JPR Advance Access originally published online on February 16, 2004
Journal of Plankton Research 2004 26(3):259-263; doi:10.1093/plankt/fbh030
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Journal of Plankton Research Vol. 26 No. 3 © Oxford University Press 2004; all rights reserved
HORIZONS |
Some ideas about the role of lipids in the life cycle of Calanus finmarchicus
Azti, Herrera Kaia Portualdea, Z/G, 20110 Gipuzkoa, Spain
* Corresponding Author: xirigoien{at}pas.azti.es
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSOME RECENT RESULTS WITH...SOME QUESTIONS AND HYPOTHESESTESTING THE MODELNEXT STEPSFOOTNOTESREFERENCES |
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A conceptual model of the possible role of lipids in the life cycle of Calanus finmarchicus is proposed. Lipid storage could play a key role at various levels: (i) by triggering diapause through variations in cholesterol and fatty acid derived hormone levels; (ii) by determining the overwintering depth in relation to the convective mixed layer; and (iii) by playing an important role in the population adaptation to the hydrological conditions of the basin. A number of ways to test the validity of the proposed hypotheses are proposed.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSOME RECENT RESULTS WITH...SOME QUESTIONS AND HYPOTHESESTESTING THE MODELNEXT STEPSFOOTNOTESREFERENCES |
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Calanus finmarchicus is a copepod that dominates the North Atlantic zooplankton biomass (Planque and Batten, 2000
). As with other high-latitude copepods, two distinctive characteristics of C. finmarchicus are that it spends a large part of the year in diapause in deep waters and that it has a large lipid store. Nevertheless, we often keep interpreting the life cycle of C. finmarchicus in terms of temperature and chlorophyll (Prestidge et al., 1995; Carlotti and Radach, 1996; Bryant et al., 1997; Radach et al., 1998; Tittensor et al., 2003), with lipids being considered just an energy storage molecule.
Recently, there has been a large amount of research focusing on C. finmarchicus [e.g. the EU projects TASC (Tande and Miller, 2000) and ICOS (Heath, 1999), or the UK NERC programme ‘Marine Productivity’], resulting in a number of discoveries that suggest new roles for lipids. This paper puts together the known facts about the role of lipids in the biology of C. finmarchicus and, on the basis of these facts, poses some hypotheses in an attempt to synthesize a testable conceptual model of the possible role of lipids in the life cycle. Rather than trying to prove a point, the objective is to summarize the available new knowledge and to present hypotheses that can be challenged and tested through observations, experimentation, or mathematical modelling.
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SOME RECENT RESULTS WITH CONSEQUENCES FOR OUR UNDERSTANDING OF THE ROLE OF LIPIDS IN THE LIFE CYCLE OF C. FINMARCHICUS |
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TOPABSTRACTINTRODUCTIONSOME RECENT RESULTS WITH...SOME QUESTIONS AND HYPOTHESESTESTING THE MODELNEXT STEPSFOOTNOTESREFERENCES |
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Lipid storage determines the diapause depth (Visser and Jonasdottir, 1999
). For diapause, it is necessary that the copepod has attained a depth where it is neutrally buoyant. Hence, the depth and physical conditions where the copepod is neutrally buoyant are largely defined by the lipid content of the animal.
The diapause depth has to be deeper than the winter convective mixed layer [CML; see details of the CML in Backhaus et al. (Backhaus et al., 2003)] and the features of the CML limit the time that can be spent at the surface. All the copepods remaining above the winter permanent thermocline when winter mixing begins will be transported to the surface regularly. On the other hand, the retreating CML could facilitate the spring ascent (J. O. Backhaus, personal communication).
Only a small percentage (
5%) of the stored lipids are consumed during overwintering (Jonasdottir, 1999). In fact, fifth copepodite stage (CV) and adult females have a large amount of lipid when they reach the surface that is subsequently used by females to produce eggs before the phytoplankton bloom, when food levels are still low (Niehoff et al., 1999). As a consequence, in oceanic waters, total egg production before the bloom (both for the individual and the population) can be much higher than expected from the food concentration (Hirche et al., 2001).
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SOME QUESTIONS AND HYPOTHESES |
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TOPABSTRACTINTRODUCTIONSOME RECENT RESULTS WITH...SOME QUESTIONS AND HYPOTHESESTESTING THE MODELNEXT STEPSFOOTNOTESREFERENCES |
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What triggers diapause?
One central and unanswered question is: what controls the beginning and the end of diapause? A number of factors have been put forward [temperature, food and photoperiod; see the review in Miller et al. (Miller et al., 1991)]. However, none of those parameters appears adequate to explain the whole distribution area of C. finmarchicus (which demonstrates wide variations in temperature and food concentration, while overwintering is too deep for light to reach the animals in some areas). The trigger could also be genetically fixed (i.e. ‘go into diapause for x time after moulting to CV’). However, the genetically fixed or ‘no external trigger’ hypothesis does not fit with the observation that a fraction of the first cohort does not go into overwintering and moults into adult, whereas the rest of the cohort does overwinter, and also with the fact that part of the population can overwinter at stage CIV (Irigoien, 2000).
One could propose here that the body lipid level could itself be the trigger. Copepods are not the only arthropods that have a diapause phase. It is known that moulting in arthropods is controlled by steroid moulting hormones called ecdysteroids and it has been shown that their variations during the copepod moult cycle are similar to those of decapods (Johnson, 2003). The ecdysteroid level is also lower in diapausing Calanus pacificus than in active individuals (Johnson, 2003). Another hormone, the juvenile hormone (JH), regulates a variety of functions in insects: metamorphosis, synthesis of vitellogenin in the adult female, deposition of vitellogenin into oocytes, accessory gland secretions involved in formation of the egg case, etc. (Nijhout, 1994). In terms of development, the JH controls progression through the life cycle and metamorphosis from larva to pupa in insects. As long as there is enough JH, ecdysone promotes larva-to-larva moults. With lower amounts of JH, ecdysone promotes pupation. Complete absence of JH results in formation of the adult (Nijhout, 1994). Apparently, insects can make JH de novo without a dietary source, but require a dietary source of sterols to synthesize ecdysone. Actually, ecdysone is not the active moulting hormone. Various tissues, including the fat body, convert ecdysone to 20-hydroxyecdysone, the active form of moulting hormone (Nijhout, 1994). The crustacean counterpart of the JH, methyl farnesoate [MF; Figure 1 (Laufer et al., 1987)], is a key regulator of oocyte development, metamorphosis in larvae and adult reproduction (Laufer et al., 1993). MF can enhance ovarian development and improve both the quantity and quality of spawn (Laufer et al., 1998). Also, MF and ecdysteroids seem to determine the control of morphogenesis in the allometric growth of crustacea (Laufer et al., 2002). In the copepod Acartia tonsa, experimental exposure to JH strongly inhibited development, whereas exposure to 20-hydroxyecdysone alone did not have an inhibitory effect on development (Andersen et al., 2001).
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Ecdysteroids are derived from cholesterol, whereas the JH and MF are fatty acid derivatives. So, being the precursors, and considering that in insects the fat body is one of the tissues where ecdysone is converted into 20-hydroxyecdysone, it is not very difficult to imagine a feedback system whereby the production of the hormones regulating moulting and diapause is controlled by (or related to) the lipid level (fatty acids and sterols) in the copepods.
Now, let us consider the situation where diapause could indeed be triggered by the lipids’ accumulation through variations in MF and 20-hydroxyecdysone levels: what should the level that triggers diapause be? It has to fulfil two conditions. (i) The lipid level has to be high enough to cover the energy required to moult from CV to adult (Rey-Rassat et al., 2002a), moulting that often occurs at depth and/or in periods with low food levels. (ii) The lipid level also has to allow for neutral buoyancy in waters below the CML or individuals will be periodically transported to the surface. In this sense, it has to be considered that the buoyant properties are sensitive to the copepod’s relative biochemical composition (Campbell and Dower, 2003) and therefore the lipid-free dry density (e.g. variations in protein content) might play a more important role than the one assumed by the Visser and Jonasdottir (Visser and Jonasdottir, 1999) model (M. R. Heath, personal communication).
How to ‘get’ the right depth to diapause?
Following these hypotheses, an obvious question arises: how does a copepod that is drifting around in a large basin ‘know’ what is the right depth at which to overwinter? The next hypothesis proposed is that the copepod does not ‘know’ the depth, but that each year the configuration of CML is a very strong source of natural selection. Those animals that overwinter at an inappropriate depth are transported to the surface, and although they may not necessarily die if they have enough lipids, their offspring are unlikely to survive with access only to the low winter food concentrations (Hirche et al., 2001; Irigoien et al., 2003). Hence, the buoyancy level results in a heritable trait that confers differential survival. Several authors have shown that overwintering individuals do have higher lipid levels than those remaining at the surface (Jonnasdottir, 1999; Miller et al., 2000) and generally these levels correspond to the density of the deep-water layers of the basin (Heath et al., 2004). There are also a number of observations of small populations of C. finmarchicus living at the surface during the winter [e.g. (Durbin et al., 1997); D. Bonnet, personal communication, for Marine Productivity winter cruises]. One may suggest that these are the animals that got their lipid level ‘wrong’ or were too late in the season and were either not able to go into diapause or went into diapause but were caught by the CLM and transported back to the surface.
How to get the right lipid level?
The next question is how does the copepod attain the right lipid level? Here it is suggested that this is a question of timing. Calanus finmarchicus accumulates lipids mainly during stages CIII, CIV and CV (Hygum et al., 2000). Therefore, the best way to build up lipid storage to the appropriate level is for stages CIII–CV to coincide with the maximum food concentration, i.e. the phytoplankton bloom. This might explain why females use lipids to produce eggs before the bloom (Niehoff et al., 1999; Richardson et al., 1999), the risk of a very high offspring mortality if the feeding naupliar stages (from NIII forward) do not find higher concentrations of food than those used by the mother being offset by the gain from matching with the phytoplankton bloom (Ohman and Hirche, 2001). Considering the development time of C. finmarchicus [25–30 days to CIII and 35–45 days to CV depending on temperature (Corkett et al., 1986)], a typical bloom might be too short for an egg produced during the bloom to reach stages CIII–CV before it ended. Therefore, the best conditions to accumulate lipids will be found by those individuals already at the sixth naupliar stage (NVI) or CI at the beginning of the bloom. Individuals resulting from eggs produced during the bloom would have to remain feeding at the surface at the low levels of post-bloom food concentration to build up the necessary lipid storage.
The need to build up a certain lipid level would also condition the timing of the ascent. The offspring of those arriving too late in relation to the bloom would have to spend a long time at the surface to build the lipid level by feeding at low food concentrations. This has three risky consequences: (i) possible starvation of the nauplii at low post-bloom food concentrations composed mainly of flagellates (Irigoien et al., 2003); (ii) high risk of predation at the surface (Kaartvedt, 1996); and (iii) individuals developing too late in the season would be caught by convective mixing and be unable to swim down even if they had the right lipid level. Therefore, the risk of reproducing too late in respect to the bloom could be as high as that of being too early. This is in fact a variation of the classic match–mismatch hypothesis (Cushing, 1990) with starvation as the main source of mortality before the bloom and predation afterwards.
It is plausible that once below the CML, this year-after-year selection process favours individuals neutrally buoyant in water masses matching high lipid levels, as these should have a higher capacity to produce eggs during the period before the bloom. Individuals with a higher lipid storage will be able to produce more eggs (Richardson et al., 1999; Rey-Rassat et al., 2002b) and for longer before exhausting their internal storage and having to stop producing eggs. Interestingly, there is again a coincidence between observations, suggesting an important role for lipids in egg production and the fact that MF seems to control ovarian maturation and the quantity and quality of the spawn in other crustaceans (Laufer et al., 1998).
This hypothesis suggests that year after year the depth of the CML and the timing of the bloom will be a strong source of natural selection, leaving animals that get their lipid level wrong without offspring. However, a range of lipid levels (or variations in protein content) would allow animals to stay at different safe depths below the CML, maintaining a pool of variability. Such variability in neutral buoyancy depths could result in different trajectories during the life cycle (Heath et al., 2004). It will be interesting to test whether the lipid levels found in one basin would allow for overwintering in another one, allowing for surface exchange of populations during spring (Heath et al., 2004).
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TESTING THE MODEL |
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TOPABSTRACTINTRODUCTIONSOME RECENT RESULTS WITH...SOME QUESTIONS AND HYPOTHESESTESTING THE MODELNEXT STEPSFOOTNOTESREFERENCES |
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Parts of this conceptual model, or even all of it, may be wrong. Here are proposed a number of ways of testing it.
(i) Several studies are now measuring ecdysterones in Calanus. One may suggest that MF should be considered as well. If no relationship between variations in the wax ester (WE) and triacylglycerol (TAG) contents and variations of the ecdysone and MF levels is found, then the hypothesis of the lipid level as a trigger for overwintering will be falsified. It is likely that food quality may play a role as well due to different fatty acid compositions.
(ii) Exposure to JH (JH III) has been shown to inhibit development in Acartia tonsa (Andersen et al., 2001). It would be of great interest to see the effect of exposure to JH (or MF) and 20-hydroxyecdysone in C. finmarchicus with different lipid levels. Another interesting experiment would be to check how temperatures (and/or pressures) simulating overwintering at depth modify the hormone effect.
(iii) No overwintering copepods collected in the field should have a lipid storage level below that allowing for moulting from CV to adult (Rey-Rassat et al., 2002a). If a significant proportion of the population has lipid levels below that limit, the role of lipids as a trigger mechanism will be falsified.
(iv) In each ocean basin, once below the CML, the depth layers allowing for the highest lipid level should be favoured, as individuals at these depths should be those with the highest survival flexibility and able to produce the highest number of eggs in the following years.
(v) After the spring bloom, overwintering copepods should have higher lipid levels than those remaining at the surface. Published data show that, on average, overwintering copepods do have higher lipid levels than those at the surface [figure 5 in Jonasdottir (Jonasdottir, 1999; Miller et al., 2000)]. However, to test this hypothesis will require detailed analysis of the data, evaluating variability in WE content between individuals and considering the percentage of outliers. It will also be necessary to evaluate TAG levels to distinguish between individuals in dormancy and specimens in which gonad development and emergence from diapause have commenced (Heath et al., 2004).
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NEXT STEPS |
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TOPABSTRACTINTRODUCTIONSOME RECENT RESULTS WITH...SOME QUESTIONS AND HYPOTHESESTESTING THE MODELNEXT STEPSFOOTNOTESREFERENCES |
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The tests related to the lipid contents will be relatively easy to carry out with the data collected during the intensive field sampling programmes mentioned above. If the proposed hypotheses do survive those tests, it will be necessary to investigate the possible mechanisms relating lipid levels and diapause hormones. Since the early work by Carlisle and Pitman (Carlisle and Pitman, 1961
), there has not been much progress in marine copepod hormone research; however, there is a large body of literature on insects and other crustaceans available that should facilitate rapid progress in that area.
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ACKNOWLEDGEMENTS |
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Thanks are due to R. P. Harris, K. J. Flynn and various reviewers for comments on previous versions, and to D. Speirs for a discussion that prompted this article. X.I. was supported by a Ramon y Cajal grant from the Spanish ministry for science and technology and by the Agriculture and Fisheries department of the Basque Country Government. This paper is a contribution to the NERC ‘Marine Productivity’ Thematic Programme.
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FOOTNOTES |
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TOPABSTRACTINTRODUCTIONSOME RECENT RESULTS WITH...SOME QUESTIONS AND HYPOTHESESTESTING THE MODELNEXT STEPSFOOTNOTESREFERENCES |
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Written responses to this article should be submitted to the Editorial Office within two months of publication. For further information, please see the Editorial ‘Horizons’ in Journal of Plankton Research, Volume 26, Number 3, Page 257.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONSOME RECENT RESULTS WITH...SOME QUESTIONS AND HYPOTHESESTESTING THE MODELNEXT STEPSFOOTNOTESREFERENCES |
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Andersen, H. R., Wollenberger, L., Halling-Soerensen, B. and Kusk, K. O. (2001) Development of copepod nauplii to copepodites—a parameter for chronic toxicity including endocrine disruption. Environ. Toxicol. Chem., 20, 2821–2829.[Medline]
Backhaus, J. O., Hegseth, E. N., Wehde, H., Irigoien, X., Hatten, K. and Logemann, K. (2003) Convection and primary production in winter. Mar. Ecol. Prog. Ser., 252, 1–14.
Bryant, A., Heath, M., Gurney, W., Bearer, D. J. and Robertson, W. (1997) The seasonal dynamics of Calanus finmarchicus: development of a three dimensional structured model and application to the northern North Sea. Neth. J. Sea Res., 38, 361–379.
Campbell, R. W. and Dower, J. F. (2003) Role of lipids in the maintenance of neutral buoyancy by zooplankton. Mar. Ecol. Prog. Ser., 263, 93–99.
Carlisle, D. and Pitman, W. (1961) Diapause, neurosecretion and hormones in Copepoda. Nature, 190, 827–828.[Medline]
Carlotti, F. and Radach, G. (1996) Seasonal dynamics of phytoplankton and Calanus finmarchicus in the North Sea as revealed by a coupled one-dimensional model. Limnol. Oceanogr., 41, 522–539.
Corkett, C. J., McLaren, I. A. and Sevigny, J. M. (1986) The rearing of the marine calanoid copepods Calanus finmarchicus (Gunnerus), C. glacialis and C hyperboreus Krøyer with comment on the equiproportional rule. Syllogeus, 58, 539–547.
Cushing, D. H. (1990) Plankton production and year class strength in fish populations: an update of the match/mismatch hypothesis. Adv. Mar. Biol., 26, 249–293.
Durbin, E. G., Runge, J. A., Campbell, R. G., Garrahan, P. R., Casas, M. C. and Plourde, S. (1997) Late fall–early winter recruitment of Calanus finmarchicus on Georges Bank. Mar. Ecol. Prog. Ser., 151, 103–114.
Heath, M. R. (1999) Introduction. Fish. Oceanogr., 8(Suppl. 1), vii–viii.
Heath, M. R. et al. (2004) Comparative ecology of overwintering Calanus finmarchicus in the North Atlantic, and implications for life cycle patterns. ICES J. Mar. Sci., in press.
Hirche, H. J., Brey, T. and Niehoff, B. (2001) A high frequency time series at Ocean Weather Ship Station M (Norwegian Sea): population dynamics of Calanus finmarchicus. Mar. Ecol. Prog. Ser., 219, 205–219.
Hygum, B. H., Rey, C., Hansen, B. W. and Tande, K. S. (2000) Importance of food quantity to structural growth rate and neutral lipid reserves accumulated in Calanus finmarchicus. Mar. Biol., 136, 1057–1073.[CrossRef]
Irigoien, X. (2000) Vertical distribution and population dynamics of Calanus finmarchicus at station India (59°N, 19°W) during the passage of the great salinity anomaly, 1971 to 1975. Deep-Sea Res. I, 47, 1–26.
Irigoien, X., Titelman, J., Harris, R. P., Harbour, D. and Castellani, C. (2003) Feeding of Calanus finmarchicus nauplii in the Irminger Sea. Mar. Ecol. Prog. Ser., 262, 193–200.
Johnson, C. L., (2003) Ecdysteroids in the oceanic copepod Calanus finmarchicus: variation during molt cycle and change associated with diapause. Mar. Ecol. Prog. Ser., 257, 159–165.
Jonasdottir, S. H. (1999) Lipid content of Calanus finmarchicus during overwintering in the Faroe–Shetland Channel. Fish. Oceanogr., 8, 61–72.
Kaartvedt, S. (1996) Habitat preference during overwintering and timing of seasonal vertical migration of Calanus finmarchicus. Ophelia, 44, 145–156.[ISI]
Laufer, H., Borst, D., Baker, F. C., Carrasco, C., Sinkus, M., Reuter, C. C., Tsai, L. W. and Schooley, D. S. (1987) Identification of a juvenile hormone-like compound in a crustacean. Science, 235, 202–205.
Laufer, H., Ahl, J. S. B. and Sagi, A. (1993) The role of juvenile hormones in crustacean reproduction. Am. Zool., 33, 365–374.
Laufer, H., Biggers, W. J. and Ahl, J. (1998) Stimulation of ovarian maturation in crayfish Procambarus clarkii by methyl farnesoate. Gen. Comp. Endocrinol., 111, 113–118.[CrossRef][ISI][Medline]
Laufer, H., Ahl, J., Rotlant, G. and Baclaski, B. (2002) Ecdysteroids and methyl farnesoate control allometric growth and differentiation in a crustacean. Insect Biochem. Mol. Biol., 32, 205–210.[Medline]
Miller, C. B., Cowles, T. J., Wiebe, P. H., Copley, N. J. and Grigg, H. (1991) Phenology in Calanus finmarchicus; hypotheses about control mechanisms. Mar. Ecol. Prog. Ser., 72, 79–91.
Miller, C. B., Crain, J. A. and Morgan, C. (2000) Oil storage variability in Calanus finmarchicus. ICES J. Mar. Sci., 57, 1786–1799.
Niehoff, B., Klenke, U., Hirche, H. J., Irigoien, X., Head, R. N. and Harris, R. P. (1999) A high frequency time series at Weathership M, Norwegian Sea, during the 1997 spring bloom: the reproductive biology of Calanus finmarchicus. Mar. Ecol. Prog. Ser., 176, 81–92.
Nijhout, H. F. (1994) Insect Hormones. Princeton University Press, Princeton, NJ.
Ohman, M. D. and Hirche, H. J. (2001) Density dependent mortality in an oceanic copepod population. Nature, 412, 638–641.[CrossRef][Medline]
Planque, B. and Batten, S. (2000) Calanus finmarchicus in the North Atlantic: the year of Calanus in the context of interdecadal change. ICES J. Mar. Sci., 57, 1528–1535.
Prestidge, M. C., Harris, R. P. and Taylor, A. H. (1995) A modelling investigation of copepod egg production in the Irish Sea. ICES J. Mar. Sci., 52, 693–704.
Radach, G., Carlotti, F. and Spangenberg, A. (1998) Annual weather variability and its influence on the population dynamics of Calanus finmarchicus. Fish. Oceanogr., 7, 272–281.[CrossRef]
Rey-Rassat, C., Irigoien, X., Harris, R. P. and Carlotti, F. (2002a) Energetic cost of gonad development in Calanus finmarchicus and C. helgolandicus. Mar. Ecol. Prog. Ser., 238, 301–306.
Rey-Rassat, C., Irigoien, X., Harris, R. P., Head, R. N. and Carlotti, F. (2002b) Egg production rates of Calanus helgolandicus females reared in the laboratory: variability due to present and past feeding conditions. Mar. Ecol. Prog. Ser., 238, 139–151.
Richardson, K., Jonasdottir, S. H., Hay, S. J. and Christoffersen, A. (1999) Calanus finmarchicus egg production and food availability in the Faroe–Shetland channel and Northern North Sea: October–March. Fish. Oceanogr., 8, 153–162.
Tande, K. S. and Miller, C. B. (2000) Population dynamics of Calanus in the North Atlantic: results from the Trans-Atlantic Study of Calanus finmarchicus. ICES J. Mar. Sci., 57, 1527.
Tittensor, D. P., DeYoung, B. and Tang, C. L. (2003) Modelling the distribution, sustainability and diapause emergence timing of the copepod Calanus finmarchicus in the Labrador Sea. Fish. Oceanogr., 12, 299–316.[CrossRef]
Visser, A. W. and Jonasdottir, S. H. (1999) Lipids, buoyancy and the seasonal vertical migration of Calanus finmarchicus. Fish. Oceanogr., 8, 100–106.
Received on September 26, 2003
; accepted on December 9, 2003
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