This paper presents a review of estimates of biomass and rate processes of
interzonal migrant copepods (also referred to as strong migrants) which were
obtained during the cruises undertaken under the umbrella of the JGOFS–North
Atlantic Bloom Experiment (NABE), between 1989 and 1990. These data have
been combined with published information, mainly on the biochemical composition of the species or genera identified as performing or being able to perform
strong migrations, in order to convert all estimates to C and N pools and fluxes,
and to characterize the metabolic strategies of the migrants. Some of the previous
estimates of active transport in which important assumptions about the
parameters used to calculate the fluxes were made have been re-evaluated.
A comparison is made of the contribution of two types of interzonal vertical
migrants in the North Atlantic. The first type corresponds to populations where
the dominant behaviour is seasonal/ontogenetic migration, represented mainly
by Calanus finmarchicus, which is found at the higher latitudes and in the northwest Atlantic. These migrants overwinter at depth (>500 m) and rise to the
surface layer (<100 m) during the spring, the diel migration being unimportant
(Longhurst and Williams, 1979, 1992). The second type corresponds to strong diel
migrants, represented mainly by species of Pleuromamma (mainly P.robusta and
P.borealis) and Metridia spp. (most likely M.lucens), which are predominant at
the lower latitudes and in the northeast Atlantic. These migrants remain at depth
(>200 m) during the daytime and perform night excursions to the surface layer
(Longhurst and Williams, 1979; Hays, 1996). These types overlap in their latitudinal distribution, but their centres of distribution are different (Williams, 1988)
and they can display the different strategies in the same environment (Grovnik
and Hopkins, 1984; Atkinson et al., 1996).
Table I summarizes the biochemical composition of interzonal seasonal and
diel migrants and their main diets. Available data are still scarce and there is a
complete description of the seasonal variation in C and N content only for
C.finmarchicus (Tande, 1982); specific data are not available for each of the
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Contribution by zooplankton migrants to active transport
dominant species of diel migrants, but there are some for the species that do occur
in the North Atlantic. Tande (1982) reported, for the Balsfjorden in northern
Norway, that the seasonal migrant stage (copepodite V) of C.finmarchicus
showed a pronounced seasonal pattern in body weight and C content, in line with
the seasonality of food availability and the accumulation of long-term energy
reserves. In general, although differences in the biochemical composition have
been described (Bamstedt, 1986) for copepod species in low, medium and high
latitudes, and also between surface- and deeper-living species, more detailed
information about the body C and N contents and their variation in dominant
interzonal migrants should provide better estimates of the export flux. Recently,
Hays et al. (1997) have applied such an approach to analyse N active transport by
diel vertical migration of Calanus helgolandicus.
The biochemical composition of the migrant copepods is assumed to provide a
good indication of the different metabolic strategies adopted by the two types of
migrant. The need for seasonal migrants, adapted to seasonal phytoplankton
availability, to accumulate large, long-term reserves of lipids (mainly as wax esters)
may lead them to ingest food richer in C content. It may, therefore, be more advantageous for the stages which are preparing for migration (stage V) to feed on
phytoplankton blooms after the peak, when growth is entering the stationary
phase and the cells are producing and accumulating mainly carbohydrates.
Table I. Biochemical composition and feeding behaviour of the two main types of migrant copepod
species found in the North Atlantic. Data derived from the literature
Composition
Seasonal migrant
(Calanus finmarchicus)
at high latitudes
Diel migrant
(Pleuromamma/Metridia spp.)
at low latitudes
Body carbon (% DW)
48–78 copepodite V (1, 2)
55 adult, summer (3)
4–6 copepodite V (1, 2)
8 adult, summer (3)
8–23 copepodite V (1, 2)
47 (10)
Body nitrogen (% DW)
Body C/N ratio (w/w)
Total lipid content (% DW)
Main type of lipid accumulated
Main diet type
13 (8, 10)
4–6 (10)
5–7 (9)
70 (4)
5–8 adult (11)
50 adult (5)
4–33 adult (5)
16–31 copepodite V (6)
14–30 adult (12)
Wax esters (5, 7)
Triacylglycerols (5)
Predominately herbivorous (4,8) Omnivorous (4,13)
(1) Tande (1982).
(2) Bamstedt (1986).
(3) Ikeda and Skjoldal (1989).
(4) Sargent and Falk-Petersen (1988).
(5) Lee and Hirota (1973), Metridia sp., Pleuromamma abdominalis and P.xiphias.
(6) Bamstedt et al. (1990).
(7) Sargent and Falk-Petersen (1988).
(8) Lee et al. (1971b).
(9) Small et al. (1983), various copepod species in the large fraction (300–500 µm).
(10) Omori (1969), Pleuromamma xiphias.
(11) Morris and Hopkins (1983), Pleuromamma abdominalis and P.xiphias.
(12) Lee et al. (1971a), Pleuromamma abdominalis, P.xiphias and Pleuromamma spp.
(13) Bennet and Hopkins (1989), Pleuromamma abdominalis, P.piseki, P.xiphias and P.gracilis.
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C.E.Morales
In contrast, diel migrants accumulate lipids mainly of the rapid turnover type
(triacylglycerol) because they tend to feed continuously throughout the year, on
any food material available, in order to obtain enough N for continuous growth
and protein production. A higher variability in the C content and lipid reserves
of seasonal migrants, and the overwintering stages in particular, might therefore
be expected, in close association with the cycle of feeding during and following
the phytoplankton bloom. The information in Table I, though incomplete,
confirms the latter statement. In addition, the review presented by Ikeda (1974)
has shown that the variation in N content was smaller than that of C, relative to
dry weight (DW), among copepods from different latitudes and that the range of
C content was far narrower (35–48% of DW) for tropical and subtropical copepods compared with that of boreal copepods (38–67% of DW). These significant
variations in biochemical composition have to be kept in mind when calculating
the active transport by migrating zooplankton.
Table II presents data on the rates of phytoplankton consumption, evacuation
rate constants and defaecation rates measured in samples of Calanus (at higher
latitudes) and Pleuromamma/Metridia (at lower latitudes) during the
JGOFS–NABE experiment (Morales et al., 1991, 1993). It is important to stress
that, usually, the errors involved in zooplankton biomass assessments and specific
ingestion rates are not reported and, therefore, the estimation of consumption
rates represents only mean values. Even more so, the biomass estimates in terms
of C and N are usually assumed to be a constant factor of DW; a value of 32%
for converting DW to C was adopted by Longhurst and Williams (1992). In fact,
this is not the case in organisms performing seasonal migrations (e.g. C.finmarchicus), which have been reported (Bamstedt, 1986) to show about a 2-fold variation
during an annual cycle (Table I).
Table II. Estimates of consumption rates and related metabolic rates of seasonal and diel migrants
(late stages/adults), derived from data obtained during the JGOFS–NABE in the North Atlantic
(1989–1990)
Rates
Phytoplankton consumption
(mg C m–2 day–1)
Based on biomass estimates
(mg C m–2)
Seasonal migrant
(Calanus finmarchicus)
7 (1)
319 (2)
700 (3)
1933 (2)
Diel migrant
(Pleuromamma/Metridia spp.)
3–71 (1, 4)
313 (2)
5–49 (5)
400 (3)
1561 (2)
240–570 (5)
Evacuation rate constant
(h–1)
1.5–2.0 (1)
0.4–0.6 (4)
Defaecation rate
(number h–1)
1–3 (4)
0.2–0.5 (4)
(1) Morales et al. (1991).
(2) Lenz et al. (1993), ingestion rates were derived indirectly.
(3) Weeks et al. (1993), total mesozooplankton biomass.
(4) Morales et al. (1993).
(5) Dam et al. (1993).
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Contribution by zooplankton migrants to active transport
There are two estimates in Table II which require further inspection. First, the
consumption rates observed by Morales et al. (1991) for C.finmarchicus are rather
low compared to other direct or indirect measurements (range 31–319 mg C m–2
day–1) obtained for the same species in other studies (Smith and Lane, 1988; Lenz
et al., 1993). In fact, the individuals captured during the sampling were already
full of lipids, suggesting that they had fed well and were ready to migrate downwards. Second, both the evacuation rate constant and defaecation rate were
significantly lower (3–4 times) in the diel migrants than in the seasonal migrants.
Most evacuation rate measurements have not included strong diel migrants
and, therefore, it has been erroneously assumed that this rate was too fast to
involve any significant active transport of faeces down the water column
(Longhurst and Harrison, 1988; Dagg et al., 1989). This kind of detrital flux, on
the other hand, was supposed to be important in the oceans (Angel, 1984). A few
recent studies also support the observations of comparatively low evacuation
rates or longer gut residence times (3–5 times) in some other diel migrant
copepod species in the Pacific, Eucalanus inermis and Eucalanus elongatus (Flint
et al., 1990), and in the subantarctic area north of South Georgia, M.lucens and
P.robusta (Atkinson et al., 1996). Batchelder (1986) and Smith and Lane (1988)
have also reported lower evacuation rates in Metridia species.
Tables III and IV summarize data on C and N fluxes, emphasizing the contribution of active transport by migrant zooplankton, estimated during the
JGOFS–NABE (1989–1990), together with related published information.
Although C:N ratios could have been applied to obtain C or N equivalent fluxes
in all cases, this has not been done because of the uncertainties involved when
Table III. Calculation of carbon flux via active transport by seasonal migrants (mainly C.finmarchicus)
in the North Atlantic. Literature and JGOFS–NABE (1989–1990) data
Rates
Daily rates
(mg C m–2 day–1)
Annual rates
(g C m–2 year–1)
Primary production
(C:N = 6.6)
Sedimentation
452–1152 (1)
689 (2)
26 (2)
160 (3)
163–420
Active transport:
Zooplankton biomass:
85–346 mg C m–2 (4)
Mortality rate: 75%
C body: 32% DW
Corrections:
Max. value C body: 75% (5)
Max. biomass estimates:
700–2000 mg C m–2 (2, 3, 6)
10–58
0.26
0.61
0.5–1.5
(1) Joint et al. (1993).
(2) Lenz et al. (1993).
(3) Harrison et al. (1993).
(4) Longhurst and Williams (1992), 59ºN–19ºW (1971–1975).
(5) Tande (1982), Balsfjorden, Northern Norway (1976–1977).
(6) Weeks et al. (1993).
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C.E.Morales
dealing with metabolic rates in animals with different metabolic strategies. In the
case of the seasonal migrant, it is even more uncertain which C:N ratio to use due
to its wide variation (Table I); therefore, no N flux estimates are provided.
Table III analyses the contribution of the seasonal migrants, considering the
data provided by Longhurst and Williams (1992) which indicated that the C flux
by C.finmarchicus in the North Atlantic is a small number represented by their
mortality rates while overwintering at depth (>500 m). As mentioned before, two
assumptions must be kept in mind when considering this conclusion, which is
based on an estimate of average mortality of 75% and a long series of abundance
data from the area. (i) At the time of migrating downwards, stage V are reported
to contain up to 2.3 times more C (75% of DW; Tande, 1982) than the figure used
for the calculations (32% of DW). (ii) Maximum numbers/biomass reported in
the time series are lower than the maximum values reported in other occasional
studies (see Table III). In these terms, the average figure (0.26 g C m–2 year–1)
presented by Longhurst and Williams (1992) could increase significantly (2–6
times) if corrected for increases in body C content or higher maximum biomass
values, or a combination of both. It must also be noted that none of the losses of
C at depth via respiration are included since they should be integrated into the
mortality rate values.
Table IV. Calculation of the carbon and nitrogen fluxes via active transport by diel migrants (mainly
Pleuromamma and Metridia spp.) in the North Atlantic. Literature and JGOFS–NABE (1989–1990)
data
Rates
Daily rates
Annual rates
——————————————— ———————————————
(mg C m–2 day–1) (mg N m–2 day–1) (g C m–2 year–1) (g N m–2 year–1)
Primary production
(C:N = 6.6)
98–252 (1)
200–1100 (2)
689 (3)
237–538 (4)
20–24 (1)
315 (2)
1.5a (3)
Sedimentation (1, 2, 5)
Active transport:
Zooplankton biomass:
5–480 mg C m–2 (2, 3, 6, 7)
C—respiration
C—defaecation
N—excretion
15–167
116 (2)
9.4 (5)
5 (6)
3–11 (1)
105 (3)
6–41 (6)
0.9–21 (7)
5–61
(0.7)a 7–115
1.8–42
1–38
0.3–7.7
31 (2)
0.72 (6)
(1) Longhurst et al. (1990), North Atlantic sites (5; 1987–1988).
(2) Dam et al. (1993).
(3) Lenz et al. (1993).
(4) Joint et al. (1993).
(5) Longhurst et al. (1989), NFLUX study site (1988).
(6) Dam et al. (1995a), Bermuda JGOFS station (1990).
(7) Morales et al. (1991, 1993).
aExtreme low value not considered in the calculations.
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36–402
0.4–11
Contribution by zooplankton migrants to active transport
Taking into consideration the above corrections and the rates measured during the JGOFS–NABE experiment (Table III), seasonal migrants (mainly
C.finmarchicus in this case) could make a significantly higher contribution than
that previously reported by Longhurst and Williams (1992). Compared to the
concurrent annual C flux, however, the range of values (considering minimum
with minimum and maximum with maximum) for active transport still represents
only 3–5% of the sedimenting C and <1% of the primary C production in the
surface layer. These estimates could, however, be 2 or 3 times higher if the calculations of the annual rates of primary production and sedimentation are restricted
to the productive season (1/2–1/3 of the year). Similarly, low percentages of N
active transport will be expected as N body content is small (<10% of DW; Table
I). On the other hand, if most of the sedimenting material [as particulate organic
carbon (POC) and particulate organic nitrogen (PON)] is predominately
composed of copepod faecal pellets (Peinert et al., 1987; Harrison et al., 1993),
and if this is derived mostly from actively feeding Calanus in surface waters, then
the main contribution of the seasonal migrants to the export flux will be by gravitational flux rather than by active transport.
By comparison, the estimated contribution of diel migrants to C and N export
(Table IV) is substantially greater than that of seasonal migrants: 19–40% of the
sedimenting C, 22–26% of sedimenting N, and 4–11% of the C and 8–18% of the
N derived from primary production. Table IV integrates figures which have
already been calculated for a specific study as well as others derived from the
JGOFS–NABE study. The range of values obtained is higher than that previously
reported by Longhurst et al. (1989) for the exportation of N [as dissolved inorganic nitrogen (DIN); mainly ammonia] via excretion at NFLUX (8% of sedimenting N), but well in the range of those derived and summarized by these
authors in other areas. In terms of C export, the values reported here are also in
the range of those estimated by Longhurst et al. (1990) for C export via respiration (13–58% of sedimenting C). Similarly, Dam et al. (1995a) estimated that an
amount equivalent to 18–70% of the sedimenting POC was due to respiratory C
export by diel migrants at the JGOFS Bermuda Atlantic Time Series station and
that the active transport of DIN was equivalent to 17–82% of the PON flux. It
must be noted that the figures estimated in Table IV include the contribution of
C via defaecation, due to lower evacuation rates; this has been calculated assuming that the faecal C amounts to 30% of the consumption estimates in Table II
(or 70% assimilation efficiency).
In none of the above cases have mortality rates of diel migrants been taken into
account, but a recent study by Zhang and Dam (1997) concluded that active
downward transport via mortality C and respiratory C flux could represent
between 31 and 44% of the sedimenting C in the JGOFS Equatorial Pacific Study
(EqPac). Applying a similar figure (but considering only the medium and large
size fractions: 2.2–3.5 mg C m–2 day–1) to the case of the JGOFS–NABE study,
the mortality C export by diel migrants could, in addition, contribute between 1
and 11% of the sedimentary C and <1% of the primary production C. This contribution, however, is represented in part by the metabolic losses mentioned before
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C.E.Morales
if the diel migrants are preyed upon at depth and, therefore, it does not represent
a simple addition to the total estimate of active transport.
In terms of differences in the contribution to active flux by zooplankton under
different oceanic regimes, Le Borgne and Rodier (1997) concluded that the active
flux by migrants was more important in an oligotrophic area, whereas the contribution of zooplankton was mainly passive in the mesotrophic situation. On the
other hand, Small et al. (1987) suggested that, at an oligotrophic site, the faecal
pellets of mesozooplankton were a higher proportion of the sinking flux
compared to that in eutrophic waters. In addition, Dam et al. (1995b) support the
view that the contribution of mesozooplankton to export production, via faecal
pellet production, increases with the degree of oligotrophy of a system. Overall,
more studies of this type and a consideration of temporal changes are required
before these observations can be generalized.
The examples of calculations presented here indicate that active transport by
zooplankton species can be a significant proportion of the overall export fluxes
out of the surface layer in oceanic areas, more importantly so in lower latitudes
where food availability is lower but constant and the biomass is dominated by diel
migrants. Considering that the diel migrants in these areas also include larger
crustaceans and fish, it becomes even more important to take into account this
transport. It is most evident, however, that for more precise estimates of C and
N export flux in the oceans, basic knowledge of the biochemical composition of
the dominant species, its variation through an annual cycle, mortality rate data
and metabolic strategies observed, are also required. The two types of migration
behaviour and biochemical composition may represent the extremes in a
continuum of strategies adopted by copepod species undergoing vertical migration in oceanic environments.
Acknowledgements
The basis for this study was developed during the JGOFS programme in the UK,
and C.M. was supported at that time by the NERC Biogeochemical Ocean Flux
Study (BOFS) Programme (special topic grant) and the British Council and
Fundación Andes (Chile). Additional support for developing the ideas was
obtained through a FONDECYT grant (Nº 1930004) and more recently by the
FONDAP-Humboldt Programme and the University of Concepción (PI-981
12052-1 IN). The author is grateful to R.P.Harris for his support during the
JGOFS programme and to A.G.Davies for critically reading the manuscript. This
is a BOFS and FONDAP contribution.
References
Aksnes,D. and Wassmann,P. (1993) Modelling the significance of zooplankton grazing for export
production. Limnol. Oceanogr., 38, 978–985.
Angel,M.V. (1984) Detrital organic fluxes through pelagic ecosystems. In Fasham,M.J.R. (ed.), Flows
of Energy and Materials in Marine Ecosystems: Theory and Practice. Plenum Press, New York, pp.
475–516.
1806
Contribution by zooplankton migrants to active transport
Atkinson,A., Ward,P. and Murphy,E.J. (1996) Diel periodicity of Subantarctic copepods: relationships
between vertical migration, gut fullness and gut evacuation rate. J. Plankton Res., 18, 1387–1405.
Bamstedt,U. (1986) Chemical composition and energy content. In Corner,E.D.S. and O’Hara,S.C.M.
(eds), The Biological Chemistry of Marine Copepods. Oxford University Press, New York, pp. 1–58.
Bamstedt,U., Hakanson,J.L., Brenner-Larsen,J., Bjornsen,P.K., Geertz-Hansen,O. and Tiselius,P.
(1990) Copepod nutritional condition and pelagic production during autumn in Korsterfjorden,
western Sweden. Mar. Biol., 104, 197–208.
Batchelder,H.P. (1986) Phytoplankton balance in the oceanic subarctic Pacific: grazing impact of
Metridia pacifica. Mar. Ecol. Prog. Ser., 34, 213–225.
Bennet,J.L. and Hopkins,T.L. (1989) Aspects of the ecology of the calanoid copepod genus Pleuromamma in the eastern Gulf of Mexico. Contrib. Mar. Sci., 31, 119–156.
Dagg,M.J., Frost,B.W. and Walser,W.E. (1989) Copepod diel migration, feeding and the vertical flux
of phaeopigments. Limnol. Oceanogr., 34, 1062–1071.
Dam,H.G., Miller,C.A. and Jonadosttir,S.H. (1993) The trophic role of mesozooplankton at 47°N,
20°W during the North Atlantic Bloom Experiment. Deep-Sea Res. II, 40, 197–212.
Dam,H.G., Roman,M.R. and Youngbluth,M.J. (1995a) Downward export of respiratory carbon and
dissolved inorganic nitrogen by diel-migrant mesozooplankton at the JGOFS Bermuda time-series
station. Deep-Sea Res. I, 42, 1187–1197.
Dam,H.G., Zhang,X., Butler,M. and Roman,M.R. (1995b) Mesozooplankton grazing and metabolism
at the equator in the central Pacific: implications for carbon and nitrogen fluxes. Deep-Sea Res. II,
42, 735–756.
Ducklow,H.W. and Harris,R.P. (1993) Introduction to the JGOFS North Atlantic Bloom Experiment.
Deep-Sea Res. II, 40, 1–8.
Flint,M.V., Drits,A.V. and Pasternak,A.F. (1991) Characteristic features of body composition and
metabolism in some interzonal copepods. Mar. Biol., 111, 199–205.
Grovnik,S. and Hopkins,C.C.E. (1984) Ecological investigations of the zooplankton community of
Balsfjorden, northern Norway: generation cycle, seasonal vertical distribution, and seasonal variations in body weight and carbon and nitrogen content of the copepod Metridia longa (Lubbock).
J. Exp. Mar. Biol. Ecol., 80, 93–107.
Harrison,W.G., Head,E.J.H., Horne,E.P.W., Irwin,B., Li,W.K.W., Longhurst,A.R., Paranjape,M. and
Platt,T. (1993) The western North Atlantic Bloom experiment. Deep-Sea Res. II, 40, 279–305.
Hays,G.C. (1996) Large-scale patterns of diel vertical migration in the North Atlantic. Deep-Sea Res.
I, 43, 1601–1615.
Hays,G.H., Harris,R.P., Head,R.N. and Kennedy,H. (1997) A technique for the in situ assessment of
the vertical nitrogen flux caused by the diel vertical migration of zooplankton. Deep-Sea Res., 44,
1085–1089.
Ikeda,T. (1974) Nutritional ecology of marine zooplankton. Memoirs of the Faculty of Fisheries,
Hokkaido University, 22, 1–97.
Ikeda,T. and Skjoldal,H.R. (1989) Metabolism and elemental composition of zooplankton from the
Barents Sea during early Arctic summer. Mar. Biol., 100, 173–183.
Joint,I., Pomroy,A., Savidge,G. and Boyd,P. (1993) Size fractionated primary productivity in the
northeast Atlantic in May-July 1989. Deep-Sea Res. II, 40, 423–440.
Le Borgne,R. and Rodie,M. (1997) Net zooplankton and the biological pump: a comparison between
the oligotrophic and mesotrophic equatorial Pacific. Deep-Sea Res. II, 44, 2003–2023.
Lee,R.F. and Hirota,J. (1973) Wax esters in tropical zooplankton and nekton and the geographical
distribution of wax esters in marine copepods. Limnol. Oceanogr., 18, 227–239.
Lee,R.F., Hirota,J. and Barnett,A.M. (1971a) Distribution and importance of wax esters in marine
copepods and other zooplankton. Deep-Sea Res., 18, 1147–1165.
Lee,R.F., Nevezel,J.C. and Paffenhofer,G.A. (1971b) Importance of wax esters and other lipids in the
marine food chain: phytoplankton and copepods. Mar. Biol., 9, 99–108.
Legendre,L. and Le Fevre,J. (1989) Hydrodynamic singularities as controls of recycled versus export
production in the oceans. In Berger,W.H., Smetacek,V.S. and Wefer,G. (eds), Productivity of the
Ocean: Present and Past. Wiley and Sons, Chichester, pp. 49–63.
Lenz,J., Morales,A. and Gunkel,J. (1993) Mesozooplankton standing stock during the North Atlantic
spring bloom study in 1989 and its potential grazing pressure on phytoplankton: a comparison
between low, medium and high latitudes. Deep-Sea Res. II, 40, 559–572.
Longhurst,A.R. (1989) Pelagic ecology: definition of pathways for material and energy flux. In
Dennis,M.M. (ed.), Oceanologie. Actualite et prospective. Centre d’Oceanologia de Marseille,
Marseille, pp. 263–288.
1807
C.E.Morales
Longhurst,A.R. and Harrison,W.G. (1988) Vertical nitrogen flux from the oceanic photic zone by diel
migrant zooplankton and nekton. Deep-Sea Res. I, 35, 881–889.
Longhurst,A.R. and Harrison,W.G. (1989) The biological pump: profiles of plankton production and
consumption in the upper ocean. Prog. Oceanogr., 22, 47–123.
Longhurst,A.R. and Williams,R. (1979) Materials for plankton modelling: vertical distribution of
Atlantic zooplankton in summer. J. Plankton Res., 1, 1–28.
Longhurst,A.R. and Williams,R. (1992) Carbon flux by seasonal vertical migrant copepods is a small
number. J. Plankton Res., 14, 1495–1509.
Longhurst,A.R., Bedo,A., Harrison,W.G., Head,E.J., Horne,E.P., Irwin,B. and Morales,C.E. (1989)
NFLUX: a test of the vertical nitrogen flux by diel migrant biota. Deep-Sea Res. I, 36, 1705–1719.
Longhurst,A.R., Bedo,A., Harrison,W.G., Head,E.J. and Sameoto,D.D. (1990) Vertical flux of respiratory carbon by oceanic diel migrant biota. Deep-Sea Res. I, 37, 685–694.
Morales,C.E., Bedo,A., Harris,R.P. and Tranter,P.R.G. (1991) Grazing of copepod assemblages in the
north-east Atlantic: the importance of the small size fraction. J. Plankton Res., 13, 455–472.
Morales,C.E., Harris,R.P., Head,R.N. and Tranter,P.R.G. (1993) Copepod grazing in the oceanic
northeast Atlantic during a 6 week drifting station: the contribution of size classes and vertical
migrants. J. Plankton Res., 15, 185–211.
Morris,M.J. and Hopkins,T.L. (1983) Biochemical composition of crustacean zooplankton from the
eastern Gulf of Mexico. J. Exp. Mar. Biol. Ecol., 69, 1–19.
Najjar,R.G., Sarmiento,J.L. and Toggweiler,J.R. (1992) Downward transport and fate of organic
matter in the ocean: simulations with a general circulation model. Global Biogeochem. Cycles, 6,
45–76.
Ohman,M.D. (1990) The demographic benefits of diel vertical migration by zooplankton. Ecol.
Monogr., 60, 257–281.
Omori,M. (1969) Weight and chemical composition of some important oceanic zooplankton in the
North Pacific Ocean. Mar. Biol., 3, 4–10.
Peinert,R., Bathmann,U., Bodungen,B. and Noji,T. (1987) The impact of grazing on spring phytoplankton growth and sedimentation in the Norwegian Current. Mitt. Geol. Palaeontol. Inst. Univ.
Hamburg, 62, 149–164.
Sargent,J.R. and Falk-Petersen,S. (1988) The lipid biochemistry of calanoid copepods. In
Boxshall,G.A. and Schminke,H.K. (eds), Biology of Copepods. Hydrobiologia, 167/168, 101–114.
Shaffer,G. (1993) Effects of the marine biota on global carbon cycling. In Heimnann,M. (ed.), The
Global Carbon Cycle. NATO ASI Series Vol. I 15. Springer-Verlag, Berlin, pp. 431–455.
Small,L.F., Fowler,S.W., Moore,S.A. and LaRosa,J. (1983) Dissolved and faecal pellet carbon and
nitrogen release by zooplankton in tropical waters. Deep-Sea Res. I, 30, 1199–1220.
Small,L.F., Knauer,G.A. and Tuel,M.D. (1987) The role of sinking fecal pellets in stratified euphotic
zones. Deep-Sea Res. I, 34, 1705–1712.
Smith,,S.L. and Lane,P.V.Z (1988) Grazing of the spring diatom bloom in the New York Bight by the
calanoid copepods Calanus finmarchicus, Metridia lucens and Centropages typicus. Cont. Shelf Sci.,
8, 485–509.
Tande,K. (1982) Ecological investigations on the zooplankton community of Balsfjorden, northern
Norway: generation cycles, and variations in body weight and body content of carbon and nitrogen
related to overwintering and reproduction in the copepod Calanus finmarchicus (Gunnerus). J.
Exp. Mar. Biol. Ecol., 62, 129–142.
Tseytlin,V.B. (1982) Transport of organic matter in daily vertical migrations of pelagic animals in
trophic regions of the ocean. Oceanology, 22, 614–618.
Weeks,A. et al. (1993) The physical and chemical environment and changes in community structure
associated with bloom evolution: the Joint Global Flux Study North Atlantic Bloom Experiment.
Deep-Sea Res. II, 40, 347–368.
Williams,R. (1988) Spatial heterogeneity and niche differentiation in oceanic zooplankton. Hydrobiologia, 167/168, 151–159.
Zhang,X. and Dam,H.G. (1997) Downward export of carbon by diel migrant zooplankton in the
central equatorial Pacific. Deep-Sea Res. I, 44, 2191–2202.
Received on November 19, 1998; accepted on April 29, 1999
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