Buoyancy and diapause in Antarctic copepods: The role of ammonium accumulation
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Limnol. Oceanogr., 55(5), 2010, 1860–1864
E 2010, by the American Society of Limnology and Oceanography, Inc.
doi:10.4319/lo.2010.55.5.1860
Buoyancy and diapause in Antarctic copepods: The role of ammonium accumulation
Franz Josef Sartoris,a,* David N. Thomas,b Astrid Cornils,a and Sigrid B. Schnack-Schiela
a Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany
b Ocean Sciences, College of Natural Sciences, Bangor University, Menai Bridge, Anglesey, United Kingdom
Abstract
To test the hypothesis that copepods are able to regulate their buoyancy via altering their ionic content, we
analyzed both the cation concentration in the hemolymph of Antarctic pelagic copepod species in late winter and
the vertical distribution pattern and population structure. High concentrations of ammonia/ammonium (NH3/
NH z4 ) were measured only in the hemolymph of Calanoides acutus, an Antarctic copepod definitely known to
undergo vertical ontogenetic migrations and diapause at great depth, and in Rhincalanus gigas, in which a vertical
ontogenetic migration pattern associated with diapause is still under debate. None of the other investigated
species showed elevated ammonium concentrations in their hemolymph. We suggest that ion replacement by
ammonium contributes to neutral buoyancy in diapausing calanoid copepods in the Southern Ocean. We
hypothesize that ammonium buoyancy changes with season and is associated with shifts in extracellular pH and,
therefore, most likely mediates metabolic depression during diapause.
Copepods are dominant members of the zooplankton 2004), and it has been suggested (Heath et al. 2004) that
biomass worldwide (Longhurst 1985), and owing to their there is a link between lipid accumulation during summer
high production : biomass ratio of 4.4 (Voronina 1998) they and the determination of the overwintering depth. Howev-
contribute greatly to the total zooplankton production. In er, the lipids of copepods are generally more compressible
Antarctic waters the dominance of copepods is mainly due and have a larger thermal expansion coefficient than
to large calanoid species such as Rhincalanus gigas, Calanus seawater (Yayanos et al. 1978). Model results show that
propinquus, Calanoides acutus, Metridia gerlachei, and the buoyancy properties of a copepod are extremely
Paraeuchaeta spp., which can make up more than 50% of sensitive to its relative biochemical constituents such as
the total zooplankton biomass (Boysen-Ennen et al. 1991). protein and chitin, and this makes neutral buoyancy
The annual production of these large copepods significant- unstable (Campbell and Dower 2003). However, change
ly exceeds that of the Antarctic krill Euphausia superba in total lipid content of only a few percentage points can
(Voronina 1998). make a significant difference to the buoyancy properties of
In polar seas herbivorous calanoid copepod species are the animal. Only a small percentage of the stored lipids are
strongly affected by the distinct seasonality in primary consumed during overwintering (Hagen and Schnack-
production and have developed specific behavioral and life Schiel 1996; Jónasdóttir 1999), but since development,
history strategy adaptations to survive long periods of food maturation, fertilization, and arousal from the resting
scarcity. Species belonging to the Eucalanidae and Calani- phase often start at overwintering depth before rising to the
dae families are known to undergo an extensive ontogenetic surface (Miller et al. 1991; Schnack-Schiel et al. 1991;
vertical migration: They descend out of the surface waters Atkinson et al. 1997), biochemical composition does
as late copepodite stages to greater depths ($ 500 m), change.
where they remain in a resting stage (diapause) for several It follows that the maintenance of neutral buoyancy in
months (Conover and Huntley 1991; Dahms 1995; zooplankton requires some other regulation mechanism.
Schnack-Schiel 2001). During this time they have severely Ion replacement, i.e., the selective disposal of heavier ions
reduced respiration and swimming activity (Schnack-Schiel (Na+, Mg2+, SO 2{ 4 ) and replacement with lighter ones (e.g.,
et al. 1991; Dahms 1995), suggesting that they have little NH z 4 , Cl ), has been proposed for diapausing copepods
2
active control over their vertical distribution. This invokes based on model calculations (Campbell and Dower 2003)
a rather fundamental question: How can an animal with but has never been observed. The replacement of heavier
reduced metabolism and swimming activity remain at a ions in body fluids by NH z 4 contributes to buoyancy
particular depth layer for such long periods of time? For regulation in pelagic deep-water cephalopods (Denton et al.
this to happen the animal must be neutrally buoyant at that 1969) and in deep-water shrimps (Sanders and Childress
depth. 1988), as well as in different groups of marine protists
Whether an organism floats or sinks depends on the (Sanders and Childress 1995; Boyd and Gradmann 2002).
density difference between the animal and the surrounding In this way, an organism can remain iso-osmotic with the
seawater, and so a neutrally buoyant animal must have the surrounding seawater while selectively reducing or increas-
same density as the surrounding seawater. In copepods ing its density.
lipid composition is considered to play a key role in To test the hypothesis that copepods are able to regulate
buoyancy control (Visser and Jónasdóttir 1999; Irigoien their buoyancy by altering their ionic content, we analyzed
the cation concentration in the hemolymph of Antarctic
* Corresponding author: Franz-Josef.Sartoris@AWI.de copepod species in late winter as well as their vertical
1860Ammonium buoyancy in Antarctic copepods 1861
Table 1. Ingestion rates (mean of three replicates) and egg production of C. acutus females (F) and CV stages at different sampling
dates. Data presented include the minimum and maximum ingestion rates of females (F) and copepodite stages V (CV) (ng Chl a
ind.21 d21), number of incubated females, the number of spawning females, the clutch size of spawning females (eggs female21), and the
presence or absence of fecal pellets in the reproduction experiments.
Feeding experiments Reproduction experiments
Sampling depth Ingestion Incubated Spawning Clutch Fecal
Station Latitude S Date Stage (m) rates F F size pellets
549 60u189 20 Sep 06 F 500–700 0.44–4.30 7 0 — —
F 700–1000 0.76–3.49
556 59u499 23 Sep 06 F 500–700 0–0.68 6 0 — —
F 700–1000 0–1.93
CV 500–700 0
CV 700–1000 0–1.97
565 61u429 29 Sep 06 F 200–300 0.24–5.37
F 300–500 0–0.12
F 500–700 0
F 700–1000 0
CV 700–1000 0
CV 1000–1500 1.43–2.64
568 62u509 02 Oct 06 F 0–500 no data 30 0 — —
598 58u009 20 Oct 06 F 0–500 181.9–290.1 19 6* 48 yes
* At 20 Oct all not spawning females had mature oocytes in their gonads.
distribution pattern and population structure in the water the difference between dissolved oxygen in the control
column. The species investigated were C. acutus, the only (water without copepods) and experimental bottles before
Antarctic copepod definitely known to undergo vertical and after the experiment. Each experiment comprised two
ontogenetic migrations and diapause at great depth, and R. replicates and two controls.
gigas, in which a vertical ontogenetic migration pattern Four feeding incubation experiments with three repli-
associated with diapause is still under debate due to cates were conducted on a plankton wheel for 24 h with
inconsistent field data (Marin and Schnack-Schiel 1993; natural phytoplankton suspension from 20-m depth as
Ward et al. 1997). These were compared with measure- food source. For each replicate 10 females from various
ments in C. propinquus, M. gerlachei, and Paraeuchaeta depths were incubated in 1 liter of seawater (Table 1).
spp., all of which do not undergo ontogenetic migration Chlorophyll a (Chl a) concentration was determined
and diapause at depth (Schnack-Schiel et al. 1991). fluorometrically at the start and the end of the experiments.
The ingestion rates were calculated using the method of
Methods Frost (1972).
For in situ egg production experiments, females were
Sampling and sorting—Stratified zooplankton samples incubated individually in 40 mL of natural phytoplankton
were collected from R/V Polarstern between 08 September suspension from 20-m depth for 48 h (Table 1). The
and 19 October 2006 in the southern Scotia Sea and the number of eggs released was counted every 24 h.
northwestern Weddell Sea, Antarctica, using a multiple
opening and closing net equipped with 100-mm mesh Hemolymph analysis—Immediately after the catch,
size. The net was towed vertically and sampled nine copepods were transferred to a Petri dish kept on an ice
successive depth layers from 6 2000 m depth to the bed, and subsequently they were carefully dried using tissue
surface. The filtered volume was measured for each net paper to avoid contamination with seawater. Hemolymph
using a digital flow meter. For experimental work and samples for the determination of extracellular ion concen-
hemolymph analysis a variety of pelagic copepods were trations were obtained with a glass capillary inserted
sorted by species, developmental stage, and sex from ventrally. The hemolymph samples were then diluted in
different depth layers. The rest of the samples were 40 mL of deionized water and stored at 220uC.
preserved in 4% borax-buffered formaldehyde seawater Sodium and ammonium concentrations were determined
solution for analyzing abundance, distribution, and age by ion chromatography (DIONEX ICS-2000) at 40uC
structure in the home lab. using an IonPac AG11-HC column with methane sulfonic
For the experimental work, live female and copepodite acid, (MSA, 30 mmol L21) as an eluent at 0.36 mL min21.
state V (CV) of C. acutus were sampled from different Owing to the small quantities of sample, they were injected
depth layers with the multinet to study the metabolic manually using a 10-mL sample loop. With this technique
activities. All experiments were carried out in the dark for 1 extracellular ion concentration in hemolymph samples
to 3 d in cooled containers at 0uC. could be measured in minimum volumes of about 10 nL.
Respiration activity was studied in 24-h long incubation Differences in ion concentration are presented as relative
experiments using oxygen concentrations measured by the cation percentages of sodium and ammonium in the
Winkler method. The respiration rates were calculated as hemolymph.1862 Sartoris et al.
Fig. 1. Relative cation percentages of sodium and ammoni-
um in the hemolymph of Antarctic copepods. Highest ammonium
levels were found in R. gigas and C. acutus independent of life
stage. Each result is given as mean value (and standard deviation)
of five to eight individuals. (F 5 Female; M 5 Male). Fig. 2. Respiration rates of C. acutus females and CV
dependent on time and depth.
Results and showed no reproductive activity (Table 1). Respiration
rates of the copepods increased at all studied water depths,
High concentrations of ammonia : ammonium (NH3 :
coinciding with the development and upward migration
NH z 4 ) were measured in the hemolymph of both C. acutus (Fig. 2). C. acutus caught at the last station in mid-October
and R. gigas (Fig. 1), whereas none of the other investi-
showed relatively high feeding and reproductive activities
gated species showed similar results. In the hemolymph of (242.24 Chl a ind.21 d21; 48 eggs ind.21; Table 1),
some of the C. acutus and R. gigas individuals, the indicative of active females, since resting females are not
concentrations of NH3 : NH z 4 replaced more than 90% of capable of releasing eggs in short incubations (Ohman et al.
the Na+ ions, reaching values as high as 450 mmol L21. 1998). In contrast, the ammonia : ammonium (NH3 : NH z 4 )
Our observations of the population structure and the concentrations varied independently of depth and time in
vertical distribution agree generally with the findings of both species, and hence no significant vertical trend is
earlier investigations on life cycle traits of C. acutus and R. obvious and no significant differences were measured
gigas in late winter : early spring (Atkinson et al. 1997; between sampling dates (Fig. 3).
Ward et al. 1997) and indicate a shift from the dormant to
the active stage of both species during our investigation Discussion
period. The population of C. acutus was dominated by late
copepodite stages (CIV, CV) and adults while the earliest The finding of high levels of ammonia : ammonium
copepodite stage (CI) was not encountered. The R. gigas (NH3 : NH z 4 ) in copepod species, which are known to
population contained mainly older copepodite stages and undergo vertical ontogenetic migration (C. acutus), and in
females; however, in contrast to C. acutus, CIII also R. gigas suggests that ontogenetic migration is related to
occurred in higher numbers. All developmental stages of R. and/or relies on ammonia-aided buoyancy. Compared to
gigas were found, although CI and males were present only the extra cost of swimming or the accumulation of low-
in low numbers. In both species, the stage frequency density organic compounds such as lipids, the energy costs
distribution shifted in dominance during the study period: involved in the production of large amounts of ammonia
In C. acutus, the decrease in the number of stage CVs was are low, since it is a waste product of the nitrogen
accompanied by an increase in the number of females. metabolism. Depending on the pH, ammonia exists in
Thus, the CV : female ratio decreased, indicating CVs solutions as both NH3 and NH z 4 . The dissociation
molting to females and, hence, the end of diapause (Sanders constant (pK) of the reaction is about 9.5, resulting in a
and Childress 1995). In contrast, the stage CIV decreased in shift to form NH z4 with decreasing pH. In addition, NH3 is
R. gigas while females increased. more toxic than NH z z
4 , and, in contrast to NH 4 , it easily
The population structure development was associated penetrates cell membranes. Owing to the toxicity and the
with a seasonal vertical migration from wintering in deep- greater diffusibility of NH3, a low hemolymph pH is
water layers (C. acutus) and mid-water layers (R. gigas) in required to favor the formation of ammonium ions
early September to the upper 100 m in mid-October. This (NH z 4 ). Ammonia concentrations, as high as those found
was more pronounced in C. acutus than in R. gigas. These in the hemolymph of C. acutus and R. gigas, would impair
features are consistent with a dormancy stage, and the nervous function in other marine invertebrates, e.g.,
metabolic measurements of C. acutus during the cruise cephalopods (Clarke et al. 1979). However, in contrast to
support the field data. The population investigated in other invertebrates, e.g., cephalopods and deep-water
September concentrated in deep- and mid-water layers had shrimps, copepods lack a specialized chamber for the
low respiratory oxygen consumption, fed only very little, storage of the potentially toxic ammoniotelic fluid.Ammonium buoyancy in Antarctic copepods 1863
Fig. 3. Vertical distribution expressed as a percentage of the total numbers and hemolymph
ammonium levels (mean and standard deviation) of C. acutus female and CV at different sampling
dates. Numbers in parentheses: abundance (ind. 100 m23) within the studied water column.
In cephalopods and in deep-water shrimps the ammoni- diapausing copepods necessary to form NH z 4 , and to
um-containing fluid is stored in specialized compartments at prevent diffusive loss, could therefore also play a funda-
low pH to cope with the potentially toxic levels of ammonia mental role in the regulation of metabolic depression.
(Clarke et al. 1979; Sanders and Childress 1988). Owing to At present it is unclear why there was no correlation
the toxicity and the higher diffusibility of NH3, we predict a between ammonium concentration and either time or
low hemolymph pH in diapausing copepods to favor the depth. The synergistic effects of ammonium accumulation
formation of ammonium (NH z 4 ), which is less toxic and in the hemolymph, lipid content, and lipid composition and
more resistant to loss by passive diffusion. On the other hand, the change in protein content during protein degradation
since it is only slightly lighter than sodium (molecular weight, (required for ammonium accumulation) could probably
MW, NH3 5 17.0307; Na+ 5 22.9898), large quantities must account for this observation.
be accumulated in order to achieve neutral buoyancy. The However, from these first results it can be expected that
storage of large amounts of fluid in specialized chambers has there is a seasonal accumulation of ammonia in diapausing
the disadvantage that it requires changes in the shape of the copepods: In the summer a low pHe would not be
animal, resulting in an increased energy demand for consistent with high metabolic activity, and in addition
swimming at a given speed (Alexander 1990). To maintain ammonium-regulated buoyancy will not be required during
a low pH in the hemolymph requires additional energy for highly active periods as shown by the nondiapausing
ion transfer, but such costs might be lower than the copepods. Such seasonality would be an additional
additional costs of swimming with a buoyancy chamber. explanation for the lack of a specialized chamber for the
This could be part of the explanation for why copepods have storage of ammonia-containing fluid, since low hemolymph
not developed chambers for ammonium storage, which has pH in winter at diapause would be an advantage. In
resulted in the hemolymph itself acting as low-density fluid. contrast ammoniotelic squid and shrimp are active
Furthermore, low pH values are known as a relevant throughout the year and have to separate the low pH
factor depressing metabolic rate during dormancy (Busa and ammonia-containing fluid from the hemolymph to avoid
Crowe 1983) or environmental hypercapnia (Hand and pHe mediated metabolic depression.
Gnaiger 1988; Rees and Hand 1990; Reipschläger and We hypothesize that the high ammonia levels in these
Pörtner 1996). Although most of the earlier studies have two species of Antarctic copepods act as a buoyancy
focused on the role of intracellular pH, there is a drop of mechanism. The energy-saving properties of this mecha-
extracellular pH (pHe) induced metabolic depression during nism during diapause in deep water, when metabolism is
hypercapnia in the sipunculid worm Sipunculus nudus reduced, and the proposed pHe-mediated metabolic de-
(Reipschläger and Pörtner 1996). In diapausing copepods, pression are likely to be part of the explanation. Further
metabolic depression is evidenced by lowered respiration studies, particularly the measurement and experimental
rates and reduced swimming activities (Atkinson et al. 1997). adjustment of pHe in summer animals, should reveal
The predicted low extracellular pH in the hemolymph of whether pHe is important for the regulation of the1864 Sartoris et al.
transition between metabolism and diapause. Clearly other IRIGOIEN, X. 2004. Some ideas about the role of lipids in the life
ontogenetic migrating copepod species from Arctic, boreal cycle of Calanus finmarchicus. J. Plankton Res. 26: 259–263,
regions and upwelling regions have to be analyzed to doi:10.1093/plankt/fbh030
establish whether or not this is a regional phenomenon or JÓNASDÓTTIR, S. H. 1999. Lipid content of Calanus finmarchicus
more cosmopolitan throughout the copepods. during overwintering in the Faroe-Shetland Channel. Fish.
Oceanogr. 8: 61–72, doi:10.1046/j.1365-2419.1999.00003.x
LONGHURST, A. R. 1985. The structure and evolution of plankton
Acknowledgments communities. Prog. Oceanogr. 15: 1–35, doi:10.1016/0079-6611
We thank the captain, the crew, and colleagues aboard R/V (85)90036-9
Polarstern for their help and collaboration in the field, and Ruth
MARIN, V., AND S. B. SCHNACK-SCHIEL. 1993. The occurrence of
Alheit for help in sorting the samples. Two anonymous reviewers are
Rhincalunus gigus, Calanoides acutus and Calunus propinquus
thanked for their constructive comments and suggestions on an
(Copepoda: Calanoida) in late May in the area of the
earlier version of the manuscript. Census of Marine Zooplankton
Antarctic Peninsula. Polar Biol. 13: 35–40, doi:10.1007/
(CMarZ), a Census of Marine Life (CoML) project, and the Natural
BF00236581
Environmental research Council, U.K., partly supported this study.
MILLER, C. B., T. J. COWLES, P. H. WIEBE, N. J. COPLEY, AND H.
GRIGG. 1991. Phenology in Calanus finmarchicus: Hypotheses
References about control mechanisms. Mar. Ecol. Prog. Ser. 72: 79–91,
ALEXANDER, R. M. N. 1990. Size, speed and buoyancy adaptations doi:10.3354/meps072079
in aquatic animals. Am. Zool. 30: 189–196. OHMAN, M. D., A. V. DRITS, M. E. CLARKE, AND S. PLOURDE.
ATKINSON, A., S. B. SCHNACK-SCHIEL, P. WARD, AND V. MARIN. 1998. Differential dormancy of co-occurring copepods.
1997. Regional differences in the life cycle of Calanoides Deep-Sea Res. II 45: 1709–1740, doi:10.1016/S0967-0645(98)
acutus (Copepoda: Calanoida) within the Atlantic sector of 80014-3
the Southern Ocean. Mar. Ecol. Prog. Ser. 150: 99–111, REES, B. B., AND S. C. HAND. 1990. Heat dissipation, gas exchange
doi:10.3354/meps150099 and acid–base status in the land snail Oreohelix during short-
BOYD, C. M., AND D. GRADMANN. 2002. Impact of osmolytes on term estivation. J. Exp. Biol. 152: 77–92.
buoyancy of marine phytoplankton. Mar. Biol. 141: 605–618, REIPSCHLÄGER, A., AND H. O. PÖRTNER . 1996. Metabolic
doi:10.1007/s00227-002-0872-z depression during environmental stress: The role of extracel-
BOYSEN-ENNEN, E., W. HAGEN, G. HUBOLD, AND U. PIATKOWSKI. lular versus intracellular pH in Sipunculus nudus. J. Exp. Biol.
1991. Zooplankton biomass in the ice-covered Weddell Sea, 199: 1801–1807.
Antarctica. Mar. Biol. 111: 227–235, doi:10.1007/BF01319704 SANDERS, N. K., AND J. J. CHILDRESS. 1988. Ion replacement as a
BUSA, W. B., AND J. H. CROWE. 1983. Intracellular pH regulates buoyancy mechanism in a pelagic deep-sea crustacean. J. Exp.
the dormancy/development transition of brine shrimp (Arte- Biol. 138: 333–343.
mia salina) embryos. Science 221: 366–368, doi:10.1126/ ———, AND ———. 1995. Nitrogen and buoyancy in marine
science.221.4608.366 organisms, p. 51–60. In P. J. Walsh and P. A. Wright [eds.],
CAMPBELL, R. W., AND J. F. DOWER. 2003. Role of lipids in the Nitrogen metabolism and excretion. CRC.
maintenance of neutral buoyancy by zooplankton. Mar. Ecol. SCHNACK-SCHIEL, S. B. 2001. Aspects of the study of the life cycles
Prog. Ser. 263: 93–99, doi:10.3354/meps263093 of Antarctic copepods. Hydrobiologia 453/454: 9–24,
CLARKE, M. R., E. J. DENTON, AND J. B. GILPIN-BROWN. 1979. On doi:10.1023/A:1013195329066
the use of ammonium for buoyancy in squids. J. Mar. Biol. ———, W. HAGEN, AND E. MIZDALSKI. 1991. Seasonal comparison
Assoc. U.K. 59: 259–276, doi:10.1017/S0025315400042570 of Calanoides acutus and Calanus propinquus (Copepoda:
CONOVER, R. J., AND M. HUNTLEY. 1991. Copepods in ice-covered Calanoida) in the southeastern Weddell Sea, Antarctica. Mar.
seas—distribution, adaptations to seasonally limited food, Ecol. Prog. Ser. 70: 17–27, doi:10.3354/meps070017
metabolism, growth patterns and life cycle strategies in polar VISSER, A. W., AND S. H. JÓNASDÓTTIR. 1999. Lipids, buoyancy and
seas. J. Mar. Syst. 2: 1–41, doi:10.1016/0924-7963(91)90011-I the seasonal vertical migration of Calanus finmarchicus. Fish.
DAHMS, H. U. 1995. Dormancy in the Copepoda—an overview. Oceanogr. 8: 100–106, doi:10.1046/j.1365-2419.1999.00001.x
Hydrobiologia 306: 199–211, doi:10.1007/BF00017691 VORONINA, N. M. 1998. Comparative abundance and distribution
DENTON, E. J., J. B. GILPIN-BROWN, AND T. I. SHAW. 1969. A of major filter-feeders in the Antarctic pelagic zone. J. Mar.
buoyancy mechanism found in cranchid squid. Proc. R. Soc. Syst. 17: 375–390, doi:10.1016/S0924-7963(98)00050-5
Lond. B 174: 271–279, doi:10.1098/rspb.1969.0093 WARD, P., A. ATKINSON, S. B. SCHNACK-SCHIEL, AND A. W. A.
FROST, B. W. 1972. Effects of size and concentration of food MURRAY. 1997. Regional variation in the life cycle of
particles on the feeding behaviour of the marine planktonic Rhincalanus gigas (Copepoda: Calanoida) in the Atlantic
copepod Calanus pacificus. Limnol. Oceanogr. 17: 805–815, sector of the Southern Ocean—re-examination of existing
doi:10.4319/lo.1972.17.6.0805 data (1928 to 1993). Mar. Ecol. Prog. Ser. 157: 261–275,
HAGEN, W., AND S. B. SCHNACK-SCHIEL. 1996. Seasonal lipid doi:10.3354/meps157261
dynamics in dominant Antarctic copepods: Energy for YAYANOS, A. A., A. A. BENSON, AND J. C. NEVENZEL. 1978. The
overwintering or reproduction? Deep-Sea Res. I 43: pressure volume-temperature (PVT) properties of a lipid mixture
139–158, doi:10.1016/0967-0637(96)00001-5 from a marine copepod Calanus plumchrus: Implications for
HAND, S. C., AND E. GNAIGER. 1988. Anaerobic dormancy buoyancy and sound scattering. Deep-Sea Res. 25: 257–268.
quantified in Artemia embryos: A calorimetric test of the
control mechanisms. Science 239: 1425–1427, doi:10.1126/
science.239.4846.1425 Associate editor: Everett Fee
HEATH, M. R., AND oTHERS. 2004. Comparative ecology of over-
wintering Calanus finmarchicus in the northern North Received: 21 August 2009
Atlantic, and implications for life-cycle patterns. ICES J. Accepted: 05 April 2010
Mar. Sci. 61: 698–708, doi:10.1016/j.icesjms.2004.03.013 Amended: 14 May 2010You can also read
