POPULATION GROWTH AND VERTICAL ... - Science Direct

Netherlands Journal of Sea Research 16:185-194 (1982) POPULATION GROWTH AND VERTICAL DISTRIBUTION OF CALANUS HELGOLANDICUS IN THE CELTIC SEA by R. W I L L I A M S and D. V. P. CONWAY J~atural EnvironmentResearch Council, Institutefor Marine EnvironmentalResearch, Prospect Place, The Hoe, Plymouth, PL1 3DH, Devon, GreatBritain CONTENTS I. II. III. IV. V. VI.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . Materials and Methods . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . .

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185 186 186 190 193 194

I. I N T R O D U C T I O N

Calanus helgolandicus Claus is one of the most i m p o r t a n t planktonic herbivores in the shelf seas a r o u n d the U n i t e d K i n g d o m . In order to understand its contribution to the dynamics of the ecosystem, it is essential to investigate the vertical distribution and seasonal m i g r a t o r y b e h a v i o u r of its d e v e l o p m e n t a l stages, as well as the overwintering strategy of the species; those are the objectives of this paper. Earlier workers who investigated the vertical distribution of Calanus spp. (RussELL, 1927; GARDINER, 1933; NICHOLLS, 1933; MARSHALL, NmHOLLS & ORR, 1934) dealt primarily with Calanusfinmarchicus with the exception of RUSSELL who worked in the P l y m o u t h area. WILLIAMS & CONWAY (1980) have shown differences in the vertical distribution of these two congeneric species (C. helgolandicus and C. jqnmarchicus) in spring from U . K . shelf seas which exposed t h e m to ranges of temperature and particulates that could affect their feeding strategies and hence their intermoult and generation times. Since the taxonomic separation of these two species, there has been little detailed work on the vertical distribution of Calanus helgolandicus from the shelf seas adjoining the U n i t e d K i n g d o m . T h e present p a p e r is an a t t e m p t to rectify this. Acknowledgements.~e thank the masters and crews of the N E R C research vessels and our colleagues of this Institute involved in the Celtic Sea p r o g r a m m e who p r o v i d e d data. This work forms part of the

186

R. WILLIAMS & D. V. P. CONWAY

Open-Sea Plankton Programme of the Institute for Marine Environmental Research, a component of the Natural Environment Research Council. II. MATERIALS AND METHODS

Calanus helgolandicus were collected from RRS "John M u r r a y " and RRS "Challenger" during 8 cruises in 1978 and 1979 in the Celtic Sea. The majority of vertical samples were taken at or around the centre (51°30'N 05°52'W) of an 8 × 10 nautical mile site, (51°26'N 06°00'W, 51°26'N 05°44'W to 51°34'N 05°44'W, 51°34'N 06°00'W). Zooplankton samples were obtained by oblique hauls with Longhurst-Hardy Plankton Recorders (LHPR) (LoNGHURST, REITIJ, BOWER & SEIBERT, 1966; LONGHURST& W I L L I A M S , 1976). The L H P R was deployed as near as possible to the sea-bed, using a N I O acoustic telemetry system, and samples were collected at intervals of approximately 5 m depth to the surface. The ambient temperature, sample depth range and flow of water through the net mouth were recorded simultaneously with each plankton sample. The mesh of the plankton net and filtering gauzes used in the cod-end was 280/lm. O f the 29 L H P R oblique hauls collected during this sampling programme only 12 are illustrated here. Measurements were made on pumped sea water ti'om 3 m and water bottle samples from the surtace to the maximum depth tot temperature and chlorophyll a. III. RESULTS The geographical distribution and mean seasonal variability in abundance of Calanus helgolandicus (copepodite stage V and adults), ti'om sampling at 10 m with the Continuous Plankton Recorder in the North Atlantic Ocean from 1958 to 1977, are given by COLEBROOK(1982). It was most abundant in the shelf seas to the west of the British Isles and in the southern part of the survey in the North Atlantic Ocean. C. helgolandicus was abundant at 10 m from May to October in the Celtic Sea and was also present there throughout the winter months although absent from the surtace waters of the open ocean at this time. A similar development of the copepod in the Celtic Sea was observed t~om the L H P R hauls in 1978, the numerical peak occurring in August and the peak of dry weight in early October (Fig. 1). During 1978 the values of chlorophyll a in the Celtic Sea were highest in May and the sea-surtace temperature rose from a winter minimum of 7.7 ° C to a summer maximum of 17.0 ° C.

VERTICAL DISTRIBUTION

CALANUS

187

The mean concentration of chlorophyll a at 3 m on 28 March 1978 was 0.26 ± 0.08 m g ' m - 3 (n = 13); that is the winter level tor the Celtic Sea. Copepodite stages I to III were already present in the water column in a L H P R haul taken on 27 March which implies that the onset of breeding and development of the copepod preceded the spring phytoplankton bloom. mg.m a

"C

Numbersper haul

0 ~J, -F-M, A- M=J- ~

mg.m z

,

d ASOND

l0

Fig. 1. Chlorophyll a (mg" m -3) measured from 3 m depth and the sea-surtace temperature (°C; broken line), together with numerical abundance (per haul. 10-3) and dry weight biomass ( m g . m -2; broken line) ofCalanus helgolandicusfrom the Celtic Sea, 1978 calculated from LHPR hauls.

By the latter halt" of M a y the sea-surtace temperature had increased to 12.3 ° C and the thermocline was well established between 15 and 20 m (Fig. 2a). Total numbers of Calanus helgolandicus had increased fourtold over the numbers present in March due to large numbers of copepodite stages I to III; in a day haul taken on 21 M a y (Fig. 2a) these stages were distributed below the thermocline and euphotic zone. The vertical distribution of the summed total of stages I to VI showed an even distribution below the thermocline (Fig. 2a). Similar vertical distribution of copepodites I to III underlying the thermocline were observed during M a y in the Celtic Sea in 1977 (WILLIAMS& CONVCAY, 1980). The spring peak of phytoplankton occurred at 3 m during May; surveys on 16 and 23 M a y gave values of chlorophyll a of 4.02 2- 2'.13 m g ' m 3 (n 30) and 4.28 ± 2.76 m g ' m - 3 (n -- 30) and sea-snrtace temperatures of 10.98°C ± 0.27 (n -- 30) and 12.34°C ±: 0.43 (n 30) respectively (Fig. 1). The sea-surtb, ce temperature had risen to 14.4 ~ C by earlyJuly and a pronounced 3 ° C thermocline existed between 25 and 35 m (Fig. 2b). The young copepodites from a day haul were tound above the thermocline. Total numbers of all developmental stages of Calanus helgolandicus were evenly spread throughout the water column (Fig. 2b). Numbers in July were lower than those taken in M a y but the mean dry weights of copepodite stage V and adults were greater (the highest recorded tor the year) and the population biomass greater than in May (Fig. 1). The

188

R. W I L L I A M S

& D. V . P. C ( ) N W A Y

average chlorophyll a at 3 m on July 1 reached a summer m i n i m u m of 0.44 ± 0.43 m g ' m 3 (n = 30). This was reflected in water bottle samples (from 0 to 70 m) taken on 1 July; the integrated m e a n chlorophyll value was 14.2 mg" m -2 (range 3.9 to 30.5 m g ' m -2; n 4';). Calanus helgolandicus reached its m a x i m u m numerical a b u n d a n c e (20 000 m - 2 ) during late August (Fig. 2c) w h e n the surtace temperature was 17.0 ~ C. Copepodite stages I to I V were above the t h c r m o c I

2Q 40

rn

6o

ilil....

80

Itl,

1510

0

I

I1[

2,9 40 0

2c

=884

14

40 0

=762

20 40

20

4,3 C

2C 4,9 0

20

40

n=131

8L

i~0 i~2 °C

0

4O

8o 80Jn,52

n~221

6

195

,/ i

10 112 14 ~C o

n 20 561 12 14

16"C

2O

40 6o 80 j n ° 48

05

8

n = 2839

, 8803

1 5 ~ 2 ~ "c

Fig. 2. Calanus helgolandicus. Vertical distribution of copepodite stages I to VI (separately and combined) ticom LHPR hauls on (a.) 21 May (10.03 h GMT), (b.) 3 J u b (11.13 h GMT), (c.) 23 August (12.05 h GMT) and (d.) 2 October (11.09 h GMT) from the Celtic Sea, 1978. The numbers in the hauls are plotted in 5 m depth intervals as percentages of the total numbers (n) present. The temperature profiles are also plotted.

VERTICAL DISTRIBUTION CALANUS

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line, stage V less strikingly so and the adults almost entirely below the thermocline. In grid surveys on 18 and 20 August chlorophyll at 3 m had increased 5 fold over the July values and gave means of 1.48 ± 0.84 and 2.29 ± 2.03 mg" m-3 while vertical profiles taken on 21 and 22 August gave an integrated mean chlorophyll a value of 50.8 m g ' m -2 (range 41.4 to 118.4 m g ' m - 2 ) , approximately 4 times the value determined in July. By October the numbers of Calanus helgolandicus had decreased to less than halt'the August figure and copepodite stages IV and V were numerically dominant. Although the older stages and adults were less numerous, they were more than twice the weight of those collected in August (for the same total length) so that the peak of the dry weight copepod biomass occurred in October (Fig. 1). The majority of all the developmental stages was found above the thermocline. The thermocline was at a depth of 40 to 45 m (Fig. 2d) and the sea-surface temperature on 2 October was 13.8 ° C, 3.2 ° C less than in August. Following the breakdown of the temperature structure in late autumn or early winter, the water column was isothermal at 9.4 ° C in 2 hauls taken at 13.08 h G M T , 2 0 J a n u a r y and 01.00 h G M T , 21 J a n u a r y 1979 (Fig. 3a and b). The winter population of Calanus helgolandicus consisted ofcopepodite stages V and VI which were distributed throughout the water column with the greatest abundance below 55 m. Only 3 copepodites at stage IV were found, 1 in the day haul and 3 in the night haul. Analyses of gut contents showed that Calanus helgolandicus was actively feeding in winter and by late March all stage V copepodites had matured and developed into adults. A pair of oblique hauls, one by night and one by day in March (when all but a tbw specimens were females) showed an obvious diel migration; adult females migrated to the upper 25 m of the water column during the night (Fig. 3c';. The v

n -

v

• 192

Vl

Vl

20

20

n = 91

40 %

40

vI

VI

20

20

40 %

n = 158 °78

n=4

80

80 t

8 a

b

9

10"C

lOOd

i

c

Fig. 3. Calanushelgolandicus.Vertical distribution ofcopepoditestages V (a.) and VI (b.) [iom LPHR hauls on 20January (13.08 h GMT) and 21 January (01.00 h GMT), and of stage VI (c.) from LHPR hauls on 24 March (11.53 h GMT) and 23 March (23.31 h GMT) from the Celtic Sea, 1979, The temperature profiles are also plotted.

190

R. W I L L I A M S

& D. V. P. C O N W A Y

water temperature measured during these hauls was 8 . 3 ° C and the water column was isothermal from the surface to 100 m. Dry weights were determined for the copepodite stages from all LHPR hauls. These weights were used to determine a dry weight biomass profile for the day and night Calanus populations during the seasons (Fig. 4). 21/5/1978 m o

20 10

0

10 20

3/7/1978 20 10

0

23/8/1978

10 20

20

10

10 20

%

20 40 60 80 i .J 110 12 14

2/10/1978

12 1~1 lt6"C 2413/1979

20/1/1979

2O 40 6O

7 cog

17

5

80 I

1o0

1o 12 I~

8

9

10

' ;-c

Fig. 4. Calanushelgolandicus.Vertical distribution of dry weight biomass, ot"6night and day pairs of LHPR oblique hauls from the Celtic Sea, plotted in 5 m depth intervals as a percentage of the total biomass present. The temperature profiles are also plotted. IV. D I S C U S S I O N The results from our series of LHPR hauls showed that the population of Calanus helgolandicus increased slowly from March through May and reached a numerical peak in abundance, approximately 100 times the winter level, in August; thereafter decreasing in numbers until a small population of late copepodite stages remained through the winter months. This is assumed to be a typical seasonal cycle for the Celtic Sea and is supported by the longer-term results from the CPR survey; a maximum in late summer or autumn has been reported for C. helgolandicus from the southern North Sea also (COLEBROOK, REID & COOMBS, 1978: fig. 4). The LHPR hauls taken in January and March 1979 sampled the overwintering population which consisted of copepodite stage V and adults. These were overwintering but they were not in a state of dia-

VERTICAL DISTRIBUTION CALANUS

191

pause (that is a period of suspended growth and development accompanied by reduced metabolism) which might have been expected in Calanus helgolandicus, living near the extreme northern range of its geographical distribution, because of the adaptive value of diapause in resisting unfavourable conditions. We have observed C. helgolandicus from the winter population actively feeding in experiments conducted onboard ship in January, numerous specimens in samples at this time had recently fed and adult females were taken with fully developed ovaries and mature eggs in their oviducts. Also females from the Plymouth area, which has a winter temperature similar to that of the Celtic Sea, can be induced to spawn by bringing them into the laboratory at any time through the winter period. The fact that Calanus, in shelf seas around the United Kingdom, does not enter a period of diapause or dormancy has been noted by MARSHALL • ORR (1958) and BUTLER, CORNER & MARSHALL (1970). These authors concluded that the copepod lives economically during the winter months in deeper, colder waters depending on predation of microzooplankton and detritus (MARSHALL, 1924; PAFFENH6FER & STRICKLAND, 1970; CORNER et al., 1974). Our analyses of gut contents of winter specimens have revealed large quantities of unidentifiable detritus together with remains of diatoms and crustaceans and would therefore support this interpretation. In contrast to these observations, HIRCHE (1979, quoted in the following reference) and HALLBERG & HIRCHE (1980) have observed Calanus helgolandicus entering a state of diapause in the winter months off the west coast of Sweden. This diapause was associated with large physiological changes, such as reduced metabolism, discontinuation of feeding and development and reduced activity of digestive enzymes (HALLBERG ~ HIRCHE 1980). HIRCHE has shown that the digestive enzyme trypsin was hardly detectable and amylase very low in the mid-gut of overwintering stage V copepodites. A diapause condition in copepods has been suggested by USSINO (1938), ANDREWS (1966), CONOVER (1962) and ELGMORK (1967), a state which HALLBERG & HIRCHE (1980) believed to be regulated by neurosecretions as suggested by CARLISLE & PITMAN (1961). From our data on Calanus helgolandicus we concluded that this copepod does not enter a diapause in winter on the shelf sea to the south-west of the United Kingdom, but does show a much slower rate of development and possibly reduced metabolism. It seems that the relatively shallow water column, temperature, available tbod, and possibly other factors, on the shelf sea prevent this copepod from entering a winter diapause as it does for 4 to 5 months in the deeper and colder layers of oceanic waters. By late March the overwintering population of copepodites stage V had moulted into adults. This was apparent from the hauls taken on 24

192

R. W I L L I A M S

& D. V. P. C O N W A Y

March 1979 when the population consisted solely of copepodite stage VI; the female to male sex ratio in these hauls was 99 : 1. The majority of adult females were migrating towards the upper layers (0 to 25 m) before midnight and we assume, from the mature state of the ovaries of a large proportion of these females, that this was an egg-laying migration. Throughout the winter months ovigerous females were present but no young developmental stages were observed in our hauls; it is of" course possible that eggs were liberated then, but suffered reduced viability, or high mortality. During May, when the spring peak ofphytoplankton occurred and a pronounced thermocline was already established between 15 and 20 m, the young copepodites were fbund below the thermocline while the copepodite stages IV and V made pronounced night vertical migrations at this time. It is probable that these older copepodites were part of"the first generation which developed from the adults seen in early March 1978. This is based on an estimate of a generation time from egg to adult, for Calanus helgolandicus of 40 d derived by I)r P. Burkill (of I.M.E.R.) from on-deck incubation experiments carried out at a temperature of 12 ° C. Much of the early development of the young stages of this first generation must have taken place at 8 ° C and in May the young copepodites, below the thermocline, were still exposed to a temperature of 8.6 ° C. It seems possible that the duration of a generation at a temperature of approximately 8 ° C for the first cohorts would be in excess of 60 d. The vertical distributions of the young stages observed in May in the colder waters below the thermocline would contribute to this long development period. Particulate matter profiles down the water column suggested that food was available for the young stages but the quality of food was unknown. At the end of May, the young copepodites changed their behaviour and were tbund above the thermocline both day and night in a water temperature of 14.4 ° C. The eggs released by the females during this month, either through increased survival, viability or female fecundity, gave rise to the maximum numbers found during August. The generation time for Calanus heIgolandicus at 16 ° C was approximately 30 d in Dr Burkill's experimemcnts; at this temperature in July, development of all copepodite stages was above the thermocline, so that ship-board incubation experiments, using pumped sea water, should accurately reflect development rates of" C. helgolandicus in the euphotic zone. The vertical spatial distribution of the copepodite stages I to IV were similar in July and August although the adult stages in August remained below the thermocline at a temperature of 13 ° to 13.5 ° C with 75°G of the adult population aggregated between 65 and 70 m in a haul on the 23 August during the day. The population below the thermoc-

VERTICAL DISTRIBUTION

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193

line is probably able to conserve its energy store by reduction of metabolic activity and oxygen demand (MCLAREN, 1963) by avoiding higher surface (17 ° C) temperatures. The main environmental variables governing the growth and development of this copepod are the available food and the temperature of the water. It is the natural variation of these biotic and physical variables and the species' response to them which govern the level of success of the species each year. We have identified, using a selection of vertical profiles, a pattern of behaviour of this copepod throughout the year which can be consistently observed in the shelf seas to the southwest of the U.K. V. SUMMARY

Calanus helgolandicus over-winters in the shallow waters (100 m) of the Celtic Sea as copepodite stages V and VI; the minimum temperature in winter is approximately 8.0 ° C. This over-wintering is not a true hibernation or dormancy, accompanied by a reduced metabolic state with a discontinuation of feeding and development, but more of a lowered activity, involving reduced feeding and development, with predation on available microzooplankton and detritus. Analysis of specimens from the winter population showed that copepodite stages V and VI were actively feeding and still producing and possibly liberating eggs. The absence of late nauplii and young copepodites in the water column until late March indicated that there must be a high mortality of these winter cohorts. The copepodites of the first generation appeared in April-May, the younger stages, copepodites I to III, being distributed deeper in the water column below the euphotic zone and thermocline. This distribution would contribute to a much slower rate of development. By August the ontogenetic vertical distributions observed in the copepodites were reversed, the younger stages occurring in the warmer surthce layers within the euphotic zone. Diurnal migrations were observed in the later copepodites only, the younger stages I to III either remaining deep in spring or shallow in summer. The causal mechanisms which alter the behaviour of the young copepodites remain unexplained. The development of the population of Calanus helgolandicus in 1978, reaching its peak of abundance in August, was typical for the shell" seas around U.K. as observed from Continuous Plankton Recorder data, 1958 to 1977.

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R. WILLIAMS & D. V. P. CONWAY VI. R E F E R E N C E S

ANDREWS, K. J., 1966. The distribution and life history of CaIanoides acutus (Giesbrecht).--"Discovery" Rep. 33:117-162. BUTLER, E. I., E. D. S. CORNER & S. M. MARSHALL, 1970. On the nutrition and metabolism of zooplankton. VII. seasonal survey of nitrogen and phosphorus excretion by Calanus in the Clyde Sea area.--J, mar. biol. Ass. U.K. 50: 525-560. CARLISLE, D. B. & W. J. PITMAN, 1961. Diapause, neurosecretion and hormones in Copepoda.~Nature, Lond. 190: 827~829. COLEBROOK, J. M., 1982. Seasonal variation in the distribution and abundance of plankton in the North Atlantic Ocean and the North S e a . ~ . Plank. Res. (in press). COLEBROOK,J. M., P. C. REXD& S. H. COOMBS,1978. Continuous Plankton Records: A change in the plankton of the southern North Sea between 1970 and 1972. Mar. Biol. 45:209 213. CONOVER, R.J., 1962. Metabolism and growth in Calanus tg'perboreus in relation to its life cycle.--Rapp. P.-v. R~un, Cons. perm. int. Explor. Met 153:190 197. CORNER, E. D. S., R. N. HEAD, C. C. KILVINGTON& S. M. MARSHALL, 1974. On the nutrition and metabolism of zooplankton. IX. Studies relating to the nutrition of overwintering Calanus.--J. mar. biol. Ass. U.K. 54: 319-331. ELOMORK, K., 1967. Ecological aspects of diapause in copepods. Proc. Syrup. Crust., Part III: 947-954. GARDINER,A. C., 1933. Vertical distribution in Calanusfinmarchicus.---J. mar. biol. Ass. U.K. 18: 575-610. HALLRERG, E. & H . J . HIRCRE, 1980. Differentiation of mid-gut in adults and overwintering copepodids of C.finmarchicus (Gunnerus) and C. helgolandicus Claus. -J. exp. mar. Biol. Ecol. 411: 283-295. HIRCnE, H. J., Untersuchungen tiber die Verdauungsenzyme von Zooplankton mit besonderer Berficksichtigung yon Calanus spec. University ofKiel, Kiel, Federal Republic of Germany: 1-151 (thesis). LONGHURST,A. R., A. D. REITH, R. E. BOWER& D. L. R. SEIBERT, 1966. A new system 1or the collection of multiple serial plankton s a m p l e s . ~ e e p Sea Res. 13: 213 222. LONOHURST,A. R. & R. WILLIAMS,1976. Improved filtration systems tor multiple serial plankton s a m p l e s . ~ e e p Sea Res. 23: 1067-1073. MARSHALL,S. M., 1924. The food of Calanusfinmarchicus during 1 9 2 3 . ~ . mar. biol. Ass. U.K. 13: 473~179. MARSHALL, S. M., A. G. NmnoLLS & A. P. ORR, 1934. On the biology of Calanus finmarch#us. V. Seasonal distribution, size, weight and chemical composition in Loch Striven in 1933 and their relation to the phytoplankton.- ]. mar. biol. Ass. U.K. 19-" 798~27. McLAREN, I. A., 1963. Effects of temperature on growth of zooplankton and the adaptive value of vertical migration.--J. Fish. Res. Bd Can. 20: 685--727. NmIqOeLS, A. G., 1933. On the biology ofCalanusfinmarchicus. III. Vertical distribution and diurnal migration in the Clyde Sea area.--J, mar. biol. Ass. U.K. 19: 139 164. PAFFENHOFER, G.A. & J. D. H. STRICKLAND, 1970. A note on the feeding ot" Calanus helgolandicus on detritus. --Mar. Biol. 5: 97~9. RUSSELL, F. S., 1927. The vertical distribution of plankton in the sea. Biol. Rex;. 2: 213-262. USSING,H. H., 1938. The biology of some important plankton animals in the t]ords of East Greenland.--Meddr Gronland 100 (7) : 1-108. WILLIAMS,R. & D. V. P. CONWAV, 1980. Vertical distributions of CalanusJinmarchicus and C. helgolandicus (Crustacea: copepoda). ~Mar. Biol. 60:57 61.