Feeding, Growth, and Food Conversion of the Marine Planktonic Copepod Calanushelgolandicus

Gustav-Adolf Paffenhofer

Limnology and Oceanography, Vol. 21, No. 1. (Jan., 1976), pp. 39-50.

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Feeding, growth, and food conversion of the marine planktonic copepod Calanus helgolandicusl

Gustav-Adolf Paffenhofer2 Institute of Marine Resources, University of California, San Diego, P.O. Box 109, La Jolla 92037

Abstract

Food intake, growth rate, and food conversion of nauplii, copepodids, and adult females of Calanus helgolandicus were investigated experimentally at 15OC. The diatom Lauderia borealis and the dinoflagellates Gonyaulax polyedra, Gymnodinium splendens, and Pro-rocentrum micans were offered separately as food at concentrations ranging from 41 to 101 pg C liter-l. Amounts of food ingested differed with concentration and species. Daily exponential growth rates were highest for nauplii and young copepodids ( k =0.29 to 0.41) and decreased gradually with increasing age of the copepods to k =0.02. Gross growth efficiency changed during the different juvenile life periods of the copepod with maximum values for the period CI to CIII. Feeding on L,borealis at lower food concentrations re-sulted in an increase in gross growth efficiency.

Investigations of feeding, growth, and food conversion of marine planktonic cope- pods have usually dealt with late copepodid stages or adult specimens of various species, rarely covering the entire juvenile life of one species. Information on the nutritional biology of juvenile stages is needed, as copepod nauplii and young copepodids can occur in larger quantities of biomass than late copepodids and adults (Cushing and Vucetic 1963).

Food intake, growth rates, and food con- version of Calanus helgolandicus and Rhin-calanus nasutus have been investigated throughout their juvenile life (Mullin and Brooks 1970a,b). Ingestion rates and gross growth efficiencies for C. helgolandicus and Acartia clausi from the Black Sea were cal- culated for all juvenile and adult stages by combining data obtained in the open sea and in the laboratory (Petipa 1967).

A specific cultivation technique made it possible to rear C. helgolandicus at low mortalities from hatching to adulthood (Paffenhofer 1970). Thus, it was intended to measure ingestion, growth, and food con- version of juveniles and adult females at

This research was supported by United States Atomic Energy Commission contract AT(11-1) GEN 10, P.A. 20, and Deutsche Forschungsge-rneinschaft grant Pa 124'2.

Present address: Skidaway Institute of Ocean- ography, P.O. Box 13687, Savannah, Georgia 31406.

different environmental food concentrations by offering separately different species of phytoplankton. Food conversion describes the degree of incorporation of food into body substance and is expressed by the term gross growth efficiency (Conover 1964) .

I am deeply indebted to the late J. D. H. Strickland who let me join his Food Chain Research Group and continuously sup-ported my investigations with advice and suggestions. The criticism of the manu-script by S. M. Marshall, D. W. Menzel, M. M. Mullin, B. W. Frost, E. D. S. Corner, and R. P. Harris is gratefully acknowledged.

material and methocls

The main food organisms of C. helgolan- dicus in the neritic waters of the Pacific Ocean off La Jolla, California, are consid- ered to be diatoms and dinoflagellates. For April through September 1967, except for a diatom bloom in May, dinoflagellates and smaller monadoid forms represented most of the phytoplankton biomass (Reid et al. 1970). To offer C. helgolandicus represen-tatives of its natural food, I selected the chain-forming diatom Lauderia borealis, which had an average diameter l9 p, and three dinoflagellates: the unarmored Gymnodinium splendens, which was almost

in shape and had ' width of 55-60 p; the armored Gonyaulax poly-

LIMNOLOGY AND OCEANOGRAPHY 39 JANUARY 1976, V. 2 1 ( 1 )

40 Paf fenhofer

edra, which had a similar shape as the former and a maximum width between 46 and 55 p ; and the armored Prorocentrum micans, which was of plumstone shape and had an average maximum width of 36 p. All of these were cultured at 15°C as de- scribed earlier ( Paffenhofer 1970, 1971 ) . Concentrations of phytoplankton offshore from Scripps Institution of Oceanography were measured regularly from mid-April to mid-August 1967 (Mullin and Brooks 1970b). At stations 2 and 3 ( 4 and 8 km offshore) the mean concentrations of phyto- plankton cells of 5-50-p diameter in the euphotic zone were 55 and 23 pg C liter1. Maximum phytoplankton concentrations in these waters are close to 300 pg C liter-l ( Strickland 1968).

The experimental methods used for C. helgolandicus were described by Paffen- hofer ( 1970, 1971 ) . Temperatures ranged from 14.7 to 153°C and salinity was 349/00. The seawater was filtered through an 0.8-p membrane filter. Experimental jars had a capacity of 8,000 ml and were filled with 7,000 ml of seawater. In each experiment a population of C. helgolandicus was cul-tured from hatched nauplius to adult stage. At specified intervals the population den- sity was decreased by removing copepods. Those removed were dried at 60°C and 80°C and their dry weights used to estimate growth rates and gross growth efficiencies. The dry body weight was converted to or- ganic carbon by different factors for differ- ent stages: CI = 0.32, CIII = 0.35, CV and adults = 0.37 (M. M. Mullin personal com- munication) . Daily growth rates were cal- culated as the coefficients of daily exponen- tial growth k by the following equation (Mullin and Brooks 1967, 1 9 7 0 ~ ) :

Wo is the weight of one copepod at the beginning, and W, is the weight at the end of a life period; t is the time in days. The remaining copepods were allowed to con- tinue to grow until the next specified time for dilution of the culture. The amount of phytoplankton ingested by the copepods in the cultures was determined at regular

intervals; food concentration in each jar was measured 1to 4 times per day using a Coulter counter at different threshold set- tings and aperture currents with an orifice of 400-p diameter. The phytoplankton con- centrations in the jars were expressed as cubic microns ( p 3 ) of algal volume per milliliter and converted to p g of particulate organic carbon per liter ( p g C liter-*) using conversion values determined with a Beck- man model 15 infrared analyzer (Table 1; Menzel and Vaccaro 1964; Strickland and Parsons 1968). No corrections were made for the growth of the phytoplankton in the copepod jars, as daily growth of diatoms and dinoflagellates (increase in particle volume in control jars) did not exceed 5% of the initial experimental food concentra- tion. The culture flasks were exposed to rather low light intensities (800 to 1,200 lux) which resulted in low growth rates of all species.

Gross growth efficiencies from NII to early adulthood were determined in terms of organic carbon, organic dry weight, and calories. This was done because different workers had used various methods, mostly based on organic carbon or organic dry weight. As for calories, Comita et al. (1966) reported that the calorific content of adults of C. finmarchicus could range from 4,975 to 8,400 cal g-l of ash-free dry weight. Since different food concentrations and species could affect the calorific content of the copepods and thus the overall gross growth efficiency, the calorific content of the food species and the adult copepods was determined. The calorific content of the NII was not taken into account. Calo-rific determinations were made in a Phillip- son (1964) microbomb calorimeter (Gentry and Wiegert ) . Phytoplankton dried for 2 4 4 8 h at 60°C and copepods for 1 h at 80°C were ground in a small grinding mill and the coarsely powdered samples were combusted completely in the calorimeter. Sample size ranged from 4 to 14 mg.

Results

Food concentrations and mortality-The juvenile life of C. helgolandicus was di-

41 Growth efficiency of C. helgolandicus

Table 1. Carbon content o f four phytoplank- ton species.

C c o n t e n t S D No. C d e t e r -( u g ) of 1 m i n a t i o n s mm o f a l - g a l v o l

L. borea l i s 19 u c e l l 85.0 -t13 .8 66 diam

L. borea l i s 36 p c e l l 33.0 -+ 3.8 6 diam

G. pozyedra 154.9 -t12.7 10 G. splendens 129.2 -+ 5.3 5 2. micans 213.8 -t17.7 11

vided in most cases into three periods: hatching to CI, CI to CIII, and CIII to adulthood. Mortalities during these periods and average food concentrations are pre- sented in Table 2. The surviving copepods were counted every 3 days and animals that died during these 3-day intervals were assumed to have fed for 1.5 days.

Most of the mortality was during the pe- riod from hatching to CI. Mortalities were lowest when dinoflagellates were offered as food. The rather high mortality in the G. splendens experiment was unusual: in earlier experiments with this species the mortality of C. helgolandicus from hatching to adulthood was between 0 and 12% (Paf- fenhofer 1970, 1971). The experiments with L. borealis indicate that with diatoms a markedly lower food concentration in-creases the mortality.

Ingestion-Feeding perfomlance of cope- pods depends on the size and shape of the food particles well as on their concentra-tion (Curl and McLeod 1961; Martin 1970; Frost 1972; Nival and Nival 1973; Paffen- hijfer 1971). The food organisms used here were readily ingested. An almost linear relationship was found between food concentration and amount of ingested food for copepods feeding on L. borealis: From NII to CV, C. helgolandicus at 49 p g C liter-l ate about 50% of the food ingested by specimens of the same species at 101 pg C liter1 (Table 3 ) . However, the body weight of all C. helgolanclicus stages reared at 49 pg C liter1 was considerably lower

Table 2. Calanus helgolandicus. Mortality* during di f ferent periods f rom hatching t o adult-hood and mean food concentration during juvenile l i f e .

Food sp. h a t c h i n g CI t o CII I t o T o t a l = and mean t o CI CI I I a d u l t - h a t c h i n g f o o d conc. hood t o a d u l t - (ug c hood 1 i t e r - l )

P. micans 3 .8 none none 3.8 70.9

P. micans 2 .8 2.0 none 4.8 41.8

G. polyedra none none none none 41.0

G. splendens 23.6 3.9 none 27.5 9- -5

L. borea l i s 33.6 2.6 none 36.2 48.3

L. borea l i s 27.8 2.4 7.9 38.1 49.9

CI I I t o T o t a l = CV h a t c h i n g

t o C V L. borea l i s 7.1 none 2.3 9.4

102.3 L. boreaZis 6.2 2.1 1 . 1 9.4

100.6

*Expressed as percentage o f t h e number o f an ima ls a t t h e b e g i n n i n g o f each exper iment .

than those grown at 101 pg C liter1. This means that if ingestion is related to unit body weight of copepod the amount of food eaten by an animal at 101 pg C liter1 would be less than double the amount of

Table 3. Calanus helgolandicus. Average amount o f food ingested ( p g C ) per animal in- cluding ranges f rom NII t o adulthood at t w o d i f - ferent food concentrations. Number o f experi-ments i n parentheses. CV at 101 yg C liter-' could no t b e raised at controlled food concentrations be- yond m e d i u m CV due t o a failure o f t h e particle counter.

Lauderia boreaZis 49 100

(ug C l i t e r - l )

NII t o CI 4.61 ( 2 ) 7.84 ( 3 ) 4.34-4.88 6.07-10.07

CI t o CII I 11.78 ( 2 ) 21.55 ( 3 ) 10.85-12.71 18.28-23.34

CI I I t o CV 48.28 12) 98.00 (31 47.35-49:zi 94.10-100.38

CV t o A d u l t 69.23 ( 2 ) "40.84" ( 1 ) 68.03-70.45

T o t a l f r o m NII t o A d u l t h o o d 133.90

42 Paf fenhofer

Table 4. Calanus helgolandicus. Amount of food ingested ( p g C ) , u p p e r number, p e r animal f rom NII t o adul thood a t different food concentrations ( a v g i n p C liter-'), lower number.

Food sp. P. micans G, polyedra P. micans G. splendens

NII t o CI 5.33 8.43 7.40 46.1 50.0 104.8

NII t o 22.55 CI I I 71.2

CI t o CIII 16.25 13.80 18.16 40.6 43.6 91.4

CIII t o 245.38 158.31 202.20 264.23 CIII t o 68.33 e a r l y a d u l t 31.7 30.8 C V

C V t o 90.1

111.07 e a r l y a d u l t

93.8

Total NII 266.96 180.54 286.78 204.96 t o e a r l y 41.8 41.0 70.9 95.4 a d u l t

food ingested by a copepod at 49 pg C at 49 pg C liter1 and 50% more than ani- liter-l. mals feeding on G. polyedra at 41.0 pg C

Calanus helgolandicus feeding on P. mi- liter1 (Table 4) . These differences in in- cans at an average food concentration of gestion of carbon are attributed to the car- 41.8 pg C liter-l ingested twice as much bon to volume ratios (Table l),as grazing carbon as specimens feeding on L. borealis rates of the copepods in these experiments

Table 5. Body weight ( p g d r y wt a n d p g C ) of copepodid stages a n d adul ts of Calanus helgolandi- cus ingesting Lauderia borealis a n d dinoflagellates a t different food levels.

S tage CI CI I I CV Youilg Medi urn

Adult Adult L .boreaZ i s a ) 3 . 8 5 ( 1 4 4 ) 13 .85 ( 8 9 ) 43.9 (41) 43.9 ( 4 1 )

49 uq C l i t e r b ) 3.60-4.10 13.60-14.20 32.1-57.0 71.3-114.0 c ) 1 .23 4.85 16.2 32 .3 d ) 48.7 46.3 49.5 47.3

L. boreal i s a ) 4.67 (156) 17.2 (58) 65 .4 (15) 129.0 (20) 1 0 1 ~ a C l i t e r b) 4 .53-4.90 15.7-19.6 ' 42.2-82.0 --

c j 1 .49 6.00 24.2 47.7 d ) 97.7 102.0 101.7 105 .5

Gymodiniwn a ) 5 .01 (128) 19.85 (46) 83 .1 (27) 165.7 (17) splendens -1 b ) 4.93-5.08 19.3-20.7 77.8-91.1 130.0-185.6

95.4 uq C l i t e r c ) 1 .62 6 .95 30.7 61.3

Prorocentrwn a j 3 .58 micans -I b) 3 .41-3.85

4 1 . 8 ~ g C l i t e r c ) 1 .15 d ) 46.1

Gonyaulaz a ) 4.38 (105) polyedra -I b ) 4.32-4.44

4 1 . 0 p g C l i t e r c ) 1 . 4 0 d ) 50 .0

P. micans -1 a ) 7 0 . 9 p g C l i t e r b)

c ) d )

* a ) Ar i thmet ic mean of d ry weight ( u g ) , number of weighed animals i n parentheses.

b ) Ranges. c j ~ o d y weight (pg C ) . d ) Food concen t ra t ion (ug C 1 i t e r - 1 ) .

43 Growth efficiency of C. helgolandicus

Table 6. Body weight (pg dry wt) of copep-odid stage V and adult male and female of Cala- nus helgolandicus originating from the Pacific Ocean off La Jolla, 1971.

P a c i f i c Ocean 23 March 118.9 221.9 176.4 30 March 95.7 183.0 148.4 14 May 162.2 -25 May 78.6 114.2 -

must have been similar, as is shown by the amount of ingested cell volume. Copepods feeding from NII to adult on L. borealis at 49 pg C liter1 ingested 1.57 mm3, com- pared to 1.25 mm3 of P. micans at 41.8 pg C liter1, and 1.17 mm3 of G, poly-edra at 41.0 p g C liter1. Although the L. borealis copepods weighed less than the dinoflagellate copepods at these food con- centrations, their grazing rates were in the same range because the L. borealis chains were larger in size than the two dinoflagel- late species, which resulted in a slightly higher grazing rate. The comparatively small amount ingested by copepods feeding on G. splendens at 95 pg C liter1 is attrib- uted to the mediocre condition of the cope- pods, as indicated by their high mortality (Table 2 ) .

Body size and grototh rates-To calculate growth rates and gross growth efficiencies the body weights of different stages of C. helgolandicus were determined (Table 5 ) . Average food concentrations indicate little

variation among life periods. No standard deviations of body weights were calculated as arithmetic means were mostly based on two to four batches of animals. Young adult refers to animals having moulted to adulthood within the previous 12 h; me-dium adults had moulted 4 to 6 days later.

The influence of food concentration on body weight is demonstrated for animals feeding on L. borealis at 49 and 101 pg C liter1, as all stages feeding at the higher concentration are markedly heavier. The data for copepods feeding on P. micans in-dicate that a higher food concentration does not always have to result in higher body weights, as CIII and early adults feeding at 41.8 pg C liter-l were in the same range as those at 70.9 pg C liter-?.

The type of food, at similar concentra- tions, influences the body weight of grow- ing copepods differently: animals feeding on L. borealis at 49, on P. micans at 41.8, and on G . polyedra at 41 pg C liter1 hardly differ as CI and slightly as CIII, but differ considerably as adults.

Copepods from the Pacific Ocean were collected for a comparison of body weights of laboratory and ocean specimens (Table 6). The specimens from the ocean should be considered as medium CV and medium adults. Dry weights of ocean females ranged widely, their range encompassing all laboratory females except those which had been feeding on L. borealis at 49 pg C liter1,

Table 7. Daily growth rates of Calanus helgolandicus for different periods of lifetin~e feeding on Lauderia borealis and three species of dinoflagellates (coefficient of daily exponential growth = k ) .

Avg f ood i. borea l i s G. splendens P. micans conc (ugC l i t e r - l )

49 101 95.4 41.8

h a t c h i n g 0.29 0.36 0.40 0.36 t o CI

CI t o CIII 0.26 0.33 0.38 0.41 CIII t o CV 0.19 0.24 0.33 CIII t o 0.19 young a d u l t

C V t o young 0.13 0.14 0.20 a d u l t

Younq t o med7 urn

0.07

a d u l t

G. polyedra 41 .o

P. micans 70.9

0.41 h a t c h i n g t o CIII

0 .41

0.195(1) 0.190(11)

0.37

0.17

0.04 0.05

44 Puff enhof er

A Lauderia borealis 49pgClliter

A L.borealis 101vgClliterI

N II C I C Ill CV adult

Calanus -stages

Fig. 1. Gross growth efficiency of Calanus helgolandicus feeding for various periods of its juvenile life on Lauden'a borealis at different food concentrations. The data are based on pg C liter-' organic carbon. The two experiments with L, bore-alis at 49 pg IiteP were run simultaneously and the results are combined. The data represented by the lower line at 101 pg C liter-' are from one experiment that was split into two when the cope-pods attained CI.

Coefficients of daily exponential growth decrease during the course of later juvenile life (Table 7). A general pattern in all these experiments is that growth coeffi-cients hardly change during the first two periods of the juvenile life (hatching to CI, CI to CIII), drop considerably during the late copepodid stages, and attain minimum values in early adult life. The pronounced decrease of k seems to begin at a stage when ocean C. lzelgolandicus starts migrat-ing vertically. The favorable effect of dino-flagellates, already shown for mortalities and dry body weights, is also expressed as highest growth rates for all periods of juve-nile life. Maximum growth rates at food concentrations between 40 and 100 pg C liter-l will probably be close to k = 0.40, as indicated in all experiments but the L. borealis at 49 pg C liter1.

Gross growth efficiency-As the amounts of ingested food per juvenile period and

I I I I I I young med~um

NII CI Clll CV adult adult 9

Z

CALANUS-STAGES

o Gymnodinium splendens 95 pgC/liter Gonyaulax polyedra 41pgC/liter Prorocentrum micans 42pgC/liter P m~cans71 pgC/l~ter

Fig. 2. Gross growth efficiency of Calanus hel-golandicus feeding for various periods of lifetime on three species of dinoflagellates. The data are based on organic carbon.

the body weight of copepodids and adults had been experimentally determined, the gross growth efficiency for the defined juvenile life periods could be calculated (Figs. 1 and 2 ) . The moults are not in-cluded in the gross growth efficiency de-terminations.

Calanus helgolandicus fed on L. borealis of 19-p diameter showed an almost identi-cal pattern of change in gross growth effi-ciency during their juvenile life in all ex-periments. Gross growth efficiency attained maximum values during the period from CI to CIII, then decreased gradually. Copepods feeding at 49 pg C liter-? had a markedly higher degree of food conversion than those at 101 p g C liter1. Maximum values during one life period were 32% gross growth efficiency at 49 and 24% at 101 pg C liter-l.

Experiments with C . helgolandicus feed-ing on P. micans and G. polyedra were con-ducted later and designed to cover a longer period of the copepods' lifetime, animals being classified as young and medium adults as described earlier. Gross growth efficiencies of juvenile copepods feeding on P. micans at 42 and G. polyedra at 41

Growth efficiency of C. helgolandicus

Table 8. Calorific content of five species of phytoplankton and the percentage of ash.

Skeletonema costatwn

( x ) * 5,247 SO 2120.9 Range 5,053-5,380 n + 5 Ash (as

% o f 40.4 d r y w t )

*

Thalassiosira r o t u l a

5,479 i 5 7 . 3 5,439-5,520

2

38.6

Lauderia Gumnodinim Prorocentrwn boreal i s splendens micans

5,418 5,708 5,218 257.3 i 1 6 6 . 1 ?52.0 5,316-5,502 5,419-5,830 5,166-5,289

7 5 4

51.5 17.7 9.0

A r i t h m e t i c mean ( c a l / g ash- f ree d r y w t ) . + Number o f c a l o r i f i c de te rm ina t ions .

pg C liter1 are a bit higher than those of animals ingesting P. micans at 71 pg C liter1, but below those of animals ingesting L. borealis at 49 pg C liter1. Efficiencies de- crease considerably when animals moult to adulthood and range from 3.7-10.1% for the first 4 6 days of adult life. The pattern of increase and decrease in gross growth efficiencies is the same for animals fed on L. borealis and all dinoflagellates except G. splenbns, in which case the highest ef- ficiency, 35%, was recorded for the period CIII to CV, the maximum recorded during all experiments. Moreover, the G. splen-dens efficiencies from CI to adulthood, de- spite the high food concentration of 95 pg C liter1, surpass the peak efficiencies re-corded for copepods feeding on L. borealis at 49 pg C liter1. I cannot explain the comparatively high efficiencies, except that G. splendens is unarmored whereas P. mi-cans and G. polyedra are armored. An un- armored dinoflagellate may be more easily digested by the copepod which can thus incorporate a larger amount of organic mat-

ter than when feeding on armored species. All copepods feeding on dinoflagellates were in excellent condition, showing frantic escape maneuvers when approached with a glass rod or a pipette and moving faster than those feeding on L. borealis or other diatoms.

In addition to the experimentally fed di- atoms the calorific content of two more species was determined (Table 8). The low standard deviations for all five species indicate that the samples were rather uni- form in composition, which is also shown by the ranges of values.

The calorific content of young adult C. helgolandicus reared at 49 and 101 pg C liter-l of L. borealis and 95 pg C liter1 of G. splendens is given in Table 9. Calorific measurements were also made of adult copepods collected from the Pacific Ocean off La Jolla between March and May 1971. Each sample was combusted separately. The calorific content of C. helgolandicus reared at food concentrations close to 100 pg C liter1 in the laboratory was about the

Table 9. Calorific content of Calanus helgolandicus adults grown at different conditions, expressed as cal per g ash-free dry wt. Symbols as in Table 8.

Laboratory Lauderia L. boreal i s Gymnodinim P a c i f i c Ocean boreaZis 101 sp lendens o f f La J o l l a

4 9 9 5 ( p g C l i t e r - ' )

( x ) S0

5,152 t167.7

5,619 t281 .3

5,790 i84 .8

5,656 t 9 2 . 8

Range n

5,020-5,385 4

5,276-6,052 5

5,730-5,850 2

5,539-5,839 8

46 Paf fenlzofer

Table 10. Gross growth efficiencies for Cala-nus helgolandicus for the period from NII to young adult, based on calories, organic carbon, and dry organic substance.

Cal ?i Organic Dry organic C % substance %

L. borealis 22.3 24.1 2 2 . 4 49 pq C liter-'

L. borealis 17.8 18.5 17.2 101 pg C liter

G. splendens -1 33.3 29.9 32.9 95 u a C l i t e r

P, micans 42 pg C l i t e r

G. polyedra -1 41 pg C liter

P. micans 20.0 71 pg C l i t e r

same as that of animals from the ocean. Adults reared at a food density of 49 p g C liter-I were significantly lower in energy content than ocean adults. There was in- sufficient material to determine the calorific content of copepods feeding on G. polyedra and P. micans.

Gross growth efficiencies for C. helgo-landicus for the entire period from NII to young adult are presented in Table 10. They range, as related to organic carbon, from 18.5 to 29.9%. The variation of gross growth efficiencies at average natural food concentrations as found off La Jolla (here 40 to 70 p g C liter1) is comparably low, between 20.3 and 24.1%. A comparison of gross growth efficiencies based on calories, organic carbon, and dry organic substance shows only slight differences.

The data on gross growth efficiencies from NII to adult for copepods feeding on L. borealis indicate that over the range of concentrations used, food conversion is in- versely related to food concentration. This could not be confirnzed, even without the G. splendens experiment, for copepods feeding on dinoflagellates. The results for animals ingesting G. polyedra and P. mi- cans range between the data for L. borealis at 49 and 101 pg C liter-I. It seems that for average phytoplankton concentrations between 40 and 100 pg C liter-l, one can expect for the period from hatching to

adulthood gross growth efficiencies in the range of 18 to 24% at 15OC.

Concentrations of dinoflagellates near 20 pg C liter-I might have resulted in conver- sion data similar to those at 49 pg C liter1 of L. borealis, as carbon ingestion of dino- flagellates at 20 pg C liter1 by copepods \vould have been similar to that of L. bore-alis at 49 pg C liter-l.

Discussion

Studies on feeding, growth, and food conversion of juveniles of marine planktonic copepods have been sparse until now be-cause of methodological difficulties. De-spite considerable differences in the meth- ods and organisms used, a brief comparison of results seems useful.

Our results on mortality are generally in agreement with those of Mullin and Brooks ( 1970a): most mortality occurs during the naupliar stages. The degree of mortality of copepods feeding on L. borealis supports earlier studies (Paffenhofer 1970, 1971) in which mortalities ranged from 1.8 to 13.5% at close to 100 pg C liter-I and 26 to 33.5% at about 50 pg C liter-I for C. helgolandicus feeding on L, borealis of 19-p cell diameter.

Mortalities of copepods feeding on dino- flagellates at 41 to 71 pg C liter1 were an order of magnitude lower than of those feeding on L. borealis at 49 pg C liter1 but similar to those feeding on the same species at 101 pg C liter1. In addition to food quality and digestibility these differ- ences could be related to the amount of food ingested per copepod. A rough esti- mate for copepods feeding on L, borealis at 101 pg C liter-I is about 260 pg C in- gested from hatching to adult, close to the amounts ingested by copepods feeding on P. micans (Table 4 ) .

The only previous detailed data on the ingestion by juvenile marine planktonic copepods at given food concentrations are those of Mullin and Brooks (1970a,b). Their C. lzelgolandicus (1970a), feeding on T. fluviatilis at 15OC at 177 pg C liter-I, ingested about the same amount of phyto- plankton carbon (127.1 pg C from NI to adult) as my animals at 49 pg C liter-I

47 Grou;d~ efficiency of C. helgolandicus

(133.9 pg C) . Not only different cultiva- tion techniques but also smaller particle size may have accounted for the compara- tively low ingestion by copepods eating T. fluviatilis. This diatom occurs mainly as a single cell 11-18 p long and 6-9 p wide, while L. borealis was 19 p wide and had particle lengths (chains) from 30 to about 200 p in my experiments.

The body weights of "medium" adult fe- males from the laboratory are well within the upper range of females from the ocean (Tables 5 and 6) . The weight of "young" adult females, being in the lower range of ocean specimens, would have matched their mehium weight after an additional 4 to 6 days of feeding. From these data one could assume that laboratory and ocean copepods had ingested similar amounts of food, which is supported by the fact that average phytoplankton concentrations in the upper 50 m of the Pacific Ocean off La Jolla were close to 50 pg C liter-I during spring, attaining peaks of 300 pg C liter1 (Strickland 1968; Mullin and Brooks 1972). The ingestion of similar amounts of food could have resulted in similar growth rates and generation times. Juveniles of C. hel-golandicus in the ocean could even have in- gested more than laboratory animals; they tended to be abundant in samples with higher crops of phytoplankton (Mullin and Brooks 1972).

The results from Mullin and Brooks (1970~)on daily exponential growth rates of C. helgolandicus indicate a moderate de- crease from the first to the third juvenile life period. Their k-values at a food concen- tration of 177 pg C liter1 almost coincide with those of C. helgolandicus feeding on L. borealis at 49 pg C Liter1. This is not unexpected, as the amount of carbon in- gested in both experiments during the ju- venile life period was almost the same.

Petipa (1967) calculated the daily incre- ment in calorific content of C. helgolandicus and A. clausi from the Black Sea by combin- ing field and laboratory data (Table 11). Whereas A. clausi had a growth pattern similar to the copepods in my experiments, her C. helgolandicus nauplii showed com-

Table 11. Mean daily increment of one cope-pod expressed as percent of the caloric content of one copepod (from Petipa 1967).

Copepod Staqe

C. heZgo-Zandicus

A. clausi

Nauplii 6 . 3 2 0 . 3 (NIII

r T- -t n N V T I

CII CIII CIV

parably slow growth. Petipa et al. (1970) found slightly slower growth: daily incre- ments for nauplii ranged from 6.3-9.4%, for early copepodids from 14.4-18.8% of their body weight.

The decrease in growth rates ( k ) during the juvenile life of C. helgolandicus is ac- companied by a decrease in ingestion rate per unit of copepod body weight (Paffen- hijfer 1971: figure 7). Copepods feeding on L. borealis at 49 (101) pg C liter-l showed a decrease of 55% (61%) in daily growth rate k as compared to a decrease of 56% (63%) in amount of ingested food per unit body weight of copepod from late naupliar stages to late CV/young adult. Changes in feeding and growth rates ap- pear to be closely connected during the juvenile life of C. helgolandicus.

The only data on gross growth efficien- cies of juveniles of marine planktonic cope- pods available for comparison are those presented by Petipa (1967) and Mullin and Brooks ( 1970~) . Petipa ( 1967) investi- gated food conversion of C. helgolandicus and A. clausi (Fig. 3 ) ; both show, with in- creasing age, a change in their ability to in- corporate ingested energy. Her C. helgo-landicus attained the highest degree of conversion at CI (SO%), gradually drop- ping to 2% for adult females. Acartia clausi, which migrates vertically little if at all, reached a peak at CIII (23%), and then de- creased to 1.8% for adult females. One can assume from Petipa's and these results that C. helgolandicus, A. clausi, and possibly

Paf fenhofer

The results of Mullin and Brooks (1970~) for juvenile C. helgolandicus and R. nasutus did not show patterns in change of efficien- cies as presented in Figs. 1to 3 except when both copepod species were feeding on T. fluviatilis at 10°C. Then gross growth effi- ciencies of the second juvenile life period exceeded those of the preceding and follow- ing periods. In four of their six experiments, gross growth efficiencies for the two cope- podid life periods exceeded that of the naupliar period.

To facilitate comparison with my results, data of various investigators on the gross growth efficiencies of three species of the genus Calanus and of R. nasutus are pre- sented in order of the years of publication (Table 12). All food concentrations ex-

NII NVI Cl Cll Clll CIV CV $? ceeded those used in my experiments. The STAGES figures for juveniles and for hatching to

adulthood (Corner et al. 1965, 1967; Mullin Fig. 3. Gross growth efficiency of Calanus

helgolandicus and Acartia clausi as nauplii, single and Brooks 1970a) surpass the gross growth copepodid stage, and adult female from the Black efficiencies for C. helgolandicus in my Sea (data from Petipa 1967). studies. A decrease in temperature did not

seem to affect the food conversion of R. nu-other herbivorous or omnivorous planktonic sutus (Mullin and Brooks 1970~) . Gross copepods have specific patterns for the de- growth efficiencies for CVs and adults gree to which they can incorporate ingested (Butler et al. 1969, 1970) are higher than food during their juvenile stages. my results for adults (3.7-10.1%) and those

Table 12. Gross growth efficiencies of Calanus finmarchicus, Calanus helgolandicus, Calanus h g p e ~ - boreus, and Rhincalanus nasutus.

Reference S p e c i e s and Temp OC Food conc. Food sp. Gross g r o w t h Based on S tages e f f i c i e n c y %

Conover C. hyserboreus 2-5 6.4-6.7 mg 1". f luvia- 13.0-17.3 a s h - f r e e 1964 m o s t l y CV a s h - f r e e ry t i l i s Oabo- d r y w t

w t 1 i t e r - P r a t o r y ) Conover C. hyperboreus 2-5 1.7-1.8 mg r. f luvia- 18.6-36.4 a s h - f r e e

1964 CV a s h - f r e e d r y t i l i s ( l a b o - d r y w t w t 1i t e r - I r a t o r y )

C o r n e r et al. C, heZgoZandicus 10 Approx 210 SkeZetonerna 35.7 N i t r o g e n 1965 C. finmarchicus u g C 1 i t e r - I c o s t a t m

C T T t n C V - - - -- - . C o r n e r et al. C, fi.marchicus 10 N o t g i v e n Not g i v e n 34 N i t r o g e n

1967 h a t c h i n g t o ( s e a ) a d u l t h o o d

B u t l e r et al. C. f i rnarchieus 12 N o t g i v e n N o t g i v e n 18.9-34.6 Phosphorus 1969 C. he Zgo Zandicus ( s e a ) 21.4-37.7 N i t r o g e n

CV and- a d u l t s B u t l e r et al. C. f invarchicus 6-18 Approx 490 I"haZassiosira 17.2 Phosphorus

1970 C. he Zgo Zandicus p g C l i t e r - ' fp . CV and a d u l t s ( s e a ) ,. costatum 26.8 N i t r o g e n

Mu1 1 i n and RhincaZanus 10 352 u g C 1 i t e r - I T , fZuv ia t iZ i s 30 Carbon Brooks nasutus 15 196 p g C l i t e r - l 1 " . fZuv ia t iZ i s 37. Carbon 1970a h a t c h i n g t o 10 200 ug C b r igh t - 1it e r - l ~ i t ~ l m

a d u l t h o o d weZZii 34 Carbon 15 148 p g C l i t e r - l o . brightueZZii45 Carbon

49 Growth efficiency of C. helgolandicus

of Petipa (1967) which were 5% for CV and 2%for adult females of C. helgolandi-cus.

Although all food concentrations given exceeded those in my experiments the re- sulting gross growth efficiencies were mostly also higher than mine. One could have expected that higher food concentra- tions should have resulted in higher inges- tion, leading to a reduced gross growth efficiency. The main reason for the differ- ences between my data and those of most other investigators cited, excluding some differences in temperature, is no doubt in the different methods used for culturing planktonic copepods.

All my results indicate that C. helgokncli-cus can grow from hatching to adulthood at environmental phytoplankton concentra- tions of about 50 pg C liter-l without being subject to excessively high mortalities or low growth rates. We do not know whether food concentrations of 50 pg C liter1 are sufficient to induce egg produc- tion or whether dense food patches of 100 pg C liter1 or more are necessary to stimu- late reproduction in C, helgolandicus.

As C. helgokndicus is at times the domi- nant copepod (by numbers) in the neritic waters off La Jolla it is of interest to detect the reasons for that. Thus, the population dynamics of other abundant copepod spe- cies should be studied in relation to food species and concentration. This and data on the seasonal occurrence of these cope- pods should infonn us to what extent they would be able to compete with C. helgo-landicus.

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50 Paf fenhofer

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Submitted: 20 November 1974 Accepted: 8 August 1975