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This is the published version: Hays,GraemeC.,Warner,AndrewJ.andProctor,CatherineA.1995,Spatio‐temporalpatternsintheDielVerticalMigrationoftheCopepodMetridialucensintheNortheastAtlanticderivedfromtheContinuousPlanktonRecorderSurvey,Limnologyandoceanography,vol.40,no.3,pp.469‐475.

Available from Deakin Research Online: http://hdl.handle.net/10536/DRO/DU:30058282Reproducedwiththekindpermissionofthecopyrightowner.Copyright:1995,AmericanSocietyofLimnologyandOceanography

Spatio-Temporal Patterns in the Diel Vertical Migration of the Copepod Metridia lucens in theNortheast Atlantic Derived from the Continuous Plankton Recorder SurveyAuthor(s): Graeme C. Hays, Andrew J. Warner and Catherine A. ProctorSource: Limnology and Oceanography, Vol. 40, No. 3 (May, 1995), pp. 469-475Published by: American Society of Limnology and OceanographyStable URL: http://www.jstor.org/stable/2838159 .

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Limnol. Oceanogr., 40(3), 1995, 469-475 ? 1995, by the American Society of Limnology and Oceanography, Inc.

Spatio-temporal patterns in the diel vertical migration of the copepod Metridia lucens in the northeast Atlantic derived from the Continuous Plankton Recorder survey

Graeme C. Hays, 1 Andrew J. Warner, and Catherine A. Proctor Sir Alister Hardy Foundation for Ocean Science, The Laboratory, Citadel Hill, Plymouth PLI 2PB, U.K.

Abstract The archived data set collected over a 45-yr period (1948-1992) by Continuous Plankton Recorders (CPRs)

towed in near-surface waters was used to investigate the diel vertical migration of the copepod Metridia lucens in the northeast Atlantic (47-63?N and 10-30?W). Although the CPR sampling intensity was uniform during the day and the night, M. lucens was caught predominantly in samples collected at night, consistent with a normal diel vertical migration pattern involving movement from greater depth during the day to shallower depths at night. The length of time spent near the surface varied seasonally and was closely correlated (r2 = 0.80) with seasonal change in length of night. The residual variation in length of time spent at the surface was nonrandom, with more time being spent at the surface in spring before the onset of the spring bloom, and less time being spent at the surface in autumn, than that predicted from the length of night at these periods. The timing of this enhanced near-surface occupation in spring varied with latitude, occurring a mean of 3.4 d later per degree of latitude.

Diel vertical migration (DVM) occurs in a diverse range of both marine and freshwater zooplankters, with the normal pattern being movement of populations from greater depths during the day to more surface waters at night (cf. Lampert 1989). In broad terms the hypotheses to explain the function of DVM fall into two categories. First, it has been suggested that diel movement across a thermocline, with zooplankters feeding at night in warmer surface waters and resting during the day in cooler deeper waters, may provide a metabolic advantage (McLaren 1963). In addition it has been suggested that zooplankters growing at a lower temperature may attain a larger body size and hence have greater fecundity (McLaren 1974). However, evidence refutes these hypotheses because copepods living under a fluctuating temperature regime have been found not to attain a larger body size nor to have

I Current address and address for correspondence: School of Ocean Sciences, University of Wales at Bangor, Menai Bridge, Gwynedd LL59 5EY, U.K.

Acknowledgments We thank the many staff, past and present, who have analyzed

Continuous Plankton Recorder samples, Harry Hunt and Sean Nicholson for help with data extraction, and Roger Harris, Steve Coombs, John Gamble, and Alistair Lindley for comments on the manuscript.

The Sir Alister Hardy Foundation for Ocean Science is funded by the Ministry of Agriculture Fisheries and Food (U.K.), the Department of the Environment (U.K.), the Department of Fisheries and Oceans (Canada), NOAA/NSF (USA), the Eu- ropean Commission, the Consortium (Netherlands), and the Inter-Governmental Oceanographic Commission.

This paper forms part of PRIME (Plankton Reactivity in the Marine Environment), a program funded by the Natural En- vironmental Research Council, U.K., and is PRIME Contri- bution 1.

greater fecundity than those living at constant warm tem- peratures (see Lampert 1989).

Second, it has been suggested that DVM may reduce the risk of predation from visually orientating predators (Zaret and Suffem 1976). In essence the predator-evasion hypothesis suggests that since zooplankters occupying surface waters during the day may be more readily perceived, and hence consumed, by visual predators, they should move out of surface waters during the day to greater depths where illumination levels are lower and hence the probability of being perceived and consumed by visual predators is reduced. There is considerable field and experimental evidence in support of this hypothesis. For example, DVM is more marked in lakes where there are planktivorous fish and less marked in fishless lakes (Gli- wicz 1986). Furthermore, Gliwicz (1986) found that the amplitude of DVM was correlated with age of the fish population, suggesting long-term natural selection for more migratory zooplankton populations in the presence of fish. In addition, experimental manipulations have shown that some marine copepods can change from a nonmi- gratory to a migratory mode very quickly (< 1 h) upon the introduction of planktivorous fish (Neill 1990), suggesting rapid phenotypic changes in migratory behavior in addition to the slower genotypic response.

Evidence for the predator-evasion hypothesis is therefore compelling. However, DVM is not a fixed trait but shows great plasticity varying both spatially and tem- porally. It has been suggested that such changes in the extent of DVM may be a result of variations in the intensity of predation (Bollens and Frost 1989; Frost and Bollens 1992), food availability (Huntley and Brooks 1982; Johnsen and Jacobsen 1987), or subsurface light levels (Dodson 1990).

Due to the plasticity of DVM, studies covering different seasons and geographical areas, and hence providing a wide variety of biotic and abiotic conditions in which

469



470 Hays et al.

65 N

60

55

50

45

40

50 w 40 30 20 10 0

Fig. 1. The study area (shaded) in the northeast Atlantic.

variations in DVM can be observed, may shed further light on both the ultimate and proximate causes of this behavior. To examine spatio-temporal variations in DVM we therefore used the extensive data set that has been collected with Continuous Plankton Recorders (CPRs). CPRs have been towed in the northeast Atlantic and North Sea for several decades. They are towed in near-surface waters (mean depth, 6.7 m) (Hays and Warner 1993), collecting a variety of zooplankton and phytoplankton (Colebrook 1960). Traditionally the data set has been used to examine patterns in plankton abundance. How- ever, since the recorders are towed at a fixed, near-surface depth there is the potential to use the data to examine DVM because species that are migrating would be expected to be caught predominantly in samples collected at night. Here we use the CPR data to examine DVM in the calanoid copepod Metridia lucens because this species is frequently caught by the recorders, has a wide geographical range, and is known to exhibit pronounced DVM (Oceanogr. Lab. 1973).

Methods

Since 1948, CPRs have been towed regularly from ships of opportunity in the North Sea and northeast Atlantic. Water entering the recorder passes along a water tunnel and then through a silk mesh of 270-,Am aperture. This silk mesh consists of a continually moving roll so that fresh silk is constantly entering the water flow. The silk and entrapped plankton then passes into a storage tank containing Formalin. Upon return of the CPR to the laboratory, the silk roll is unwound and cut into sections representing 10 nm (- 18.5 km) of tow. The abundance of various plankton groups is then quantified in a routine manner and from a record of the time and position that the CPR was deployed and recovered on each tow, the position and local time of the midpoint of each 10-nm sample is calculated (Colebrook 1960). All these data are then stored in an electronic database. The mean towing

speed of CPRs is -6.7 m s-', so a 10-nm sample takes -45 min to collect. The CPR survey continues to be operative to the present day and is currently under the auspices of the Sir Alister Hardy Foundation for Ocean Science (SAHFOS), Plymouth.

In the routine CPR plankton analysis those M. lucens that are identified are predominantly adult females. From the CPR database the position, local time, and abundance of M. lucens were extracted for every sample taken between 1948 and 1992 in the area bounded by 47-63?N and 10-30'W (Fig. 1). This region was selected because the water is predominantly deep, and hence patterns of DVM were unlikely to be complicated by variations in water depth, and because the abundance of M. lucens in the CPR samples from this area is high (Oceanogr. Lab. 1973). The length of the night (i.e. sun elevation <00) at different times of year in this area was calculated with Telonics satellite predictor software (Telonics Inc.). The mean monthly cloud cover was calculated from routine meteorological observations made at ocean weather stations India (19?W, 590N) and Juliett (19?W, 530N) between 1947 and 1982.

Results

A total of 34,099 samples were collected in the study area; of these, 8,178 contained at least one specimen of M. lucens. The mean latitude of these samples was 55?N. The sampling intensity was equally distributed through the day and night with -3,000 samples being taken in each 2-h period of the 24-h cycle (Fig. 2a). However there was a clear diel pattern to the times of day when M. lucens was caught: this species was caught more often in samples taken around midnight and less often in samples taken around midday (Fig. 2b).

To calculate the length of time that M. lucens was present near the surface, we first expressed the time of each sample in relation to local midnight. When expressed in this way, the frequency distribution for the times of day when M. lucens was caught followed a normal distribution centered on midnight (Fig. 3a). Furthermore, when M. lucens was found in samples taken at night, their absolute numbers in those samples tended to be higher than when specimens were found in samples taken during the day (Fig. 3b). To give an index of the length of time that M. lucens occupied the near-surface waters in different times of year and in different geographical areas, we calculated the standard deviation (6) of the distribution consisting of the local time in hours since midnight that M. lucens was found in samples (x) and the numerical abundance of M. lucens in those samples (j). The equation for this calculation is (cf. Bailey 1981)

62 = 1 K(fX2) - ( fX)21 (1)

The standard error (SE) of this standard deviation (i.e. measure of the accuracy with which 6 was estimated) was calculated as (cf. Sokal and Rohlf 1969)



Diel vertical migration 471

4000 X)_ (a)

E 3000-

(lCM o 2000-

.0 Q

E 1000-

Or-_ 1 3 57 91113151719 2123

2000- _n (b)

E 1500-

o a. 1000 m _

0)

E 500 z

0- 1 3 5 7 9 11131517192123

Local time (hours) Fig. 2. [a.] Total number of samples collected in the study

area at different times of day. [b.] Number of samples collected at different times of day that included at least one Metridia lucens.

SE = (2n)1/2 (2)

where n is the total number of M. lucens in that data set. To illustrate the calculation of 6, consider three simple

hypothetical data sets for the times of day when M. lucens was found on CPR samples (Table 1). In cases 1 and 2 there are identical distributions in the occurrence near the surface, but there are different abundances with twice as many specimens in each sample in case 2 compared to case 1. However, this difference in absolute abundance has no noticeable effect on the calculated value of 6, which is 2.0 in both cases. In case 3, M. lucens was caught both earlier and later in the night than in either cases 1 or 2, and 6 is consequently larger (( = 3. 1), reflecting this longer period of time spent by the population near the surface.

There was a marked seasonal variation in the length of time that M. lucens spent near the surface (Fig. 4a). Of this variation, 80% was explained by the mean monthly length of night (Fig. 4c). Thus in midsummer, nights were about half as long as they were in midwinter; similarly, M. lucens spent about half as long near the surface.

There was, however, an apparently nonrandom distri-

2000 (a)

~.1500 E 4-

? a.1000 -

E 500- 3

0Li -11-9 -7 -5-3-1 1 3 5 7 911

12 -

0) E Z 10

m* 8 -

E

0 6-

E 4- z

-11-9 -7-5-3 -1 1 3 5 7 9 11

Local time (h from midnight) Fig. 3. [a.] Total number of samples per 2-h interval that

included at least one Metridia lucens, with time expressed in relation to local midnight (i.e. - 1 represents the number of samples collected 0-2 h before local midnight, + 1 represents the number of samples collected 0-2 h after midnight, etc.). [b.] For the 8,178 samples containing at least one M. lucens, the mean number of M. lucens per sample in relation to local midnight.

bution in the residual length of time spent at the surface. In spring/early summer M. lucens tended to spend more time at the surface and in late summer/autumn less time at the surface than that predicted on the basis of length of night. This residual variation was not significantly correlated with mean monthly cloud cover (n = 12 months, F1,,o = 0.2, P = 0.68).

To investigate how this more prolonged surface occupation in spring/early summer compared to late summer/autumn varied with latitude, we did not use length of night as a reference point with which to compare the time at the surface since illumination levels at "night" (i.e. when the sun is below the horizon) vary latitudinally. Instead, to calculate the date when this more prolonged surface occupation in spring/early summer occurred, we compared the length of time at the surface for equivalent 20-d periods either side of the summer solstice (21 June). Thus the mean daily length of time spent at the surface



472 Hays et al.

5 l + (a) 2 (c)

14 - 0)

3- l

2 -2 T--- J F MAMJ JA SON J FMAMJ J ASON D

18- ~-16 - (b) 14

-

012-

8-

6- J F MAMJJ AS O D

Fig. 4. [a.] Mean length of time (6?2 SE) that Metridia lucens was present near the surface in each month. [b.] Mean length of night in each month at 55?N. [c.] Graphs in panels a and b reduced to zero mean and unit variance to facilitate visual comparison. There was a sig- nificant linear relationship between length of time that M. lucens was present at the surface in each month (- - -) and mean length of night in each month ( ). (n = 12 months, F,1,0 = 42, r2 = 0.80, P < 0.001.)

Table 1. Three theoretical distributions for the number of specimens in samples collected at different times of day. The calculated value for 6 is the same in cases 1 and 2, indicating similar lengths of surface occupation; 6 is greater in case 3, indicating a longer surface occupation. x-local time in hours since midnight; f-numerical abundance of specimens.

Case 1 Case 2 Case 3

x f

-12 0 0 0 -10 0 0 0 -8 0 0 0 -6 0 0 5 -4 5 10 30 -2 30 60 30

0 30 60 30 2 30 60 30 4 5 10 30 6 0 0 5 8 0 0 0

10 0 0 0 12 0 0 0

6 2.0 2.0 3.1

between 1 and 20 June was compared with that between 22 June and 9 July, the mean daily length of time spent at the surface between 12 and 31 May was compared with that between 10 and 29 July, and so on through the year. The increased length of time that M. lucens spent at the surface in spring compared to autumn was clearly seen by this analysis (Fig. Sa). For example, for the entire data set, in the period 4-24 April (midpoint = 14 April; i.e. day 103), M. lucens spent 1.5 times longer near the surface than in the equivalent period the other side of the summer solstice (22 July-I 1 August, midpoint = 1 August; i.e. day 243). The date in the first half of the year when M. lucens spent longest at the surface when compared to the second half of the year varied with latitude (Fig. Sb), being 3.4 d later per degree of latitude (95% C.L. 2.8-4.0 d).

Discussion

In previous field studies, DVM has tended to be quantified by taking samples at a series of discrete depths and then examining day-night differences in these depth distributions (cf. Bollens and Frost 1989; Frost and Bollens 1992). This approach gives useful data on the amplitude




of migration (i.e. the vertical distance that a population migrates through the water column), but it tends to give poor resolution on the timing of this migration, with typ- ically only a few nighttime profiles being compared with a few daytime profiles. In contrast the fixed depth sampling by CPRs cannot be used to describe the amplitude of vertical migration, but the large number of samples that are collected can be used to accurately quantify the timing of movement into near-surface waters and the length of time spent near the surface.

The predator-evasion hypothesis views DVM as a trade- off between the cost (a reduced foraging time in the food- rich surface waters) and the benefit (a reduced predation risk) of moving to a greater depth during the day (Lampert 1989). If these relative costs and benefits change, then changes in the length of time that a species spends at the surface would be expected. A higher food level may, for example, decrease the cost of DVM since when food is abundant, copepods may feed to satiation after which time surface occupation provides no further benefit (i.e. food consumption stops). Such modification of DVM by food availability has indeed been shown. For example, Huntley and Brooks (1982) and Johnsen and Jacobsen (1987) found that when food availability was low, individuals ceased to migrate vertically and remained con- tinuously in the surface waters, but when food availability was higher the species migrated. Conversely if the abundance of planktivorous fish increases then the benefits of DVM may rise and hence a greater extent of DVM induced. Again such predator-induced modification of DVM has been reported (Bollens and Frost 1989; Frost and Bollens 1992; Neill 1990). Similarly subsurface light levels may alter the costs and benefits associated with DVM. For example, Dodson (1990) found that generally in more turbid waters the amplitude of vertical migration was reduced. Presumably in such conditions the lowered subsurface illumination levels reduce the probability of zooplankton being perceived by fish, thus reducing the benefits derived from DVM.

For M. lucens in the northeast Atlantic we found that the major seasonal changes in length of time spent near the surface were highly correlated with seasonal changes in length of night. The implication of this correlation is that changes in predation intensity need not be invoked to explain the major seasonal changes in the timing of DVM behavior by this species. However, while our results suggest that length of night is the proximate cue causing seasonal changes in length of surface occupation, these results still support predator evasion as the ultimate cause of DVM. If vertical migration functions to reduce the risk of predation, then zooplankton should restrict their surface foraging to times when illumination levels are sufficiently low to minimize their risk of being perceived (i.e. they will have a dark illumination foraging window near the surface). If predation intensity remains constant then a migrating zooplankton population would be expected to change the length of time it spends near the surface in accord with variations in this dark illumination foraging window, as was found for M. lucens (Fig. 4).

Day of the year 23 43 63 83 103 123 143 163

1.6

(a) (l 1.2 - ~

1.0 -

1 0.8 -

0.6 -

0.4 I

323 303 283 263 243 223 203 183 Day of the year

150 140- 130- lbl

4 120 - 0 110

0

80 70

48 50 52 54 56 58 60 62

Latitude (ON) Fig. 5. [a.] Comparison of the length of time that Metridia

lucens was present in near-surface waters for 20-d intervals either side of the summer solstice between 47 and 63?N. The Y-axis = Ts/a, ITend, where Tsta,, is length of time at the surface for that 20-d period in the first half of the year and Tend is length of time at the surface in the equivalent period (i.e. equidistant from the summer solstice) in the second half of the year. The midpoint of the periods in each comparison are shown at the top (first half of the year) and bottom (second half of the year) of the graph. Deviations above 1 (shaded) thus reflect a greater amount of time at the surface in the first half of the year and vice versa. [b.] Mean timing of the positive deviations from panel a, calculated for different latitudes. These values represent when M. lucens spent longest at the surface in the first half of the year compared to the equivalent period in the second half of the year. This timing was significantly later farther north. Timing (day of year) = 3.41 x lat (ON) - 82.7. (n = 8 latitudes, F16 = 132, r2= 0.98, P < 0.001.)

There was, however, an apparently nonrandom pattern to the residual variation in length of time spent at the surface (Fig. 4c). This pattern was probably not caused by cloud-cover-induced seasonal changes in the near-surface illumination levels because the residual variation was not correlated with mean monthly cloud cover at the two



474 Hays et al.

ocean weather stations in the study area. Independent of variations in length of day-night, there would, therefore, seem to be a seasonal change in the trade-off between the costs and benefits of DVM. Thus in spring it would appear that the benefits of DVM decreased or the costs increased so that M. lucens spent longer at the surface, and vice versa in autumn. Such cost-benefit changes could poten- tially occur through variations in availability of food or intensity of predation. Testing these hypotheses would, however, be extremely difficult. First, the principal visual predators of M. lucens in this area are not known and, even if these predators were identified, predation intensity might not be a simple function of their numerical abundance. Second, M. lucens is an omnivore, consuming a variety of phytoplankton and small zooplankton and showing prey selectivity when offered a heterogeneous diet (Haq 1967). Thus the "availability of food" may not correlate with a simple index such as chlorophyll concentration, but is likely to be a function of chlorophyll concentration, phytoplankton species, and the concentration of small zooplankton such as naupliar stages of copepods. In an alternative attempt to shed some light on the cause of the more prolonged surface occupation in spring compared to autumn, we therefore examined how the timing of this phenomenon varied with latitude.

The timing of the spring bloom between 47 and 60?N at 20?W has been reported in detail by Taylor et al. (1993) who described the seasonal cycle of chlorophyll abundance in phytoflagellates, diatoms, and dinoflagellates. Measuring the timing of the peak in diatom abundance from figure 6 of Taylor et al. (1993) shows it is delayed by 3.2 d per degree of latitude [day of the year of peak in diatom abundance = 3.20 x lat (?N) - 27.3], which is very similar to, and not significantly different from, the latitudinal variation in the seasonal timing of the enhanced occupation of surface waters by M. lucens in spring (3.4 d per degree of latitude, Fig. Sb). The close similarity between the gradients of these two relationships suggests that the enhanced near-surface occupation by M. lucens in spring may be causally linked with the spring phytoplankton bloom. However, the timing of the enhanced surface occupation by M. lucens was earlier than the peak in diatom abundance. For example, using the equations for the two functions shows the peak in the enhanced surface occupation at 50?N is on day 88 (29 March), but the peak in diatom abundance is on day 133 (15 May) (a difference of 45 d); at 60?N the timings are days 122 and 164 (2 April and 13 June) (a difference of 42 d).

During winter, M. lucens, in common with other copepods, may undergo a decrease in dry weight associated with lipid catabolism (Hopkins et al. 1984; Robertson 1968; Tande 1982) and then in spring grows rapidly and has high rates of egg production (Smith and Lane 1988). The benefits of high fecundity at this time of year may be large because food (i.e. phytoplankton) for the devel- oping nauplii is abundant (cf. Taylor et al. 1993) and hence their rate of development and probability of sur- vival may be increased. If egg production is tightly cou- pled with the onset of the spring bloom, then gonadal maturation would need to occur before the onset of the

bloom. Such prebloom gonadal maturation has indeed been reported for several calanoid copepods. For example, Smith (1990) reported that in the Fram Strait Calanus hyperboreus, Calanus glacialis, Calanusfinmarchicus, and Metridia longa all had well-developed gonads prior to the spring bloom, and Nielsen and Richardson (1989) reported fully mature M. lucens in the North Sea in Feb- ruary and March, prior to the spring bloom in this area. The prolonged surface occupation by M. lucens before the spring bloom in the northeast Atlantic and the variation in the timing of this phenomenon at different latitudes (Fig. 4b) may be the result of greater benefits associated with surface occupation at this time since food availability is relatively low (and hence individuals may be unable to feed to satiation, Smith and Lane 1988) and yet the benefits of food consumption are large (increased somatic growth and hence synchronization of egg production with the spring bloom).

In conclusion, the length of time that M. lucens spent near the surface of the northeast Atlantic varied seasonally in accord with length of night. This covariation suggests that length of night is the main proximate cause of seasonal changes in the timing of DVM by this species, but predator evasion is the ultimate cause. The pattern of the residual seasonal variation at different latitudes was consistent with an increased benefit associated with prolonged surface occupation prior to the onset of the spring phytoplankton bloom.

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BOLLENS, S. M., AND B. W. FROST. 1989. Predator-induced diel vertical migration in a planktonic copepod. J. Plankton Res. 11: 1047-1065.

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DODSON, S. 1990. Predicting diel vertical migration of zooplankton. Limnol. Oceanogr. 35: 1195-1200.

FROST, B. W., AND S. M. BOLLENS. 1992. Variability of diel vertical migration in the marine planktonic copepod Pseu- docalanus newmani in relation to its predators. Can. J. Fish. Aquat. Sci. 49: 1137-1141.

GLIwIcz, Z. M. 1986. Predation and the evolution of vertical migration behavior in zooplankton. Nature 320: 746-748.

Haq, S. M. 1967. Nutritional physiology of Metridia lucens and M. longa from the Gulf of Maine. Limnol. Oceanogr. 12: 40-51.

HAYS, G. C., AND A. J. WARNER. 1993. Consistency of towing speed and sampling depth for the Continuous Plankton Recorder. J. Mar. Biol. Assoc. U.K. 73: 967-970.

HOPKINS, C. C. E., AND OTHERS. 1984. Ecological investigations of the zooplankton community of Balsfjorden, northern Norway: An analysis of growth and overwintering tac- tics in relation to niche and environment in Metridia longa (Lubbock), Calanusfinmarchicus (Gunnerus), Thysanoessa inermis (Kr0yer) and T. raschi (M. Sars). J. Exp. Mar. Biol. Ecol. 82: 77-99.

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JOHNSEN, G. H., AND P. J. JACOBSEN. 1987. The effect of food limitation on the vertical migration in Daphnia longispina. Limnol. Oceanogr. 32: 873-880.

LAMPERT, W. 1989. The adaptive significance of diel vertical migration of zooplankton. Funct. Ecol. 3: 21-27.

McLAREN, I. A. 1963. Effect of temperature on growth of zooplankton and the adaptive value of vertical migration. J. Fish. Res. Bd. Can. 20: 685-727.

1974. Demographic strategy of vertical migration by a marine copepod. Am. Nat. 108: 91-102.

NEILL, W. E. 1990. Induced vertical migration in copepods as a defence against invertebrate predation. Nature 345: 524- 526.

NIELSEN, T. G., AND K. RICHARDSON. 1989. Food chain struc- ture of the North Sea plankton communities: Seasonal variations of the role of the microbial loop. Mar. Ecol. Prog. Ser. 56: 75-87.

OCEANOGRAPHIC LABORATORY (EDINBURGH). 1973. Continu- ous Plankton Records: A plankton atlas of the North At- lantic and the North Sea. Bull. Mar. Ecol. 7: 1-174.

ROBERTSON, A. 1968. The Continuous Plankton Recorder: A method for studying the biomass of calanoid copepods. Bull. Mar. Ecol. 6: 185-223.

SMITH, S. L. 1990. Egg production and feeding by copepods

prior to the spring bloom of phytoplankton in Fram Strait, Greenland Sea. Mar. Biol. 106: 59-69.

AND P. V. Z. LANE. 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 Res. 8: 485-509.

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ton community of Balsfjorden, northern Norway: Gener- ation cycles, and variations in body weight and body content of carbon and nitrogen related to overwintering and reproduction in the copepod Calanusfinmarchicus (Gun- nerus). J. Exp. Mar. Biol. Ecol. 62: 129-141.

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Submitted: 29 April 1994 Accepted: 28 September 1994

Amended: 18 October 1994



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