seasonal density and production estimates of the commoner planktonic copepods of northumberland...

Estuarine and COaStal ?~arine Science (1977) 5, 223-241

Dove Marine Laboratory, University of Newcastle on Tyne, Cullercoats, North Shields, Tyne and Wear, England

Received 6 January 1976 and in revised form I p May 1976

The seasonal density of five copepods, Acartia clausi, A. longiremis, Pseudo- calanus elongatus, Oithona similis and Temora longicornis in the Northumber- land plankton for a five year period is presented. Size of adult copepods is shown to be closely correlated with sea temperature during their period of development. Adult copepods do not grow. So during a period of temperature change alteration in mean size of copepods indicates a turnover of population, while unaltered mean size indicates an unchanging population. To obtain a production figure separate generations of adult females throughout a year are distinguished statistically on a size criterion. The average weights per unit volume of sea water of these separate generations is summed to give an annual production figure for adult females. Earlier work suggests that the statistically separate generations may generally be successive, each separate generation arising directly from the preceding one. Then the weights of all stages, not only the adults, may be summed to give a higher and more accurate production figure for each species.

Introduction

Qualitative records of the Northumberland plankton extend from the last century and have been the subject of several compilations (Norman & Brady, Igog; Bossanyi & Bull, 1971; Evans, 1973). Although many of these records contain an estimate of copepod numbers, the methods of collection varied greatly, so that only the most general quantitative comparisons can be made between them.

To provide quantitative data, an intendedly long term uniform method of plankton sampling was begun in 1969. A collection was made, at monthly intervals so far as was practicable, at a single station about five miles from the coast. Its purpose was to show seasonal fluctuations in the density of the commoner species, to identify longer term trends and to form a basis for production studies.

Parsons & Takahashi (1973) wrote: ‘Production is defined as the total elaboration of new body substance in a stock during unit time, irrespective of whether it survives to the end of that time. . . . The simplest relationship for the estimation of production is to consider the average standing stock of the population and multiply this by an estimation of the generation rate, both determined over short intervals. For example, if. the average standing stock of zooplankton is I g mV2 and the average generation rate (or doubling time) is one month, the annual production is 12 g m- a. The obvious difficulty in making this determina- tion is in obtaining figures for the average standing stock and generation rate of a zooplankton population in situ. ’

224 F. Evans

It is upon the estimation of standing stock and generation rate that the production estimates in this account are based. For the five years treated here plankton samples were taken in all except seven months. The copepod species considered are those most commonly found in the netplankton; they are Acartia clausi Giesbrecht, A. longiremis Lilljeborg, Oithona similis Claus, Pseudocalanus elongatus Boeck and Temora longicornis (0. F. Miiller). A further species, Microsetella norvegica Boeck, although known to be very common (Evans, 1974) was absent from the net samples and is not included.

Production depends in part on turnover time but the copepods referred to all reproduce continuously for much of the year and for this reason it is difficult to discover their turnover time in the field. Information is now accruing of the generation rate of a number of the species bred in the laboratory but while the indications from the results are most useful, in particular the relationship between temperature and development rate (Corkett & McLaren, 1970) the laboratory animals are not kept under a natural feeding regime and food is almost always present in excess of requirements; this cannot be true in the sea.

It has long been known that there is a relationship, albeit imperfect, between seasonal sea temperature and copepod size. For example, Adler & Jespersen (1920) showed this in extensive seasonal length measurements of adult Pseudocalanus, Temora and Calanus from the eastern North Sea for the years 1911 to 1914. In 1950 Digby at Plymouth used seasonal length variation to separate the generations of a number of copepod species, including all those commonly found off Northumberland with the exception of Acartia longiremis. His method, which utilized information on seasonal abundance of all stages as well as on adult female size, produced plausible results but had the disadvantage of being essentially sub- jective. Nevertheless, given the appropriate weights of individual copepods the production of each generation and hence the annual production could be estimated from his data.

In the present work, a statistical method is used to distinguish seasonal size differences of adult copepods. Since adult copepods do not grow, a significant difference in size between two groups of copepods caught at different times must indicate that they are of separate generations. The average weights of all the separate generations of adults can be summed to give an annual production figure. In a constantly breeding population this does not necessarily mean that the generations so distinguished are successive; only that the adults are successive; the juveniles may overlap the preceding generation. But comparison with other results (McLaren et al., 1969; Corkett, 1970) suggests that where separate generations of adults are identified statistically they may be truly successive, the second generation arising directly from the first. Then the weights not only of the adults but also of the juveniles may be summed to give a higher and more accurate annual production figure.

Methods

Sampling location

From 1969 a standard sampling station was adopted in a position 55”07’N, 1’2o’W, about 5 miles east of Blyth Lighthouse. At the station the ship’s position was adjusted by small amounts until the depth of water was exactly 54 m.

Net samples

Net samples were taken with the WP2 plankton net recommended in the UNESCO (1968) manual. This net has a mesh aperture of 200 l.t and a mouth area of 0.25 m2. Ballasted with a 25 kg weight, it was lowered 50 m vertically into the sea and then hauled up, thus filtering

Planktonic copepods in Northumberland coastal waters 22.5

all but the lowest 4 m of the water column. The operation was repeated four times and the samples bulked together. Hence the bulked sample represented vertical hauls totalling 200 m and an uncorrected filtered volume of 50 m 3. Since flow meters have been available to me only fairly recently and the earlier samples were unmetered, the errors introduced by clogging and by imperfect vertical hauling have been neglected. The magnitude of the clogging error is indicated by a recent set of four samples with flow meters fixed inside and outside the net. The filtered volume was reduced to an average of 96% of the uncorrected value, with a transformed s.d. of f1*5%.

Twelve metered plankton samples taken in 1974 in various sea conditions gave a mean recorded distance of 191.15 m with a 95% confidence limit of 7.5 m. This shortfall from 200 m is almost totally accounted for by the clogging effect. These results thus suggest that the animal numbers recorded from net samples may be generally some 4% too low.

Water bottle samples

Using a net of 2oopm aperture, while it has the advantage of remaining almost completely unclogged over such short distances, has the disadvantage that many juvenile copepods and a few adults are lost through the meshes. To overcome this problem, from March 1971 to April 1972 a separate series of monthly samples was collected at the standard station using an 8-1 water bottle. Samples were taken at IO m intervals from the surface to 50 m and filtered on deck through a woven wire test sieve of 44 pm aperture.

TABLE I. Monthly average numbers m-a of Oithona sampled by WPz net and by 8-l water bottle from April to October, 1971 (C=copepodite)

CI c2 c3 c4 c5 ? 6

Net 0 17 80 366 726 81

Water bottle 6008 563 459 414 608 855 89

TABLE 2. Numbers of adult Q Oithona mm3 measured by WP2 net and by 8-l water bottle, I 97 I

Apr. May June July Aug. Sept. Oct.

Net I92 417 1367 1667 783 400 256 Water bottle 4.18 458 1.583 1646 1417 271 167

TABLE 3. Numbers of Oithona, adults and copepodites together, taken in IO successive 8-l water bottle samples at 20 m, July 1972

Sample I 2 5 6 7 8 9 10 Numbers 77 103 6; 6: 122 102 97 47 79 50

Table I shows a comparison of the catches of the various copepodite stages of Oithona by net and by water bottle during April to October 1971. The net/water bottle ratio for adult females is 0.85 and for males 0.91. But the net is seen to be very inadequate for sampling earlier stages, and this is doubtless true for other species.

Seasonal densities are derived from the more extensive net data but production estimates require an accounting of all stages of development and are constructed upon the water bottle samples. The degree of agreement between water bottle and net samples is indicated in Table 2; the variation of the catch in replicate water bottle samples is shown in Table 3.

226 P. Evans

Measurement of body lengths

Lengths of adult females of the five species were measured using a graduated eyepiece. In Oithona the total length excluding furcal setae was measured but in the calanoid species, following common practice, it was the cephalothorax that was measured. Measurements were generally of 50 animals from each monthly sample but some samples were too small to provide sufficient animals for this.

For Pseudocalanus, Acartia clausi and A. longiremis measurement of body lengths extended from February 1971 to July 1972 by which time the pattern of seasonal fluctuation in size had become clear. Temora measurements were harder to interpret; adult females were scarce or absent in many months, so measurements were continued for the three years 1971-1973. Oithona was also measured over a three year period.

Body lengths of all stages, nauplius, copepodite and adult of the copepods taken by water bottle were measured. In this way the numbers and sizes of the monthly standing stock of copepods for 14 months was recorded. It may be noted that the juvenile lengths reflect proportionately those of the adults in the same sample. Marshall (1949) found such a pattern for the copepods of Loch Striven and Digby (195 ) o o served it for Pseudocalanus at Plymouth. b The simultaneous fluctuation of larval and adult sizes is what would be expected in continuously breeding populations of short life span.

The separation of generations by criterion of size

For comparison of body lengths of a species in a time series the mean monthly measurements of, generally, 50 adult females were arranged in ascending order of size. Significant differences in size from one month to the next were sought using the Student-Newman-Keuls stepwise procedure as described by Sokal & Rohlf (1969).

Mar. 1971 Olng2mzO n Oct. 1971 0.8306 Feb. 1971 0.8420

Dec. 1971 0.8544

Feb. 1972 0.8510

Mar. 1972 0.8674

Nov. 1971 0.8678

Jan. 1972 0.8702

Jul. 1971 0.8856

Aug. 1971 0.8961

Sep. 1971 0.9076

Jul. 1971 0.9104

Jun. 1972 0.9250

Apr. 1972 0.9474

Jun. 1971 0.9548

Apr. 1971 I.0364

May 1971 1.0498

May 1972 I.1172

Figure I. Ranked mean cephalothorax lengths of ad& female Pseudocalnnus. Each month represents a mean of 50 animals, except March 1971 (40). Values in the squared area above the stepped line do not differ significantly from each other. The sequence of generations is shown at the bottom of the figure.

Planktonic copepods in Northumberland coastal waters aa7

The method is described and then an example using Pseudocalanus is given. The residual mean square of the sample measurements is first found. This is converted to the pooled standard error of the group mean, l/(M5’Wi,,i,/n), where lecithin is the residual mean square and n is the number of copepods in each sample. A small modification to this expression is required if the number of animals is not the same in all samples.

A series of tabulated values is next extracted of the quantity Q, the critical values of Student’s t-distribution. The Q table is entered with the quantities a=the level of signi- ficance desired (p=o.og in the present instance), v=d.f.witbin and K=I +difference between the ranked position of the monthly means. The extracted values are thus of Qa[k,v] and there is a Q value for each pair of means; months I and 2, months I and 3, months 2 and 3, etc. Each Q is then multiplied by the pooled standard error of the group to give a quantity called the least significant range (LSR).

Pseudocalonus

1971 1972 5 generations

7 generaf ions

A. longiremis

4 generations

Temora 6 generations

4 generations

5 generations

Oifbona 5 generations

5 generations

6 generations

Figure 2. Generation tables produced by SNK analysis for the 5 copepod species.

The actual difference between the means of one month and another is then compared with the LSR for that k value. If the actual difference is found to be greater than the LSR then the two months are regarded as significantly different and the copepods are of separate generations. An outline for the procedure is given for Pseudocalanus in Figure I but for the remaining species only the results are quoted (Figure 2).

Figure I shows the monthly mean cephalothorax lengths of Pseudocalanus arranged in increasing size. The stepped line within the right-angled triangle represents the level of significant difference at p=o*og ; each pair of values which falls on two sides of this line is

228 F. Evans

taken to be heterogeneous. For example, the cephalothorax lengths of March 1971 differ significantly from those of December 1971; they do not differ from those of October rg7r or February 1971. But March 1971 is significantly different from April 1971. Therefore although March and October are statistically homogeneous they are separated by the heterogeneous April and so represent two separate generations, while March and February are truly homogeneous and represent one generation.

Sea temperature and body lengths

On 8 occasions in 1971 and 1972 sea temperatures were taken at the time of phurkton sampling (Table 4). For comparison the mean monthly sea temperatures at the Longstone Lighthouse (55’39’N, 1'37'W) are given. The comprehensive Longstone temperatures are most nearly related to those at midwater at my standard station and have been used as a basis for examining temperature/body length relationships (Figure 3).

TABLE 4. Sea temperatures (“C) at the standard station and at the Longstone Lighthouse

Depth(m) o IO Standard station

20 30 40 50 Longstone

surface

Date x971-2 June 11.7 IO.9 10.x 10'1 9.0 8.7 9.0

i:. 13’3 13.8 13.2 12.8 11.6 11.7 10'1 11.3 11'2 9.8 11'0 9'4 11.4 12.3 March 5’8 5’8 5.8 5’8 5’8 5’8 5.8 April 6.5 6.5 6.5 6.5 6.5 6.5 6.2 May 7’S 7’8 7.8 7.8 7.8 7.8 7.6 June 10'0 10'0 9.8 9’4 9’2 9’2 9’5 July 14’4 11'2 10.6 10'2 10'0 9’9 10.6

JFMAMJJASONDJFMAMJJ Figure 3. Sea temperature at the Longstone Lighthouse and phytoplankton colour in arbitrary units for the Plankton Recorder Survey area C2 (NW North Sea), January 1971 to July 1972.

Planktonic copepods in Northumberland coastal waters 229

Production

The separate generations found by SNK analysis are effectively an indication of the turnover times for adult female copepods during the 14 months considered. By summing the weight of all the generations of a species through the year a production figure for adults is arrived at. This production figure is a minimum since there may be more generations in the year than the analysis reveals. A second and more probable production figure is obtained by summing the weight of standing stock of juveniles as well as adults.

TABLE 5. Numbers of copepods in the water bottle samples from March 1971 to April 1972. Each figure represents the actual 48 1 sampled, not numbers rnW3. C = Copepodite. N = Nauplius

Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr.

A. clausi 60 3

Acartia spp. N I7 17

A. longiremis do 1 90 1 co 5

Pseudocalanus

c II N 18 i:

Temora 6 0 90 f, c 0 N 8 ;:

Oithona 6 1 ? 8 2: c 37 110

N 22 109

0

0

57

31

8 12 21

I 18

3.5 34

3 22 I7 8

0 6 0 I

34 II

i II

I3 I 0 0

27 II 2 2

50 IO 3 0

28 48 I9 88 4

12 IO

36 32 IO 8

2 I

0

0

0

2

4 5 3 0 0

I4 IO I4 4 I

40 38 23 32 36 60 39 20 I3 3

34 18 26

0

IO

14

2

5

i 28

2

2

5 20

3

i 24

4 I9 74 79

441 122

I87 116

6; 57

I53

I

I3 52 98

ii 30 74

3 0

0

0

0

0

2

0

0

0

II

9

I

4 39

2

0 I 0 0

3 4 7.8 8

3 0

IO I9 49 40

164 33

0

0

0

I

0

I

0

0

I

3 5

0

0

ii

I

4 8 9

0

0

0

14

0

I 0

0 2

5 3

0

0

I

II

0 0

7 3

0

0

0

0

0

0

0

I 2

I

3

0

0

2

0

0

2

5 2

0

0

9

20

I

I 0

0 0

4 12

0

4 2

I7

I

6: 120

To find the weight of standing stock the numbers, stages and lengths of the copepods in the water bottle samples were found. Numbers and stages are given in abbreviated form in Table 5. For converting length to dry weight Robertson’s (1968) equations have been used. He investigated the length-weight relationships of calanoid copepods in the Firth of Clyde and derived regression equations for, among others, Acartia clausi, Temora longicornis and a mixture of Pseudocalanus elongatus and Paracalanus parvus. These equations are based on measurements of cephalothorax length and so can be applied unchanged to the present calanoid data. The formula for A. clausi is taken to apply to the similarly shaped A. Zongiremis; Robertson was satisfied that the formula for the mixed P. elongatus-P. parvus was adequate for P. elongatus alone.

230 F. Evans

An expression for Qithona for 700 animals taken off the Northumberland coast, preserved and weighed in batches of IOO, is added. In juvenile cyclopoid copepods the cephalothorax length is an unsatisfactory parameter to measure and since Oithona specimens mostly die extended the overall length has been measured instead. The equations are:

Log w=2.86 log Z,-1*74 (Acartia) Log w=2*39 log II-r&r3 (Pseudocalanus) Log w=1*79 log Z,---0.51 (Temora)

Log w=2+3g log Z,-2.33 (Oithona)

where w=weight in pg, Z,=cephalothorax length and E,=overall length, in units of 100 pm.

TABLE 6. Growth factors derived from 8-I water bottle catches. For each species and stage internal values were found for each month and then averaged. N= Nauplius, C = Copepodite

Pseudocalanus Temora Acartia clausi Oithona

NI - II 1'20

III 1.28 IV 1.26 2 1’21

1.17

CI - 2 1.27 3 I.18 4 1.16

G 1.13 1.16

Mean growth factor 1'20

- 1’33 x.17 1.27 1.30 I'43 1'20

1'20 1.16 1'20 1.14

- 1.16 1.24 1.17 1'22 1.14

1.24 1'20 1.18

- 1.29 1.19 1'22 1.16 1.19

-

1'25

1'10 1'20 1.17

1.71 I.18 1.18 1.18 1.18 1.13

Since the shape of copepods changes comparatively little during the copepodite and adult stages weights of these stages may be calculated directly from the regression equations. How- ever, discovering the weight of nauplii is more difficult and an indirect method has been used, depending on the growth factor at each moult. The growth factor is taken to be the length after a moult divided by ,the length before a moult, the length being overall length or some other measurement, as for instance the cephalothorax length. The growth factor has been determined for all stages of the four genera (both Acartia species being considered equal) with the exception of the moult from the last naupliar to the first copepodite stage (Table 6). Here the pararneter measured changed from overall length in the nauplius to cephalothorax length of all species except Qithona. In Oithonn there was a very large increase in the growth factor at this moult, 1.71 compared with about 1.2 for every other moult. Microscopic examination showed that this one moult produced an exceptionally large growth factor not because of a real increase in size but because of a sharp change in shape, from the rounded nauplius to the elongate copepodite. Gurney (193 I) found a similar jump in the growth factor of the fresh water calanoid Diaptomzcs vulgaris at this stage in development. If we suppose that the true nauplius-to-copepodite growth factor in Oithona, i.e. that related to volume or weight, has a value not of 1.71 but close to the average growth factor during development, 1.18, then it is possible by a process of successive division to derive the weight of the naupliar stages from the length of adults or copepodites. This


method has been followed for the calanoid species also, using a growth factor for metamorphosis from nauplius to copepodite equal to the average during the whole development.

Any errors introduced by these estimated figures at metamorphosis will be very small since the weight of a nauplius is so low compared with that of later stages. As an example, if the weight of an adult Pseudocalanus of I mm cephalothorax length is by Robertson’s equation 18-2 pg then the weight of a stage 6 nauplius will be 1.64 l.tg and of a stage I

nauplius o-15 pg, using the method described. Two production figures, a minimum one of adult females and a higher one based on all

juvenile and adult stages of both sexes, obtained as described above, are derived for each generation. Generations are counted for a year from the demise of the overwintering generation of 1971, i.e. from March 1971 in the case of Oit!zona, from April for Acartia spp. and Psezkdocalamq and, on the evidence, from June for Temora (Figure 2). Annual production is given by totalling the production of each generation.

Results

Seasonal density

Acartia clausi and A. longiremis (Figure 4). Acartia spp. were not generally separated in the net sample counts. They are together common from spring to autumn with a tendency to produce peaks around a decline in summer. 1 have earlier shown (Evans, 1973) that both species are commoner inshore than offshore, A. 1ongiTemis having a more extreme gradient,

1969 1970 1971 1972 1973

Figure 4. Seasonal density of Acavtia spp., xg6g to 1973 (above) and a density curve averaged for the 5 years. Ordinate values are numbers III-~.

and further that A. clausi is the more abundant species in the autumn, A. longiremis in summer. This is confirmed for 1971 adults in Table 5. It was not found possible to distinguish routinely the nauplii of the two species but Acartia spp. nauplii are found in almost every month. Copepodites, however, were absent in winter.

Pseudocalanus elongatus (Figure 5). This copepod is also present throughout the year. In three of the five years considered it reached a maximum in spring and in the remaining two

232 F. Evans

years in late summer. The dramatic decline in numbers between May and June 1973 was associated with the arrival off Northumberland of an immense shoal of ctenophores, Bolinopsis infundibulum. A parallel decline is seen in the other copepod species. Pseudo- cuEanus nauplii and copepodites are present throughout the winter but, like the adults, are found at a low density.

““l: 1969 1970 1971 1972 1973

1000 -

500 -

o- I I I I I I I I I I I I I I

(D) J F M A M J J A S 0 N D [J)

Figure.5. Seasonal density of Pseudocalanus, 1969 to 1973 (above) and a density curve averaged for the 5 years. Ordinate values are numbers rnm3.

-“I: 1969 1970 1971 1972 1973

1000 -

500 -

O-Q q - 0

I Ii I I I I I I I I I I I

(D) J F M A M J J A S 0 N D (J)

Figure 6. Seasonal density of Temora, 1969 to 1973 (above) and a density curve averaged for the 5 years. Ordinate values are numbers mm3.

Temora longicornis (Figure 6). Adults never quite disappear from winter samples but a density of <I m--3 is not unusual. In four years out of five there was a single peak, sometimes in May and som,etimes in September, so that the composite density curve shows two apparent


maxima, in spring and in autumn. Although adults are almost absent in winter over-wintering copepodites and nauplii are not uncommon.

Oithona similis (Figure 7). Oithona is rarely at a density below IO m-a. There is no clear seasonal density distribution other than a winter minimum and all stages are found throughout the year.

‘““:I 1969 1970 1971 1972 1973

(D) J F M A M J J A S 0 N D (J)

Figure 7. Seasonal density of Oithonn, 1969 to 1973 (above) and a density curve averaged for the 5 years. Ordinate values are numbers m+.

L

I.1 -

p IO-

E c _ ‘- G -1 0.9-

0.8t, , , , , , , , , , , , , , , , , ,

FMAMJJASONDJFMAMJJ

1971 1972

Figure 8. Cephalothorax lengths of adult female Acartka clausi from February 1971 to July 1972. Each point represents a mean of 50 animals and the bars indicate 95 oh confidence limits of those means.

Body lengths

The lengths of adult females of the five species treated are shown in Figures 8-12. Large specimens of all species are found in spring but there is generally only a weak, inverse agreement (p>o*og) between size and sea temperature. Acartia spp., Pseudocalanus and

234 F. Evans

Oithona all follow a fairly simple pattern of declining size from the spring maximum until the following autumn and of a winter population of small animals. The Temora size curves are very different in that there is additionally an increase in each August, very marked in two years of the three, a decline in early autumn and, in the two years with sufficient data to show it, a further steep increase in size towards the end of the year.

“.?I FMAMJJASONDJFMAMJJ

1971 1972

Figure 9. Cephalothorax lengths of adult female Acar& Zongiremis from February 1971 to July 1972. Each point represents a mean of 50 animals, except March 1971

(41), and the bars indicate 95% confidence limits of those means.

0.8 ’ I I I I I I I I I I I I I I I I I

FMAMJJASONDJFMAMJ.

1971 1972

Figure IO. Cephalothorax lengths of adult female Pseudocalanus from February 1971 to July 1972. Each point represents a mean of 50 animals except March 1971 (40), and the bars indicate 95% confidence limits of those means.

Generation separation

The results produced by SNK analysis for all the species is shown in Figure 2. The annual number of separate generations is counted from the first generation of the new year. Only one annual cycle is quoted for Acartia spp. and for Pseudocalanus but three for Temora and Oithona. The results for Temora are difficult to reconcile, partly because of their lack of consistency, and partly because of the paucity of winter animals. For Oitllona there is good agreement between the three years.

Flanktonic co$epods in Northumbevland coastal waters e5

CoTrelation of sea temperature and body lengths

The fit of the Pseudocalanus size curves to the sea temperature curves is much improved if generation patterns are taken into account. So long as copepods are not moulting or are moulting infrequently changes in sea temperature will hardly affect their size. Figure 13 shows a cephalothorax length curve for adult female Pseudocalanus plotted against a modified

I.0 I.0 1971

0.9 0.9

0.8 0.8

I.2 1972 0

2 \

I.1 0

-L--l f I

p I.0 9 3 \ /”

0.9 $-”

JFMAMJJASOND

Figure II. Cephalothorax lengths of adult female Temora during 1971-3. Each point represents a mean of 50 animals except April 1971 (31) and the bars indicate 95% confidence limits of those means.

It I I I I1 I I I I I I I JFMAMJJASOND

Figure 12. Cephalothorax lengths of adult female Oithona during 1971-s. Each point represents a mean of 50 animals and the bars indicate 95 y, confidence limits of those means.

236 F. Evans

sea temperature curve. The temperature ordinate is scaled one month earlier than the cephalothorax length on the general ground that adult body size is related to sea temperature during the preceding period of growth. In plotting the curve the temperature at the start of each generation is held constant over the whole generation period, e.g., the cephalothorax lengths

1970 1971 1972

OFMAMJJASONDJFMAMJ I , , I, I, I I I, I I I I I I),

-5

1.1 - -6

-7

0.9- -II

- I2

- 13

0.0 t ’ ’ ’ ’ ’ ’ ’ ’ ’ ’ ’ ’ ’ ’ 1 ’ ’ ’ - FMAMJJASONDJFMAMJJ

1971 1972

Figure 13. The cephalothorax length of adult female Pseudocalanus plotted against a reversed temperature curve one month earlier (October, 1970 for the overwintering stock of February and March 1971). The temperature level is held constant from the start to the finish of each generation. A, Temperature; 0, length.

TABLE 7. Correlation of cephalothorax length of adult females (overall length for Oithona), in units of IOO pm, with sea temperature at the month of capture and with sea temperature at the time of development, 1971-1972

Correlation with Correlation with sea temperature modified sea

at month of capture temperature Y P Y P

Linear regression of body length, y,

against modified sea temperature, x

A. clausi A. longiremis Pseudocalanus Temora Oithona

0.06 >0*1

0’02 >O.I

-0’09 >O,I

-0.33 >O.I

-0.38 >O.I

-0.90 <O.OOI

-0.91 <O.OOI -0.85 <O.OOI -0.28 >O.I

-0.53 (0.02 y=10.23 -0.16~

for July, August and September 1971 are fitted to the June temperature, resulting in an acceptably good fit between the two entities. The correlation coefficient is highly @<O.OOI)

significant and the regression equation is

y=1zqg-o-36x

where y is the cephalothorax length in units of IOO pm and x is the sea temperature appropriate to each generation. The size of Pseudocalanus is largely described in terms of sea temperature; if the growth period had been exactly known for each generation no doubt the fit would be even better.


Correlations and linear regressions are shown for all the species in Table 7. The generally poor fit between size and concurrent temperature is greatly improved for all except Temora by considering the temperature prevailing not at the time of capture but at the time of development.

Production

The average dry weight of standing stock of adult female copepods for each separate generation from spring 1971 to spring 1972 is listed in Table 8. Table 8 represents the minimum possible production value for the year. A second production figure obtained by summing all juvenile and adult stages of both sexes as described earlier is given in Table 9. These figures,

TABLE 8. Minimum production, mgm- 3, for each species, adult females only, from spring 1971 to spring 1972

Generation I 2 3 4 s 6 7 Total

A. clausi 0.69 o 0.51 1.30 5.07 1.58 0.16 9.31 A. longiremis 1.31 5'0.5 o-70 0'12 7.18 Pseudocalanus X.98 4’30 2.61 0.46 16.56 Temora 5’9.5 3.58 292 0.59 1.33 1.36 15’73 Oithona 0.34 1.48 3.21 0.39 0’33 5’75

TABLE g. Estimated production, mg m- 3, for each species, all stages, from spring 1971 t0 SpriIlg 1972

Generation I 2 3 4 5 6 7 Total

A. clausi 3’03 2.64 2.95 3.46 12.05 2*55 0.19 26.87 A. longiremis 3’0 j-24 0.92 0.14 11.30

Pseudocalanus 24.20 9.76 7.67 5.06 1.17 47.86 Temora 19.70 IO.43 6.36 2.16 3'34 2.04 44’04 Oithona 1.08 3’17 7.12 1.04 0.87 13.28

it will be recalled, are average values mW3 over a sampling depth of 50 m. To obtain an estimate of the production under I m2 of the sea surface at the standard station, which stands in 54 m of water, we multiply by 54. The minimum annual production under I m2

for adult females of the five species was thus 2.94 g while the estimated production figure for all stages, assuming successive generations, was 7.74 g. Of this estimated production 19%

was contributed by Acartia clausi, 8% by A. longiremis, 33% by Pseudocalanus, 31% by Temora and 9% by Oithona.

Discussion

Seasonal density

The annual density of three of the five copepods, Acartia clausi, A. longiremis and Pseudo- calanus may be compared directly with published data for the same years collected by the Plankton Recorder Survey (Glover & Robinson, 1970, 1972; Robinson, 1973, 1974, 1975).

For the overlapping area Cz the Recorder Survey indicates a maximum for Acartia spp.

generally later in the year than for Pseudocalanus, as was found off Northumberland.

238 F. Evans

Seasonal distribution of Temora in the North Sea was examined by Rae & Rees (1947).

They discovered the species to be rare there over much of the year, with a spring increase in April or May and with generally a much shorter period of abundance than Pseudocalanus. This shorter period is not found, we have seen, in Northumberland although the total density during the five years studied was below that of Pseudocalanus. But the scarcity of Temora that Rae & Rees found everywhere in winter suggests that the very low numbers taken off Northumberland in that season were due not to emigration but to death.

Oithona was the only species of the five to lack a marked depression in the density profile during June and July; it thus failed to correspond with the general trend of the local phytoplankton, which is reduced in these months (Figure 3) (Colebrook & Robinson, 1965).

In general both phytoplankton and copepod density showed a winter minimum and two maxima, one in the spring, the other in the autumn.

Body lengths and temperature

McLaren (1965), utilizing reports from many places, concluded that the size of Pseudo- calanus was dependent only on the temperature during the time of development although as he pointed out growth and development may be thwarted by food shortage. He believed that this type of determinate growth may be general for calanoid and cyclopoid copepods. El-Maghraby (1965) found that at Alexandria, with a seasonal sea temperature range of 13O, temperature was the main factor in influencing copepod size. Katona & Moodie (1969) found that Pseudocalanus cultured at 15’ with abundant food grew to the same size as animals taken at approximately the same temperature from many places at sea. Corkett and McLaren (1970) found experimentally that development rates and hence size of well fed Pseudocalanus and Temora longicornis were temperature related. Bernard (1970) found the same for Temora stylajzra.

Figure 13 shows a clear relationship between size and temperature for each statistically separate generation of Pseudocalanus. Changing sea temperature produces a change in adult size of a developing population of animals but no change in one where development is suspended; it is upon this that the method of identifying separate generations depends.

Off Northumberland a size-tem.perature relationship similar to that of PseudocaZanus appears valid for Acartia spp. and Oithona but the more complex size curves for Temora call for further enquiry. The additional size peak of this species in August, very marked in two years of the three studied, are not related to a local temperature minimum either then or in July when development was presumably proceeding. This curious result reflects a similar anomaly found by Adler and Jespersen (1920) for this species in about the same latitude in the eastern North Sea. As well as a size maximum in the spring they found ‘unlike Pseudocalanus . . . a secondary, very well marked maximum in November’ (my translation). They ako found, as I did, that size differences between corresponding peaks in different years could be very marked.

If the size of Temora is indeed reflecting the development temperature we must suppose that cohorts of the species move into local seas from colder waters elsewhere. This colder water could have one of two possible origins, one of which is the deep water of the Atlantic to the north of Scotland. Although not generally plentiful in the Atlantic Temora is common north of Scotland (Edinburgh Oceanographic Laboratory, 1973). West of Shetland the surface water temperature in July is about 12' (Anon., 1962) but in the same month the temperature at 200 m is some 8” (Schroeder, 1963). Objections are that this temperature, although low, seems unsatisfactorily high to produce such large animals as are found off


Northumberland in August and that an oceanic influx of Temora would bring other oceanic plankton indicators; no such indicators were seen in August of any of the three years.

Alternatively, cold water may have spread in from the central North Sea. Fraser (1965) regards Temora in the North Sea as typically associated with central water. Laevastu (1963) presented an east-west profile of temperature across the North Sea in the latitude of Northumberland in August. It showed temperature below 8” to the west of the Dogger Bank. If such water were to drift up to the Northumberland coast there would be much less biological indication of its presence than there would be of Atlantic water. Physically, however, temperatures at the standard station during 1971 and 1972 gave no indication of such a cool influx. Bottom temperatures at these times were only marginally below the long-term July average of IO' (manuscript records of H. 0. Bull). Yet there are parallels to be found in other crustacean species, For instance, the amphipod Parathemisto gaudichaudi is found generally as a small local form [=P. grac%pes (Sheader & Evans, 1974)] rarely exceeding 8 mm but in the spring of many years it is replaced by a cold water form twice as long (Evans, 1973).

Alternatively two genetically distinct forms of Temora, one or both being allochthonous, may occupy the area successively. Woods (1969) found large and small forms of Pseudo- calanus in two adjacent Canadian fjords; they had differently timed life cycles and she showed that the larger form was polytenic. Temora may be similarly organized in the North Sea.

Generation times

The development time of Pseudocalanus eggs in the laboratory was shown by McLaren et al. (1969) to be a function of temperature, expressed by the equation D=2144 (T+

13.4)-+05 where D is the development time in days and T is the temperature in “C. Corkett (1970) gave the development time of Pseudocalanus from NI (inadvertently cited as CI in his account) to adult female as D=26714 (T$13.4)~~‘~~.

Temperature 6.4 9.0 12.3 12.2 IO.8 8.2 6.4 Days 64 49 37 37 42 53 64

I 2 345 6 7

II I I I I I I I II I I AMJJASONDJFM

Figure 14. Development time of Pseudocalanus using the equations of McLaren et al. (1969) and Corkett (1970). Temperatures are for Northumberland waters in 1971.

Combining these two expressions and inserting appropriate Northumberland sea temperatures we may estimate the maximum number of generations possible locally in a year under conditions of abundant food. Figure 14 shows that beginning with April, when the first generation of the new year appears, this works out at 7. The number of generations counted in the sea in 1971 using SNK analysis was 5. The difference is accounted for by there being only one overwintering generation instead of the two predicted in a condition of abundant food and by a missing generation in the sea in summer. This accords with the known reduction in the level of phytoplankton at this season (Figure 3) and with the suggestion that there must have been some reduction in Pseudocalanus development owing to food

240 F. Evans

shortage. Otherwise the two results are in good agreement. The calculated laboratory generations are successive, which indicates that allowing for the two periods of food shortage the 5 generations in the sea are also successive.

In the somewhat warmer waters of Plymouth Sound, Digby (1950) also estimated 5 generations of Pseudocalanus. But he found only 5 or possibly 6 generations of Acartia clausi compared with my 7. Gaudy (1962) similarly found 5 or 6 Acartia generations in the year in the Gulf of Marseille, while Conover (1956) f ound only 4 off Long Island. Much of the importance of A. clausi as a producer off Northumberland is due to its rapid summer breeding for, owing to the animal’s small size, the weight of the standing stock is not high at any time of year except September. Acartia longiremis appears to breed more slowly.

Temora presents an unclear picture throughout this work. The annual number of separate generations found is not constant, the calculations being affected by the diminished populations at the beginning and end of each year. The breeding rate is at times very high and with such a comparatively large animal this results in high production; however some of this production may be imported since the two forms of Temora present in the summer are, as stated above, not necessarily both autochthonous. More generally, Marshall (1949) believed that in Loch Striven the time from a peak in nauplius production to a peak of adults was 3-4 weeks in most species of small copepods and that the usual number of broods in the summer was 3 or 4.

Production

The weaknesses of the method of estimating production are twofold. First, the exact figure produced is a minimum and undoubtedly much too low, while the more probable higher figure is less accurate. Second, the method is effective only at a time of changing sea temperature; so that extra generations around the warmest and coldest periods of the year may not be distinguished. Nevertheless, the results represent the only estimates of Northumberland planktonic copepod production and the method is applicable elsewhere.

Acknowledgements

From 1968 to 1972 I was in receipt of a Natural Environment Research Council research grant. I am further indebted to N.E.R.C. for supplying the phytoplankton data collected by the Continuous Recorder Survey shown in Figure 3. The Meteorological Office kindly sent me sea temperatures taken at the Longstone Lighthouse. My thanks are due to Dr H. 0. Bull for sea temperature records collected over many years, and to Mr T. Bibby who sorted much of the net plankton.

References

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seasonal density and production estimates of the commoner planktonic copepods of northumberland...

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