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
1.8_+ 0.3
10.1_ 0.2
25.9-t- 0.5
32.1-+ 0.7
47.4_+ 1.9
107_+ 0.7
267_+14
801 +_11
7 026_+93
-
N cell-,
(Pg)
C:N
n
0.3+ 0.0
1.6-+ 0.1
3.0_+ 0.1
4.0_+ 0.2
11.6_+ 0.3
13.5_+ 0.5
35.7_+ 1.5
98.1 _+ 1.8
919-t-53
-
6.2_+0.1
6.4_+0.2
8.7-+0.2
7.9-+0.3
4.1 _+0.0
7.9_+0.4
7.4+__1.0
8.2 _+0.2
7.7+_0.3
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
Average initial concentration
#g C 1-1
A
B
0
0
86 __19
93+_23
123 _ 18
129_+22
222 -+ 19
228-+23
407 -+ 32
443-+35
812 ___ 96
878_+105
Average reduction d - 1 %
A
B
0
0
2_+20
18-+18
17+14
21-+17
36+ 9
25___17
41-+15
27-+14
23_+12
18_+ 7
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-
1,0
Nil, NIII
Nil, NIII
Nil, NIII
/-\
T
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\
~" 0.1
1:3
r-
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4- '--
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Cl, Oil
Cl, CII
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•
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t
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100
Equivalent spherical diameter, ~Jm
I
I
L I
10
L
U. Berggreen et al.: Food size spectra and growth in Acartia tonsa
30
Is 9
Pay
10
.../
o9
9o
/
23
T23
1
.c
E
345
./"
0.1
r
L
n Jnl
0.01
n
I
I n~l
0.1
e
I[
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4
0,01
0.1
1
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100
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oo,~/
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c-
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Amp
/..-
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0.01
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~
J,,I
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0.1
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,,
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./"
Tha
/J
9
10
-r
23
7
23 1
.=_
100 - -
/
0.1
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0.1
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0.01
0.1
I II
1
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8
Gym
e9
9
e 9ee.~
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100 - -
Scri
n
i~JI
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6
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Body weight, ~g C
gressions have exponents not significantly different from
unity. The only exceptions are I s o c h r y s i s g a l b a n a and Thall a s i o s i r a f l u v i a t i l i s with exponents slightly and significantly
higher, respectively.
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
I I E
8
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--
1000 m
7 0.5
Copepodites
Nauplii
6
7"
,/
300
100
rn
50
~176
.../'
1000
9
500
9149
/-
/!
300
20
!
i
o.oI .~I
"
I I
t
12t
I
I
I
I I
I I
I
I I I
I
500
1000
1500
ConcentrationR. baltica, [Jg C 1-1
Fig. 5. Acartia tonsa. Specific growth rate ( + SD) over entire developmental period (Fig. 4, Table 4) as a function of concentration of
Rhodomonas baltica. Graph fitted by eye
~176
30
0.2
Olp/
/
/
.2
Jc
o
"/v
2000
j 7.
200
s 0.3
3000
/
O
"~ 0.4
J=
/
,r
./
5000
500
/
200
Table 4. Acartia tonsa. Specific growth rate. Regressions of body
i l l
150
I
300
I
I
500
300
Pros9
I
II1[
1000
500
I
=
I
2000
length, lum
Fig. 3. Acart& tonsa. Relations between body weight (W, ng C) and
pros 9 length (L, #m) in nauplii and copepodites. Only samples
totally dominated by either nauplii or copepodites are included.
Regressions are: Nauplii: W=3.18 x 10 -6 L T M @2=0.91); copepodites: W = 1.11 x 10 .5 L 2'92 (rZ=0.98). C:N-ratio was independent of food level and developmental stage and averaged (X + 95%
eL) 4.1 +0.1
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
W9
#g C
0
1
2
3
4
5
6
0.028
0.029
0.019
0.023
0.017
0.017
0.013
g _ SD
(d- 1)
- 0.13 _+0.09
0.01 + 0.01
0.15_+0.01
0.26 +_0.02
0.37_+0.01
0.414-0.01
0.45 _+0.02
r2
n
0.61
0.49
0.99
0.98
0.99
1.00
0.99
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
o 1
D3
E
u~ 0.5
m
baltica.
0.1
z,2
oJ
0.05
0.01
Stage duration
2
4
6
8
10
Time, d
12
14
16
Fig. 4. Acartia tonsa. Weight increment over time at seven different
concentrations of Rhodomonas baltica. Samples with mature stages
are not included, since matured individuals do not grow. Values
refer to food-level (see Table 2). Parameters of regression analyses
are given in Table 4. Symbols: food level 0 (A), 1 (v), 2 (A), 3 (m),
4 (O), 5 (O), 6 (| Weight at start of experiment: 9
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
a)
cei
C5
C4
2.5 - -
-9
b)
5
C3
C2
//
& cl
9
_ _ - - - - . - - 9 C5
2.0
o
_
03 N6
N5
N4
N3
N2
N1
9~"
--
en
I
I
I
I
50
100
150
200
I
I
I
I
I
250
300
350
400
450
6 (see Table 2). Time required to reach a particular stage is estimated from 50% fractile. Developmental rate at Food level 5 and
6 were inseparable, and only data for Level 6 are shown. Open and
filled symbols are used only to facilitate visual separation of food
levels. Parameters of regression analyses are shown in Table 5
9
9/ ~
9~
0.1
v
- - e C 3 ._o
~
9
.-~
9
oN5
o...~ 9 _..__.__--
+
"'~- 9
0
,/
,/
./
'9
9
t.O
,,/./'
oN4
0.05
0.01
/-/
~ 1,5
- - " C 2 y=
9 ~ 1 4 9
9~
Time, h
Fig. 6. Acartia tonsa. Developmental rate at Food level 2, 3, 4 and
Q.,~.
9
Jc:
+33
-~ 0.5
~
--oN2
pl~tl~ppl~lnnl
500
1000
1500
Concentration R. baltica, [Jg C 1-1
0.5
I~ i i p l l l l l l l
N1
C1
Stage
Fig. 8. Aeartia tonsa. (a) weight at stage as a function of food
concentration. (b) weight ratio at Food level 6 and 3 as a function
of developmental stage
1.0
~
23
-
m 0.6--
/
/
oo
9
the linear relationship to body mass found above (cf. Fig. 2,
Table 3). Specific ingestion rates (i) were therefore constant
throughout development at each food concentration and
were estimated as:
8~
0.2
I
-;
,-J~"
-0.2
I
0.2
1
1
1
,
0.4
1
Specific growth rate, d -1
Fig. 7. Aeartia tonsa. Developmental rate as a function of specific
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
0.004
0.028
0.037
0.039
0.040
263
35.8
26.8
25.7
25.2
0.94
0.99
0.99
0.99
0.99
T
i = T t~-"=1It~ Wt'
where T = duration of the experiment in days; W~ and I t
=estimates o f body mass and ingestion (both in terms o f
carbon) on Day t, respectively. Specific ingestion rate varied
with food concentration in a manner similar to the growth
rate (Fig. 9 a), and specific growth rate increased linearly
with specific ingestion rate (Fig. 9 b). The slope of this regression (dg/di=0.44) is an estimate of the efficiency by
which ingested carbon in excess of maintenance requirements is converted into body carbon.
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
&
1.0
g
O
0.5
O3
-/
/9
0o
I
I
I
500
1000
1500
Concentration R. baltica, ~g C I-~
b)
9
0.4
Jm
0.3
99
0
o~ 0.2
.o
o.
O3
0.1
9 J
/0.2
/
-0.1
0.4
0.6
0.8
1.0
I
1.2
I
1.4
Specific ingestion rate, d -1
-0.2 -
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 ,,,,,,
9 NIV
80
/ / ~#~-,
//#
1/ l
ANVl
o Oil
60
4O
/f" #o/
-6 20 ,
E
E
100
~6
"~ 80
,
,
I i
ll ~ ~
C. pacificusC) l - - i 9
D. silicis
~/
~
9
a_ 60
:/
40
\
20
0 _A~',/I
r ,ill
t
q t I I llll
I
I
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
x= 0,3
~0.2
.s
t
& o.1
09
0.0
-0.1.
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
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Date of final manuscript acceptance: June 8, 1988.
Communicated by T. Fenchel, Helsingor