Acartia tonsa

Marine BiOlOgy

Marine Biology 99, 341 352 (1988)

..............

9 Springer-Verlag 1988

Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implications for determination of copepod production U. Berggreen, B. Hansen and T. Kiorboe * Danish Institute for Fisheries and Marine Research, Charlottenlund Castle, DK-2920 Charlottenlund, Denmark

Abstract

Introduction

Clearance rates on different sizes of spherically shaped algae were determined in uni-algal experiments for all developmental stages (NII through adult) of the copepod Acartia tonsa, and used to construct food size spectra. Growth and developmental rates were determined at 7 food levels (0 to 1 500 #g C 1- 1 of Rhodomonas baltica). The lower size limit for particle capture was between 2 and 4 #m for all developmental stages. Optimum particle size and upper size limit increased during development from ~ 7 #m and 10 to 14 #m for NII to NIII to 14 to 70 #m and ~250 #m for adults, respectively. When food size spectra were normalized (percent of maximum clearance in a particular stage versus particle diameter/prosome length) they resembled log-normal distributions with near constant width (variance). Optimum, relative particle sizes corresponded to 2 to 5% of prosome length independent of developmental stage. Since the biomass of particulate matter is approximately constant in equal logarithmic size classes in the sea, food availability may be similar for all developmental stages in the average marine environment. Juvenile specific growth rate was exponential and increased hyperbolically with food concentration. It equaled specific female egg-production rate at all food concentrations. The efficiency by which ingested carbon in excess of maintenance requirements was converted into body carbon was 0.44, very similar to the corresponding efficiency of egg-production in females. On the assumptions that food availability is similar for all developmental stages, and that juvenile and female specific growth/egg-production rates are equal, female egg-production rates are representative of turnover rates (production/biomass) of the entire A. tonsa population and probably in other copepod species as well. Therefore, in situ estimates of female fecundity may be used for a rapid time- and site-specific field estimate of copepod production. This approach is shown to be fairly robust to even large deviations from the assumptions.

In the last decades a voluminous literature has dealt with feeding, particle selection, growth and fecundity in planktonic copepods in relation to concentration and composition of food. Most of these studies however, have considered adults, and comparatively little is known about nutrition and growth of juveniles, particularly nauplii. Adult copepods generally feed upon particles 5 to i0 #m in size or larger (e.g. Mullin 1980). Since the morphology of the feeding appendages in nauplii differs from that of copepodites (Fernandez 1979), their particle capture is presumably different. Owing to their smaller body size one might, therefore, hypothesize that nauplii are able to feed on smaller particles. Thus, copepod nauplii may potentially constitute a link between the "microbial loop" (e.g. Azam et al. 1983) and the "classical" food chain. Several laboratory studies on copepod growth and development have been conducted under conditions of food satiation. Thus, the effect of temperature is now well described (e.g. Miller et al. 1977, McLaren and Corkett 1981, Peterson 1986). A major aim of such studies has been to develop methods for determining copepod production in the sea (e.g. McLaren and Corkett 1981). However, an increasing body of evidence suggests that planktonic copepods are often food limited in nature (e.g. Boyd 1985, Checkley 1985, Frost 1985, Runge 1985). Still, very few studies deal with the effect of food concentration on development and growth in juvenile copepods (e.g. Vidal 1980). Phytoplankton biomass and production is very variable in nature, from seasonal and oceanwide scales to daily and kilometer scales (e.g. Legendre 1981). In view of the patchy distribution of copepods in the sea, it is therefore of interest to study variation in secondary production on the same spatial and temporal scales. However, the traditional cohort approach to estimate production does not allow a fine-scaled resolution. We need rapid timeand site-specific methods for measuring secondary production comparable to the C-14 method for determining primary production. In the present study we used the planktonic

* Author to whom correspondence should be addressed

U. Berggreen et al. : Food size spectra and growth in Acartia tonsa

342 eopepod Aeartia tonsa, representing one of the most abundant genera in neritic waters. Our aims were: (1) to determine changes in the food size spectrum during development: (2) to determine stage-specific growth rates in relation to food availability: (3) to consider these results in the context of site- and time-specific methods to estimate copepod production.

Materials and methods

Copepods were obtained from a laboratory culture of Acartia tonsa (Stottrup et al. 1986). All experiments were conducted in prefiltered (0.2 #m) seawater (27%o S, 16 to 18 ~ Phytoplankton species of approximate spherical shape were selected and grown in batch cultures. Algae in exponential growth were used for experiments. Linear dimensions of algae (length and breadth) were measured under the microscope and volume and equivalent mean spherical diameter (ESD) determined by a Coulter Counter (TAII with 50, 100 or 140 #m orifice). Carbon and nitrogen content were measured in algae filtered (0.3 bar) onto precombusted (550 ~ W h a t m a n n G F / C filters (Perkin Elmer CHN-instrumental analyzer 240 C) (Table 1). F o o d size spectra Particle size selection in copepods may depend on their feeding prehistory and on the size distribution and "quality" of particles available (e.g. D o n a g h a y and Small 1979, Poulet 1973, 1974). In the present experiments, the first two factors were considered by standardizing the feeding prehistory and offering only one algal species (size) at a time, respectively. F o o d size spectra were derived from clearance measured on up to 10 algal species for individual developmental stages. An artifical cohort of copepods was obtained by transfering eggs hatched within 10 h to a 100 1 tank where they

were fed ad libitum a mixture of all the experimental algae offered in equal biomasses. This cohort passed through ca. 1 developmental stage per day. Clearance experiments were carried out each day with copepods from the cohort until maturity was reached. Copepods were staged and total length (nauplii) or cephalothorax length (copepodites) measured daily (n=30). Prior to experiments copepods were acclimated for 2 to 3 h in glass jars with suspensions of the different algal species. Copepods were then pipetted into 133 ml (small nauplii), 300 ml (large nauplii, small copepodites) or 600 ml (large copepodites) screw-cap bottles filled with the appropriate algal suspensions. Algal growth medium was added in sufficient amounts to prevent nutrient limitation. The bottles were fixed on a slowly rotating (2 rpm) wheel and incubated for 24 h in dim light (16 h light: 8 h darkness). Initial algal concentrations were 0.6 to 0.7 ppm, which is below the incipient limiting concentration of Acartia tonsa for all algal species (Jensen 1987). Concentrations of copepods were varied according to size. Pilot experiments with naupliar Stage III (NIII) revealed that clearance was independent of the concentration of individuals up to ca. 1 m l - 1 (equivalent to a biomass of ca. 250 #g C 1 t), where upon it declined. In all experiments we attempted to maintain a nominal concentration of individuals of 75 to 100 #g C 1-1, corresponding to ca. 3 to 4 N I m1-1 or 0.025 copepodite stage VI (CVI) m l - 1. U p o n termination of the incubation, the actual concentration of copepods was determined and duplicate 50-ml water samples were analysed on the Coulter Counter. For large algae (Gymnodinium splendens, Coccinodiscus granii), samples were filtered onto 8 #m pore size Sartorius filters with a preprinted grid, and algae were counted under the dissecting microscope (n_> 400, or entire bottle content counted). During incubation algal concentration was reduced on the average by ca. 25%. Three experimental and two control bottles were run for each treatment (algal species, copepod stage). Clearance was calculated by the equations of Frost (1972).

Table 1. Linear dimension (length x breadth), equivalent mean spherical diameter (ESD) and carbon and nitrogen content of cultured phytoplantkon used in experiments. ESD was measured by a Coulter Counter except for Gymnodium splendens and Coccinodiscus granii where it was calculated from linear dimensions. C:N=weight ratio of carbon to nitrogen, n=number of determinations of N- and C-content. Mean _+SD

Species

Nannochlorisrnaculata Pavlovalutheriii Isochrysis galbana Dunaliellabioculata Rhodomonas baltiea Amphidinium earterae Thallasiosirafluviatilis Scripsiella far6ense Gymnodinium splendens Coceinodiseus granii

Linear dimensions (~m) 1.8 3.6-4.5 4.5 7.2 7 x 13 11 x 14 11 x 14-18 26 x 28 - 40 47-71 x 7 1 - 9 4 141 - 188 x 235 -259

ESD (#m)

C cell- 1 (pg)

1.90 4.04 4.70 6.36 6.91 9.33 14.20 19.00 71.00 247.00

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3 3 3 3 4 3 3 3 2 0

U. Berggreen et al.: Food size spectra and growth in Acartia tonsa

343

Table 2. Rhodomonas baltica. Growth experiments. Average (_+ SD) initial concentration after food addition and average (_+ SD) reduction in cell concentration per 24 h. A and B series shown separately Food level

0

1

2

3

4

5

6 1 549 -+460 1 737_+208

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0 0

86 __19 93+_23

123 _ 18 129_+22

222 -+ 19 228-+23

407 -+ 32 443-+35

812 ___ 96 878_+105

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0 0

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17+14 21-+17

36+ 9 25___17

41-+15 27-+14

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Ingestion and growth Experiments to determine ingestion and growth rates during development in Acartia tonsa were run in two replicate series, A and B. In both cases, nauplii hatched within ca. 10 h were distributed between seven 5.5 1 polypropylene, screwcap bottles. Initial concentrations were 3.3 +0.4 N I m l - 1. The copepods were either starved or fed Rhodomonas baltica at six different concentrations (Table 2). The bottles were fixed on the plankton wheel in dim light (12 h darkness:t2 h light). Each day individuals were sampled for determination of concentration (25 to 1 000ml or 80 to 25 copepods counted), length and stage distribution (n > 30) and C- and N-content (every 2nd day). Copepods for CHN-analysis were rinsed of particulate matter by sedimentation and decantation and then anaesthetized (MS222) for counting. Between 2 500 and 5 000 NI and 40 CVI, equivalent to ca. 100 #g C and 25 #g N, were rinsed three times in artificial seawater (where they woke up) and remaining particulates were removed under the dissecting microscope. Finally the copepods were concentrated in a pile on a glass slide, excess water was removed by a capilar, and the sample was freezedried for 24 h ( - 3 0 ~ and stored in a desiccator until analysis. The algal concentration was measured (Coulter Counter, 100 #m orifice) daily and fresh phytoplankton culture was added to reach the nominal food concentrations. Between 25 and 50% o f the water was changed daily, and the eopepods were transfered to rinsed bottles every 3rd day. We attempted to keep the biomass of copepods and the grazing pressure constant throughout the experiments. Where necessary, additional individuals were removed and counted to allow computation o f mortality rates. The experiments were continued until maturation or until all copepods had died (either due to sampling or "natural" mortality). Control bottles without copepods were run to determine algal growth rates, and copepod clearance and ingestion rates were calculated by the equations of Frost (1972).

Results F o o d size spectra Clearance is plotted as a function of algal ESD in Fig. 1 for all naupliar and copepodite stages (log scales) of Acartia tonsa. It is obvious that clearance depends consistently on algal size except for two algal species. Scripsiella fardense

25-+ 13 16_+ 9

Table 3. Acartia tonsa. Regressions of clearance (F, ml ind- 1 d- 1) versus body mass (W, #g C ind -~) on eight algal species: In F = lna + b In W. r z = coefficient of determination, n = number of determinations. See Fig. 2 for a graphical presentation Algal species Pavlova lutherii lsochrysis gaIbana Dunaliella bioeulata Rhodomonas baltica Amphidinium carterae 7hallasiosirafluviatilis Scripsiella far6enese Gymnodinium splendens

a 0.73 2.41 0.94 5.17 3.69 14.36 6.23 10.86

b-+95% CL

r2

n

1.00 + 0.27 1.31 _+0.20 0.46 +_0.70 0.93_+0.18 1.11 _ 0.32 1.80__0.26 1.08 _ 0.80 1.01 +0.46

0.90 0.95 0.71 0.90 0.90 0.95 0.61 0.90

11 11 6 15 9 13 8 6

was cleared less efficiently than expected on the basis of its size by copepodite and adult copepods (not offered to nauplii). Amphidinium carterae was cleared inefficiently by copepodite stages. These two species were therefore ignored when determining the food size spectra for the abovementioued developmental stages (Fig. 1). Size spectra were similar in shape between stages, and based on cases where large algae were offered, appeared bell-shaped. The particle size of maximum clearance increased with increasing stage. It was close to 7/~m ESD for NII-NIV, ca. 14 #m ESD for N V - C I I I and 14 to 70/~m ESD for subsequent stages. The lower limit for measurable clearance was, for all stages, between 1.9 and 3.7 #m ESD (Nanocloris maculata and Pavlova lutherii, respectively). Clearances measured by the Coulter Counter on N. maculata were often negative, indicating "production" of small-sized particles during incubation. Clearance on N. maculata, estimated by direct cell counts (by inverted microscope), however, also revealed near zero clearances. The upper size limit for particle capture increased with stage from 10 to 15/~m for the youngest nauplii to 250 #m for adults. In addition, the width of the particle size spectra tended to increase with developmental stage, at least when comparing early nauplii (NII to NIII) with subsequent stages. The absolute magnitude of clearance rates increased 2 to 3 orders of magnitude during development (Figs. 1 and 2). In Fig. 2 clearances are plotted against body mass (estimated from length-weight regressions, Fig. 3) for the different algal species and fitted by allometric power functions (Table 3). Only algae well within the appropriate food size spectra for each experiment were included. Most of the re-

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U. Berggreen et al.: Food size spectra and growth in Acartia tonsa 30

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Growth In the growth experiments, instantaneous mortaliy o f A c a r tia tonsa was a p p r o x i m a t e l y constant t h r o u g h o u t development. It was zero at the highest food level and increased

I 1

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Fig. 2. Acartia tonsa. Clearance vs body mass on eight different algal species. For each developmental stage (size) only algal species well within food size spectrum are included. Parameters of regression analyses are given in Table 3

monotonically with decreasing food concentration to 0 . 1 5 d -1 at F o o d level 1 and 0.59 d -1 at starvation. We conclude that the experimental conditions per se did not cause any mortality, and that m o r t a l i t y was caused only by food limitation at the lower food levels. In the following presentation, results from the two replicate growth experiments were pooled since they are statistically indistinguishable from one another. C a r b o n was used as a unit o f measure, but since the C:N-ratio o f the copepods was independent o f stage and food concentration (C:N = 4.1 4-0.1, 95% confidence limit) and similar to that

1. Acartia tonsa. Clearance in different developmental stages relative to equivalent spherical diameter of food algal species. Composition of developmental stages (dominating stage in bold types) at start of each experiment shown on each graph. Approximately one developmental stage will be passed during incubation, except for mature individuals. + Nannochloris maeulata; * Pavlova lutherii; 9 Fig.

Isochrysis galbana ; [] Dunaliella bioeulata ; ~xRhodomonas baltica; | Amphidinium earterae ; 9 Thallasiosira fluviatilis ; 9 Scripsiella faroensis ; o Gymnodinium splendens; x Coecinodiscus ~ranii

346

U. Berggreen et al.: Food size spectra and growth in Acartia tonsa 10000--

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8

weight (W, #g C) vs time (t, d) at seven different food levels: In W,=ln Wo+gt. g=estimate of specific growth rate; r2=co efficient of determination, n = number of determinations. See Fig. 4 for graphical presentation Food level

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3 5 6 t0 12 13 t2

5 of the food algae (Rhodornonas baltica, Table 1), we obtain the same results in terms of N. G r o w t h was exponential and constant t h r o u g h o u t development at all food concentrations (Fig. 4). We m a y therefore use the slopes of the exponential regressions (Table 4) to estimate specific growth rates. G r o w t h was negative in starved individuals, zero at the lowest food concentration, and then increased to a plateau o f 0.45 d - 1 at higher food concentrations (Fig. 5). G r o w t h was nearly independent of food concentration above ca. 500 #g C 1-1 o f R h o d o m o n a s

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Developmental rates of A c a r t i a tonsa in terms of median times required to reach a certain stage are given in Fig. 6 for the five highest food concentrations. Time to N I I was independent o f food concentration. Starved individuals and individuals fed the lowest food concentration did not moult beyond NII. A t food concentrations above Level 3 development was isochronal from N I I through CVI. The regression slopes (Table 5) estimate the developmental rates (stages time 1) and the reciprocal slopes the average stage durations (time stage t). These two parameters increased and

U. Berggreen et al. : Food size spectra and growth in Acartia tonsa

347 I

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growth rate. Data from Tables 4 and 5. Graph fitted by eye

Table 5. Acartia tonsa. Developmental rate (D) and stage duration

(l/D). See also Fig. 6 Food level

Developmental rate (stages h -1)

Stage duration (h stage -1)

rz

2 3 4 5 6

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263 35.8 26.8 25.7 25.2

0.94 0.99 0.99 0.99 0.99

T

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Discussion

decreased, respectively, with food concentration. There was a non-linear, sigmoid relationship between specific growth rate and developmental rate (Fig. 7) and, consequently, the stage weight varied with food concentration (Fig. 8 a). This trend became increasingly pronounced during development. (Fig. 8 b). The implication is that changes in growth rate due to variable food availability is mediated both by variation in size at stage and development rate.

Efficiency of growth At all food concentrations in the growth experiments, clearance and ingestion rates on Rhodomonas baltica confirmed

F o o d size spectra F o o d size spectra of Acartia tonsa were based on uni-algal experiments. It may be questioned to what extent these spectra are representative of food size-selection in the field, where a range of algal species/sizes are simultaneously available. Rigorous tests o f this question have been performed by Bartram (1981, Acartia tonsa and Paracalanus parvus) and Vanderploeg et al. (1984, Diaptomus silicis) and both found that size-selection spectra in adult females were invariant over a wide range of composition and concentration of natural seston and cultivated phytoplankton. A number of authors have, on the other hand, found that the (realized) size spectrum in suspension feeding copepods may be quite vari-

C6

348

U. Berggreen et al.: Food size spectra and growth in Acartia tonsa 1.5

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Specific ingestion rate, d -1

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Fig. 9. Acartia t~nsa. (a) Specific ingestion (i, d-t) integrated over entire experimental period relative to concentration of R. baltiea (C, #g C 1-1). Graph shows relationship established by Kiorboe et al. (1985) of ingestion - food concentration for female A. tonsa, corrected by length-carbon regressions of Fig. 3: i = t.51 e - 15v/c (b) Specific growth rate (g, d-1) vs specific ingestion rate (i, d-1), both integrated over entire experimental period. Regression is: g=0.44i-0.081, r2=0.95

able and modified by "taste" (e.g. Huntley et al. 1986, cf. also the low clearances on Amphidinium carterae and Scripsiella far6ense in the present experiments), quality (e.g. Donaghay and Small 1979, Paffenh6fer and Van Sant 1985, Ayukai 1987), and species and size distribution (e.g. Poulet 1973, 1974, Richman et al. 1977, Huntley 1982) of food particles available as well as by the feeding prehistory of the copepod (e.g. Donaghay and Small 1979, Price and Paffenh6fer 1984). Paffenh6fer (i 984 a, b) compared feeding of Paracalanus parvus in uni- and multi-algal experiments. While the slopes of the log-log ingestion-weight regressions were similar between three algal sizes in uni-algal experiments - as in the present experiments (Fig. 2), ingestion of the largest alga increased faster with copepod weight than ingestion of smaller algae when offered in mixtures. However, ingestion and clearance on any particular algal species was always highest in uni-algal experiments where it probably delineates the maximum clearance capacity on that particular algal species/size. Thus, there is ample evidence that particle selection in copepods - although probably variable between species - is not determined solely by particle size as suggested for example, by Frost (1972, 1977) - but may be modified by the composition of available food. However,

the maxmimum clearance rate of a copepod is probably defined mainly by particle size. We suggest that the sizespectra obtained from unsaturated Acartia tonsa in uni-algal experiments with edible algae (i.e., omitting Amphidinium carterae and Scripsietla fargense) approximate this maximum potential. The lower size limit for particle capture in Acartia tonsa is to 2 to 4 #m and fairly constant during development. Similar or higher minimum particle sizes have been found in other species, e.g, 3 #m in Pseudodiaptomus marinus nauplii and copepodites (Uye and Kasahara 1983), 4 to 11 pm in Calanuspac~'cus nauplii and copepodites (Fernandez 1979), 1 to 4 #m in A. tonsa and Paracalanus parvus females (Bartram 1981), and 3 to 4 #In in Diaptomus sicilis females (Vanderploeg et al. 1984). In all cases efficiency of particle capture was very low near the lower end of the food size spectra. The size of planktonic bacteria and bacterivorous flagellates is < 1 #m and 3 to 7 #m, respectively (Fenchel 1982). Thus, neither copepod nauplii nor older stages constitute a particularly efficient link between the "microbial loop" and the "classical" food chain. All developmental stages of suspension feeding copepods are apparently adapted to feed on particles > 5 to 10:#m. For Acartia tonsa, optimum cell size increased with developmental stage. Similar trends have been found in Paracalanus parvus (Paffenh6fer 1984 a, b) and Pseudodiaptomus marinus (Uye and Kasahara 1983). Few authors have attempted to determine the upper size limit for particle capture, and most particle size spectra have been presented as monotonically increasing curve- or rectilinear relationships. However, the present data suggest that particle size spectra for A. tonsa are bell-shaped. The size spectra of selected stages of A. tonsa are normalized in Fig. 10 to facilitate comparison between stages and with other species. Clearance (ordinate) is expressed as the percentage of the maximum clearance rate recorded for a particular developmental stage, and algal size (ESD) is expressed relative to the linear dimension (prosome length) of the copepod. In spite of differences between spectra, there are striking similarities. They resemble log-normal distributions with optimum relative particle size (ESD/prosome length) varying by less than a factor of 3 (2 to 5%). Optimum particle size in the latest stages is poorly determined, since we had no (edible) particles between 14 and 70 #m, and the variation may, therefore, be even less. Similar size spectra calculated for Calanus pacificus (prosome length ~2.5 mm, Frost 1972) and Eudiaptomus silicus (~0.8 mm, Vanderploeg et al. 1984) fit this pattern. That is, over 1 to 2 orders of magnitude in length and more than 4 orders of magnitude in body mass, relative, optimum cell size is remarkably stable, both within copepod species (A. tonsa) and, as suggested by the limited data, also between copepod species. There may, however, be exceptions to this generalized pattern (e.g. subarctic Pacific Neocalanus sp., Frost et al. 1983). Average particle size distributions in the sea suggest that the biomas of particulate matter is approximately constant in equal, logarithmic size classes (e.g. Sheldon et al. 1972), although significant deviations from this average pattern

U. Berggreen et al.: Food size spectra and growth in Acartia tonsa

100

A. t o n s a

|

Growth and development

*~

/'vX. 7

9 N ,,,,,,

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80

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60

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-6 20 , E E 100 ~6 "~ 80

,

,

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ll ~ ~

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\

20

0 _A~',/I

r ,ill

t

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0.005 0.01 0.05 0.1 Relative particle size, ESD/prosome length

Fig. 10. Normalized food size spectra in (a) selected developmental stages of Acartia tonsa and (b) Calanus pacificus females (calculated from data in Frost 1977) and Diaptomous silicis females (data from

Vanderploeg et al. 1984). 0.5 , 0.4

/tS

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t

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349

I

I

500 1000 Concentration R. baltica, ~g C 1-1

I

1500

-0.2

Fig. 11. Acartia tonsa. Specific growth rate integrated over entire experimental period vs concentration of Rhodomonas baltica (filled

symbols from Fig. 5) compared to specific egg-production rates (open triangles) in A. tonsa females calculated from Kiorboe et al. (1985) may occur in any particular environment. If we accept that the food size spectra in all copepod stages can be approximated by log-normal distributions, the (relative) food availability for a particular stage in the average environment is determined only by the variance (width) of the distribution. With the exception of the smallest nauplii (NII to III), the width of the normalized particle size spectra for Acartia tonsa is strikingly similar between developmental stages. The implication is that food availability is similar for different developmental stages of A. tonsa in the average marine environment. The similarity to females of two other copepod species suggest that this may be a good approximation for other copepod species as well, although further information on size spectra during development in more species is needed to substantiate this generalization.

Isochronal development and exponential growth have previously been demonstrated for Acartia spp., including A. tonsa, at superabundant food concentrations, and it has been shown that growth and development both depend on temperature (e.g. Miller et al. 1977, Sekiguchi et al. 1980). The present data show that growth and developmental rates depend, in addition, on food availability and that growth is exponential and development isochronal also in unsaturated A. tonsa. Sekiguchi et al. (1980) demonstrated that maximum specific preadult growth in A. clausii hudsonica was similar to maximum specific egg-production in females. This has also been demonstrated for other species, Eurytemora herdrnani (McLaren and Corkett 1981), Pseudocalanus sp. (Corkett and McLaren 1978, Sekiguchi et al. 1980) and possibly Calanus pacificus (Runge 1984). In Fig. 11, specific egg production rates of A. tonsa females fed various concentrations of Rhodomonas baltica (data recalculated from Kiorboe et al. 1985) are compared to the specific pre-adult growth rates (from Fig. 5). As in A. clausii hudsonica growth and egg-production are similar at unlimited food availability but, moreover, the two rates depend on food concentration in the same manner - at least above maintenance concentration of food (egg production, unlike growth, cannot be negative). The dependence of ingestion rate on food concentration is also similar between female and juvenile A. tonsa (Fig. 9 a). It is, therefore, not surprising that the slope of the growth-ingestion relationship for pre-adults (0.44, Fig. 9b) is close to that found for females (0.36, Kiorboe et al. 1985). Thus, for A. tonsa, and probably other Acartidae as well, ingestion and growth proceed at the same foodand temperature-dependent rates, and utilization of ingested food is constant throughout the entire life cycle. Adult males are a possible exception to this, but nothing is known about sperm production rates. The relationships between ingestion and growth on the one hand and food concentration on the other are not universal, but depend on the size of the food algae. Larger-sized food algae lead to lower incipient limiting food concentration for Acartia tonsa (Jensen 1987) and other species (e.g. Calanus pacificus Frost 1972). Thus, comparison of the exact relationships between species (or studies) is not warranted, as in Runge (1984), unless food particle size/quality are comparable. However, the types of relationships may be compared. Numerous studies have considered the dependence of female egg-production on food concentration (e.g. Checkley 1980a, Uye 1981, Runge 1984, Kiorboe et al. 1985) and have generally found functional relationships similar to the present results. However, few studies have looked into food concentration effects on growth of juveniles. In some cases there was hardly any relationship to food concentration (e.g. Pseudocalanus elongatus, Paffenh6fer and Harris 1976, Temora longicornis, Harris and Paffenh6fer 1976), probably owing to the limited range of experimental food concentrations. However, Klein Breteler et al. (1982)found that juvenile growth in several neritic copepod species declined with

350 decreasing food concentration, and Vidal (1980) established relationships between stage-specific growth rates and food concentration in Pseudocalanus sp. and Calanus pacificus copepodites very similar to those found for A. tonsa here; i.e., growth increased hyperbolically with food concentration. However, in the species studied by Vidal (1980), growth was not exponential but tended to decline with age. McLaren (1986) suggested that this discrepancy between exponential growth in Acartia spp. and other species (e.g. Eurytemora herdmani, McLaren and Corkett 1981) and decreasing growth with size found by Vidal (1980) and others (e.g. Mullin and Brooks 1970 and Paffenh6fer 1976 in Rhincalanus nasutus and Calanus heIgolandicus, respectively) could be attributed to differences in amounts of stored lipid. Neither Acartia spp. nor E. herdmani seem to store substantial lipid (McLaren 1986, cf. also the constancy of the C:N-ratio and the independence of length-weight regression on food concentration, Fig. 3), whereas this is the case for Calanus spp. and others. When removing stored lipid McLaren (1986) found that "structural" growth in C. finmarchicus was indeed exponential, and suggested that this pattern may very well be true of calanoid copepods in general. Vidal (1980) found that the respiration rate of C. pac~'cus was proportional to the 0.82 power of its dry weight. However, when relating the respiration to structural weight, Harris (1983, manipulating Vidal's data) found that the two were directly proportional. Since growth and respiration rates are closely related (e.g. Kiorboe et al. 1985, 1987), this further supports McLaren's (1986) thesis. There is no simple relationship between growth and developmental rates for Acartia tonsa. Both depend on food availability, but the sigmoid relationship between the two (Fig. 7) suggests that growth continues to increase above the food concentration that supports the highest developmental rate. A similar pattern was found by Vidal (1980b) for Pseudoealanus sp. and Calanus pacificus. The consequence of this is that weight at stage increases with food concentration and that growth rate cannot easily be predicted from moulting rate (or vice versa). Hence, moulting is not determined solely by growth rate or size. Miller et al. (1977) reached a similar conclusion comparing the dependency of growth and developmental rates on temperature in Acartidae. Determination of copepod production in the field There are several approaches to the estimation of secondary production in situ. One group of methods considers the development of distinct cohorts and estimates the production from changes in abundance and weights of individual age (stage) classes over time (see review by Rigler and Downing 1984). This approach is very often not applicable to planktonic copepods, since populations are often continuously reproducing and distinct cohorts, therefore, cannot be separated. Also, patchiness and advection processes make sampling of the same population/cohort over time difficult. One additional drawback of this approach is that it yields production estimates integraded over fairly large areas and time periods.

U. Berggreen et al. : Food size spectra and growth in Acartia tonsa Another group of methods, collectively known as the growth rate method, takes an approach that potentially makes production estimates time- and site-specific, thus allowing analysis of temporal and horizontal variation in productivity. In principle, growth rates are measured for individual stage/age classes and multiplied with the biomass of that particular stage. Production rate of the entire population is obtained by summing the product of stage-specific growth rates and biomasses over all stages. This approach does not require knowledge of mortality rates as erroneously assumed by many workers (see Kimmerer 1987). In its simplest form, growth rates are derived from temperature-developmental rate relationships found in excess fed copepods in the laboratory, in situ temperature, length at stage and length-weight regressions (e.g. Durbin and Durbin, 1981, McLaren and Corkett 1981, Uye et al. 1983). There is accumulating evidence, however, that copepods are often limited by food availability in the sea (e.g. Dagg 1978, Checkley 1980b, Durbin et al. 1983, Lampert (ed.) 1985). This approach, therefore, tends to overestimate production and renders analyses of relations between primary and secondary production meaningless. Landry (1978) solved this problem by estimating stage-specific growth rates from cohort analysis, with the consequence, however, that the production estimates were less site- and timespecific. The most recent advance of the growth rate approach, originally proposed by Tranter (1976), is to estimate stage-specific growth rates by shipboard incubation experiments. Individual stages are sorted out (Burkhill and Kendall 1982, Fransz and Diel 1985) or artificial cohorts are created by size fractionation (Kimmerer and McKinnon 1987), and incubated in in situ water for i to 5 d for determination of developmental rates. Since the relationship between growth and developmental rates is not simple (cf. Fig. 7) and because weight at stage varies with food availability (Fig. 8) and temperature (e.g. Vidal 1980), this approach requires site- and time-specific weight at stage information. Although this approach is conceptually appealing, the number of replicates required to keep confidence limits acceptably narrow is high (see Kimmerer 1983 and Miller et al. 1984) and thus the method is very laborious. Consequently, the number of sites, times and species covered by this method is limited in practice. Also, Miller et al. (1984) criticized the approach, because they found diurnal variation and pronounced moulting bursts in incubated copepods. An alternative and much less labour-intensive approach was adopted by Kiorboe and Johansen (1986). They measured egg-production rates in several copepod species, either by incubation experiments or by the egg-ratio method, and on the assumption that specific female egg production was representative of specific growth rates in other stages, they computed copepod production. They were able to cover 20 stations within 2 x 24 h using this approach, which allowed a fine-scale analysis of horizontal variations in copepod productivity. Our experimental results lend some support to this approach. Growth-food relationships are similar for all stages ofAcartia tonsa. Moreover, we have argued that food avail-

U. Berggreen et al. : Food size spectra and growth in Acartia tonsa ability, in spite of differences in food size spectra, is similar for most stages in the avarage environment. Given these assumptions, specific female egg-production in A. tonsa is representative of the specific growth rate of all stages (except N I and males), and, hence, for population turnover rate (P/B). The somewhat smaller width of the food size spectra in small nauplii, as well as deviations from the average food particle size distribution and from the potential food size spectra due to selection/adaptation in any particular situation, may of course violate the assumptions. However, three (of four) of the above-mentioned studies using the growth rate approach actually found that in situ growth rate was constant (Landry 1978, Kimmerer and M c K i n n o n 1987) or almost constant (Fransz and Diel 1985). In addition, the two former studies found that in situ growth rate was approximated by female fecundity. Thus, field data collected at various seasons and localities support the assumptions. Another argument in favour of the egg-production approach is that the biomass distribution of continuously reproducing copepods in the sea is often in favour of older stages, particularly adults. Thus, data collected during October 1985 in the N o r t h Sea on Acartia spp. (Kiorboe unpublished) revealed that females made up 35 to 45% of the Acartia spp. biomass, whereas N I - I I I constituted only 3 to 5. Similar weight-stage distributions were found for other species. Therefore, adult females contribute most to production, and an overestimation of the production of NI-III, for example, will only slightly influence the population estimate. Thus, the egg-production approach seems to be fairly robust to even rather large diviations from the assumptions. Even though production estimates by this approach may at times be slightly biased, it has the major advantage of allowing a fine-scale resolution of horizontal and temporal variation with a realistic effort. The extent to which the egg-production approach is applicable to other species awaits further testing. However, the approach is restricted to species or populations that contain reproducing females throughout the productive season (e.g. most neritic species in temperate - tropical waters). Secondly, some species possess resting stages at times; e.g. lipid-rich CV in Calanus spp. These must be considered separately. Finally, not all species exhibit stage-independent specific growth rates, but as mentioned avove and suggested by McLaren (1986), this m a y be due to deposition of lipids. Most authors express copepod body size and production in untis of dry weight, ash-free dry weight or carbon. If "structural" growth is indeed exponential (except for resting stages), nitrogen may be a more useful unit, since protein presumably quantifies structure better than carbon or dry weight. Nitrogen is also often considered the limiting nutrient for both primary (e.g. Smetacek and Pollehne 1986) and secondary (e.g. Checkley 1985) production in the sea, rendering this unit even more relevant in studies of copepod production in the marine environment. Acknowledgements. Thanks are due to E. Bagge for doing the CHN-

analyses, and to B. Frost, J. Roff and J. Runge for critically reading the manuscript.

351 Literature cited Ayukai, T. (1987). Discriminate feeding of the calanoid copepod Acartia clausi in mixtures of phytoplankton and inert particles. Mar. Biol. 94:579-587 Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A., Thingstad, F. (1983). The ecological role of water-column microbes in the seas. Mar. Ecol. Prog. Ser. 10:257-263 Bartram, W. C. (1981). Experimental development of a model for the feeding of neritic copepods on phytoplankton. J. Plankt. Res. 3:25-51 Boyd, C. M. (1985). Is secondary production in the Gulf of Maine limited by the availability of food? Arch. Hydrobiol. Beih. 21: 57-65 Burkill, P. H., Kendall, T. F. (1982). Production of the copepod Eurytemora affinis in the Bristol Channel. Mar. Ecol. Prog Ser. 7:21-31 Checkley, D. M. Jr. (1980 a). The egg production of a marine planktonic copepod in relations to its food supply: laboratory studies. Limnol. Ocenaogr. 25:420-446 Checkley, D. M. Jr. (1980 b). Food limitation of egg production by a marine, planktonic copepod in the sea off southern California. Limnol. Oceanogr. 25:991-998 Checkley, D. M. Jr. (1985). Nitrogen limitation of zooplankton production and its effect on the marine nitrogen cycle. Arch. Hydrobiol. Beih. 21:103-113 Corkett, C. J., McLaren, I. A. (1978). The biology of Pseudocalanus. Adv. mar. Biol. 15 Dagg, M. (1978). Estimated, in situ, rates of egg production for the copepod Centropages typicus (Kroyer) in the New York Bight. J. exp. mar. Biol. Ecol. 34:183-196 Donaghay, P. L., Small, L. F. (1979). Food selection capabilities of the estuarine copepod Acartia elausii. Mar. Biol. 52:137-146 Durbin, A. G., Durbin, E. G. (1981). Standing stock and estimated production rates of phytoplankton and zooplankton in Narragansett Bay, Rhode Island. Estuaries 4:24-41 Durbin, E. G., Durbin, A. G., Smayda, T. J., Verity, P. G. (1983). Food limitation of production by adult Acartia tonsa in Narragansett Bay, Rhode Island. Limnol. Oceanogr. 28:1199-1213 Fenchel, T. (1982). Ecology of heterotrophic microflagellates. I. Some important forms and their functional morphology. Mar. Ecol. Prog. Set. 8:211-223 Fernandez, F. (1979). Nutrition studies in the nauplius larvae of Calanus pacificus (Copepoda: Calanoidea). Mar. Biol. 53: 131-147 Fransz, H. G., Die1, S. (1985). Secondary production of Calanus finmarchicus (Copepoda: Calanoidea) in a transitional system of the Fladen Ground area (northern North Sea) during the spring of 1983. In: Proc. 14th Europ. mar. biol. Symp. p. 123-133. [Gibbs, P. E. (ed.) Cambridge University Press, Cambridge] Frost, B. W. (i 972). Effects of size and concentration of food particles on the feeding behaviour of the marine planktonic copepod Calanus pacificus. Limnol. Oceanogr. 17:805-815 Frost, B. W. (1977). Feeding behaviour of Calanus pacificus in mixtures of food particles. Limnol. Oceanogr. 22:472-491 Frost, B. W. (1985). Food limitation of the planktonic marine copepods Calanus Pacificus and Pseudocalanus sp. in a temperate fjord. Arch. Hydrobiol. Beih. 21:1-13 Frost, B. W., Landry, M. R., Hasset, R. P. (1983). Feeding behaviour of large calanoid copepods Neocalanus cristatus and N. plumchrus from subarctic Pacific Ocean. Deep-sea Res. 30A: 1-13 Harris, J. R. W. (1983). The development and growth of Calanus copepodites. Limnol. Oceanogr. 28:142-147 Harris, R. P., Paffenh6fer, G.-A. (1976). Feeding, growth and reproduction of the marine planktonic copepod Temora long# cornis Mfiller. J. mar. biol. Ass. U.K. 56:675-690 Huntley, M. (1982). Yellow water in La Jolla Bay, California, July, 1980. II. Suppression of zooplankton grazing. J. exp. mar. Biol. Ecol. 63:81-91

352 Huntley, M., Sykes, P., Rohan, S., Marin, V. (1986). Chemicallymediated rejection of dinoflagellate prey by the copepods Calanus pacificus and Paracalanus parvus: mechanisms, occurrence and significance. Mar. Ecol. Prog. Set. 28:105-120 Jensen, J. (1987). Fodeindtagelse, ~egproduktion og fedtsyresammensaetning hos den marine planktoniske copepod Aeartia tonsa. Unpublished Masters thesis, Odense University, Odense Kimmerer, W. J. (1983). Direct measurement of the production: biomass ratio of the subtropical calanoid copepod Aeroca/amts inermis. J. Plankt. Res. 5 : 1 - 1 4 Kimmerer, W. J. (1987). The theory of secondary production calculations for continuously reproducing populations. Limnol. Oceanogr. 32:1-13 Kimmerer, W. J., McKinnon, A. D. (1987). Growth, mortality, and secondary production of the copepod Acartia tranteri in Westernport Bay, Australia. Limnol. Oceanogr. 32:14-28 Kiorboe, T., Johansen, K. (1986). Studies of a larval herring (Clupea harengus L.) patch in the Buchan area. IV. Zooplankton distribution and productivity in relation to hydrographic features. Dana 6:37-51 Kiorboe, T., Munk, P., Richardson, K. (1987). Respiration and growth of larval herring Clupea harengus: relation between specific dynamic action and growth efficiency. Mar. Ecol. Prog. Set. 40:1-10 Kiorboe, T., Mohlenberg, F., Hamburger, K. (1985). Bioenergetics of the planktonic copepod Aeartia tonsa: relation between feeding, egg production and respiration, and composition of specific dynamic action9 Mar. Ecol. Prog. Ser. 26:85-97 Klein Breteler, W. C. M., Fransz, H. G., Gonzales, S. R. (1982). Growth and development of four calanoid copepod species under experimental and natural conditions. Neth. J. Sea Res. 16:195-207 9Lampert, W. (ed.) (1985). Food limitation and the structure of zooplankton communities. Proceedings of an international symposium held at P16n, W. Germany, July 9-13, 1984. Arch. HydrobioI. Supp121, E. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart Landry, M. R. (1978). Population dynamics and production of a planktonic marine copepod, Aeartia elausi, in a small temperate lagoon on San Juan Island, Washington. Int. Rev. Ges. Hydrobiol. 63:77-119 Legendre, L. (1981)9 Hydrodynamic control of marine phytoplankton production: The paradox of stability. In: Niboul, J. C. (ed.) Ecohydrodynamics. Elsevier, Amsterdam, p. 191-207 McLaren, I. A. (1986). Is "structural" growth of Calanus potentially exponential. Limnol. Oceanogr. 31:1342-1346 McLaren, I. A., Corkett, C. J. (1981). Temperature-dependent growth and production by a marine copepod. Can. J. Fish. aquat. Sci. 38:77-83 Miller, C. B., Huntley, M. E., Brooks, E. R. (1984). Post-collection molting rates of planktonic, marine copepods: Measurement, application, problems. Limnol. Oceanogr. 29:1274-1289 Miller, C. B., Johnson, J. K., Heinle, D. R. (1977). Growth rules in the marine copepod genus Acartia. Limnol. Ocenaogr. 22: 326-335 Mullin, M. (1980). Interactions between marine zooplankton and suspended particles. In: Kavanaugh, M. C., Leckie, J. (eds.) Particulates in water. Adv. Chem. Ser. no 189, American Chemical Society, Washington D. C., p. 233-247 Mullin, M. M., Brooks, E. R. (1970). Growth and metabolism of two planktonic, marine copepods as influenced by temperature and type of food. In: Steele, J. H. (ed.) Marine Food chains. University of California Press, Berkeley, p. 74-95 Paffenh/Sfer, G.-A. (1976). Feeding, growth, and food conversion of the marine planktonic copepod Calanus helgolandicus. Limnol. Oceanogr. 21:39-50 Paffenh6fer, G.-A. (1984a). Food ingestion by the marine planktonic copepod Paracalanus in relation to abundance and size distribution of food. Mar. Biol. 80:323-333

U. Berggreen et al.: Food size spectra and growth in Acartia tonsa Paffenh6fer, G.-A. (1984b). Does Paracalanus feed with a leaky sieve? Limnol. Oceanogr. 29:155-160 Paffenh6fer, G.-A., Harris, R. P. (1976). Feeding, growth and reproduction of the marine planktonic copepod Pseudocalanus elongatus Boeck. J. mar. biol. Ass. U.K. 50:327-344 Paffenhtfer, G.-A., Van Sant, K. B. (1985). The feeding response of a marine planktonic eopepod to quantitiy and quality of particles. Mar. Ecol. Prog. Ser. 27:55-65 Peterson, W. T. (1986). Development, growth and survivorship of the copepod Calanus marshallae in the laboratory. Mar. Ecol. Prog. Ser. 29:61-72 Poulet, S. A. (1973). Grazing of Pseudocalanus minutus on naturally occurring particulate matter. Limnol. Oceanogr. 18:564-573 Poulet, S. A. (1974). Seasonal grazing of Pseudocalanus minutus on particles. Mar. Biol. 25:109-123 Price, H. J., Paffenhtfer, G.-A. (1984). Effects of food experience in the copepod Eucalanus pileatus: a cinematographic study. Mar. Biol. 84:35-40 Richman, S., Heinle, D. R., Huff, R. (1977). Grazing by adult estuarine calanoid copepods of the Chesapeake Bay. Mar. Biol. 42:69-84 Rigler, F. H., Downing, J. A. (1984). The calculation of secondary productivity. In: Downing, J. A., Rigler, F. H. (eds.) Manual on methods for the assessment of secondary production in fresh waters, 2nd edn, Blackwell Scientific Publications, Oxford, p. 19-58 Runge, J. A. (1984). Egg production of the marine, planktonic copepod Calanus paeifieus Brodsley: Laboratory observations. J. exp. mar. Biol. Ecol. 74:53-66 Runge, J. A. (1985). Egg production rates of Calanusfinmarehieus in the sea off Nova Scotia. Arch. Hydrobiol. Beih. 21:33-40 Sekiguchi, H., McLaren, I. A., Corkett, C. J. (1980). Relationship between growth rate and egg production in the copepod Aeartia clausi hudsonica. Mar. Biol. 58:133-138 Sheldon, R. W., Prakash, A., Sutcliffe, W. H., Jr. (1972). The size distribution of particles in the ocean. Limnol. Oceanogr. 17: 327-340 Smetacek, V., Pollehne, F. (1986). Nutrient cycling in pelagic systems: a reappraisal of the conceptual framework. Ophelia 26: 401-428 Stottrup, J. G., Richardson, K., Kirkegaard, E., Pihl, N. J. (1986). The cultivation of Acartia tonsa Dana for use as a live food source for marine fish larvae. Aquaculture 52:87-96 Tranter, D. J. (1976). Herbivore production. In: Cushing, D. H., Walsh, J. J. (eds.) The ecology of the seas. Blackwell Scientific Publications, Oxford, p. 186-224 Uye, S.-I. (1981). Fecundity studies of neritic calanoid copepods Acartia elausi Giesbrecht and A. steueri smirnov: a simple empirical model of daily egg production. J. exp. mar. Biol. Ecol. 50:255-271 Uye, S.-I., Iwai, Y., Kasahara, S. (1983). Growth and production of the inshore marine copepod Pseododiaptomus marinus in the central part of the Inland Sea of Japan. Mar. Biol. 73:91-98 Uye, S.-I., Kasahara, S. (1983). Grazing of various developmental stages of Pseudodiaptomus marinus (Copepoda: Calanoida) on naturally occurring particles. Bull. Plankt. Soc. Japan 30: 147-158 Vanderploeg, H. A., Scaria, D., Liebig, J. R. (1984). Feeding rate of Diaptomus silicis and its relation to selectivity and effective food concentration in algal mixtures and in Lake Michigan. J. Plankt. Res. 6:919-941 Vidal, J. (1980). Physioecology of zooplankton. I. Effects of phytoplankton concentration, temperature, and body size on the growth rate of Calanus paeifieus and Pseudoealanus sp. Mar. Biol. 56:111 - 134 Date of final manuscript acceptance: June 8, 1988. Communicated by T. Fenchel, Helsingor