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Filtration rate of zooplankton community during spring bloom in Akkeshi Bay
J. exp. ~nc(r. Biul. EC&., 1975, Vol. 19, pp. 145-144; IC*North-Ho~~nd
Publishing Company
FILTRATlON RATE OF ZOOPLANKTON COMMUNITY DURING SPRING BLOOM IN AKKESHI BAY ’ SATORU TAGUCHI’ Faculty qf‘ Fisheries,
and MITSUO FUKUCHI
Hokkaido Unicersit_r, Hakodnte, Jopun
Abstract: The filtration
rate of a natural zooplankton community at the time of the spring bloom in Akkeshi Bay was estimated using changes in concentration of chlorophyll a, of particulate carbon, and changes in cell numbers. The size range of phytoplankton cells utilized indicated that the maximum length of chain consumed depended upon the size-range of the zooplankton community. Evidence for size-selection of food by animals is presented. The possible explanation of relation between the filtration efficiency - the ratio of respiration rate to the product of filtration rate and dissolved oxygen - and the quantity and quality of food is discussed. When there is a wide range of phytoplankton sizes or a small amount of phytoplankton, the filtration efficiency decreases.
Most estimations of filtration rates have been made for single species of zooplankton in an experimental container. In the natural marine environment, however, the community structure of zooplankton is so complicated that few have tried to determine the relationships between filter-feeders and their food. In the freshwater environment, Richman (1958), Burns & Rigler (1967), Ghwicz (t969), and Ivanova (1970) have tried to establish the relationship between the filtration rate of zooplankton community and size of food. In the present study we report observations on the filtration rate and selectivity by a natural zooplankton community cles during the spring bloom.
caught with net as it fed on naturally
occurring
parti-
MATERIALS AND METHODS
Five experiments
were carried
out on the zooplankton
community
in Akkeshi
Bay
(Fig. I) on 23rd February, 23rd March, and 21st April, 1971 at the central station (42”58.5’N: 143”49.4’E). Experimental animals were caught with a conical plankton net (30 cm in mouth diameter, 100 cm Tong, 0.35 mm mesh apertures) towed for 10 min about noon. The animals were acclimatized in a IO-1 bucket in the dark for z 8 h. For each experiment, surface water was sampled with a plastic bucket and passed through 0.35 mm mesh net to remove large planktonic animals. All of the experiments ’ Contribution from JIBP-PM. ’ Present address: Fisheries & Marine Service, Marine Ecology Laboratory, Oceanography, Dartmouth, Nova Scotia, Canada. 145
Bedford Institute of
146
SATORU
TAGUCHI
AND
MITSUO
FUKUCHI
were begun at 20.00 h and lasted for 24 h. The experimental than the in situ temperature
at which the animals
temperatures
were collected
were higher
by 4.30 “-7.15 ‘C
(Table I), but varied less than +0.5 “C during the experiments. In the first experiment 25 healthy individual Calanuspacijhs were transferred to 2-l dark bottles filled with net (0.35 mm mesh) moved and 15 animals
filtered
surface
water.
After incubation,
were frozen for chemical
analysis
the animals
were re-
and 10 were fixed in formalin
43=‘N
43ON
I
I
I
144O5O’E Fig. 1. Map
of location
of experimental
station.
for identification of stage. Weight was measured after the frozen samples were dried at 60 “C for 1 h. The organic carbon and nitrogen of animals were measured with a Hitachi CHN Analyser. In the Experiments 2 to 5, the same procedure was followed except that mixed populations of zooplankton rather than a single species were used. Before and after incubation, subsamples of water, excluding faecal pellets, were taken to determine oxygen, chlorophyll, phytoplankton cells, total seston carbon, and nutrients.
HLTRATION
RATE OF ZOOPLANKTBN
DURING
SPRING BLOOM
147
tninutus
Kr0yer
Thompson
ptrciJiw.7 Brodski
Crdtnus
Total
Uitlruno
sintilis
Ciaus
Tt,rfrrtzusdisc~tt{d~~tiis Thompson
pctcijfcn
Brodski
he~dftz~t~ii
Willey
Metriditr
Euryte,norri
Acctrticr turmdu
Acurtiu lungirewzif (Lillijeborg)
Pseudoculunus
_ -_ _.-._-. ..-l__-_l-.
Species
& Scott
& Scott
II--.--
-..
Species composition
V IV
Female Malt
Copepodid
Ii
Copepodid V Copepodid IV Copepodid I1I
Female Copepodid Copepodid
Female Male Copepodid
Female Male
Female Male Copepodid
Female Male Copepodid
-..-_. ._. ._
Stage
of the rooplankton
25
(4) 113) (8)
_. _
_ -.
_
._
-
1
591
I
I
^...
5
523
I
^_
372
I
__
162
13 ^.
-
-.
-
-
.-
__
-. i_
_.
5
13 5
96 21 2
12 2 2
3
2
__
-_
2
1
IO
_ -
123 38 4
160 4 22
1
2
“,.
I 3 4
._
-
2 ._
85 21
375 I 14
4
_ ~.-...__--- .___ ”
number
__~__.
3
3 2
_
Experiment
1
.-
50 8
490 9 22
2
incubated during the experiments.
E
FILTRATION
RATE
The rate of respiration experimental determined excretion
OF
ZOOPLA~KTON
was obtained
and control by the Winkler
rate was obtained
bottles method
DURING
from the difference
after 24 h incubation. as described
SPRlNG
in oxygen concentr~~tion Oxygen
by Strickland
from the difference
between
I49
BLOOM
concentrations
& Parsons
ammonia-N
in
were
(1968). The concentration
and phosphate-phosphorus concentration in experimental and control suspensions after incubation. Ammonia-nitrogen was determined by the method of Solorzano (1969), and phosphate-phosphorus by the one-solution method of Murphy & Riley (see Strickland &Parsons, 1968). The filtration rate was obtained from the calculated rates of decrease of three different values: chlorophyll a concentration, phytoplankton cell numbers, and particulate organic carbon concent~tion. chlorophyll a concentration was measured by the method of Saijo & Nishizawa (1969). Phytoplankton ceils were counted under an inverted microscope. Size was measured for each phytoplankton ceil; in the case of chain-forming species, the maximum and minimum size of the chain was measured. Particulate organic carbon was determined by the method of Nakajima (1969). BODY STAGE COPEPODITE
DRY
Fig. 2. Size distribution
BODY
WEIGHT
of CWanw
!N
pncificus
m LEIN%H V IV
1.95 .-_2.45 190
ug
used for Experiment
I.
At the same station, vertical observations of temperature, ammonia-N, phosphate-P, chlorophyll a, and seston carbon, down to 20 m, were made. The standing stock of zooplankton community was obtained from a vertical tow with a 0.35-mm mesh net. A series of in situ primary production experiments was also carried out at this station by the method of Strickland & Parsons (1968).
150
SATORU
TAGUCHI
AND
MITSUO
FUKUCH1
RESULTS BODY SIZE,
WEIGHT
AND SPECIES COMPOSITION
Species and stage composition of zooplankton community is shown for each experiment in Table II. In Experiment 1,25 stage III, IV and V, C,paci$clrs were selected. Their weight distribution and length are shown in Fig. 2. In Experiment I, C. pacijicus with a body length of % 1.90 mm was assumed to be dominant. In Experiment 2, carried out in February, P.~eadoc~i~us rnj~a~~swith a body length of 0.70-f .25 mm was over 87.5 % of total number while Aearria Zo~g~re7nis,0.75-0.95 mm long, constituted only 9.7 % of the total number (Table III). In Experiment 3 in March the percentage of the two species changed to 75.704 for Pseudoculanus minutus (0.85-1.05 mm iong)and20.2~~ for Acartia ~o~giremjs~O.80-1.00 mm Iong). As the average body length of the two species increased from Experiment 2 to Experimelit 3, the average dry weight increased from 13.5 pg to 24.6 /lg. In Experiment 4, Pseuducalanus minurus (0.80-I .05 mm long) and Acartia longiremis (0.80-1.00 mm long) made up 50.0 ‘;i and 44.3 O,;, respectively of the total. The portion of smaller-sized A. Iongiremis more than doubled and consequently the average body dry weight decreased by one-half. In Experiment 5, A. lo~zgire~~is(0 X0-1.05 mm long) was 73.4 %, A. tumidu (0.95-1.35 mm long) 13.5 “/6,and Pseadocalun~~srn~n~~~.~ (O.SO-1.15 mm long) 9.8 :I:;of the total. In addition to the small-sized Acarfiu Iongjremjs, larger A. rumida occupied over lo:, of total number, which might have caused the increase of average body dry weight to 14.7 ,WJ. CHEMICAL
COMPOSITION
Chemical analyses for all experiments are summarized in Table IV. Average carbon and nitrogen content per body dry weight of CalanuspaciJicus was 52.6 “/, and 9.64 ‘;,;, respectively. These values are similar to 48.0 to 58.4 % for carbon content and 7.8 to 12.7 “/:,for nitrogen content for C. pacz@cus, collected in the northern North Pacific Ocean by Omori (1969). The carbon and nitrogen content varied with stage but for C. ~~~~~ci~~greater than 700 pg dry weight, carbon and nitrogen were constant at ?Z 54 ‘?Gand 9.12 %, respectively. For mixed populations, i.e., Experiments 2, 3, 4, and 5, carbon and nitrogen contents fell within a narrow range: 42.6-46.2 Y/i carbon and 8.25~8.50% nitrogen. Average dry weight per animal ranged from 1I .O-24.6 pg and the maximum dry weight was observed in March when primary production was at a peak. RESPIRATION
AND EXCRETION
RATES
Data from the respiration and excretion experiments are summarized in Table V. The respiration rate increased during the dev~iopment of the spring bloom from 1.92 to 4.20 jug-at. oxygen. (mg body dry wt)-‘. day-’ in February and to 9.79 pg-at. oxygen. (mg body dry wt)-‘. day-’ in April.
minutus
longiremis
similis
pacijica
herdmanii
3
tumida
tumida
Acartia
herdmanii
Total
~~erdl~laflii
tumida
Eurytemora
Acartia
It
I 30 I I 33
I 10
langiremis
Pse~o~alan~
Acartia
72
i~l~nlitas
20 48 3
15 25
L
83
1
45 37
133
43
I
22 20
70
4
19
110
40
2
2
1 2
61 6
fotai Experiment 5
Temora discaudatus
Oithona similis
Eurytemora
Calanus pacificus
longiremis
Acartia
Pseudacaianus
Total Experiment 4
ninutus
herdmanii
Oithona similis
Eurytemora
Calanus pacijicus
Acartia
minutus
longiremis
Acartia
Pseudocaianus
experiment
Total
Temora discaudatus
Oithora
Metridia
Eurytemora
Calanus pacijkus
Acartiu
Pseudacalanus
Experiment 2
-~----___
Species
of the zooplankton
51
1
3 47
59
28 31
81
69 21 1
128
2
113 13
-.-.._-__ ._.__ __... ~ --.~__.___. -r: 0.70 0.70- 0.75- MO- 0.8.5- 0.900.75 0.80 0.85 0.90 0.95 --1 .._,. ~__-_______~~______l^
Size distribution
TARLE III
18
I5 3
43
2
I
16
2
1
10
3
44
2
6
34
73
25 17
67
I
3
2
4
66
74
I
73
57 7
88
80 8
8
I
5
2
26
4
3
19
30
1
I
28
24
1
23
1 3
2
8
I
7
14
t
1
12
10
10
2 4
2
6
1 2
3
7
I I
5
6
2
4
1.20
7
5
5
5 2
2
2
4
1
3
3
i
2
2
2
1.25 _.
2
2
1
J
1.301.35 --
I
I
1
1
3
3
1.3% 1.401.40 1.45 .~--.. -~
-l-_.__-._ .---~--“.
1.251.30 . _-_~..
1.20-
_-
2, 3, 4, and 5.
--.. 1.1%
used for Experiments
__ ._.__ Size groups 0.95- I.Oo- l.OS- I.lO1.00 1,05 1.10 1.15
community
I
1
I
1
1
I
12
12
I
1
3
2
1
5
2
3
1.50
11_--1.4% 1.50
of
87.8 %
9.7 % 15.7 %
20.2 % 50.0 %
44.3 % 13.4 %
Pseudocalanus minutus
Acffrtia longiremis P~e~doc~lanus minutus
Acarfia longirem~s Pseudocalanus minutus
Acartia longiremis Acartin longiremis
__~ -...~_-__. 02
Icg-at. Oy, N
I 2 3 4 5
1.92 4.20 3.09 8.12 9.79
Or
162
372
523
593
25
No. individuals
3714
TABLE V
(42.6 %) 1034 (43.3 %I
(43.0 %I 1756
146.2 %, 5535
680.9
(8.56 %I
(8.25 %-t 204.5
(8.34 %I 399.9
(8.47 %, 1073
1575 (9.64 %)
Gig)
(E”g) 8603 (52.6 %)
Nitrogen/ sample
Carbon/ sample
__ .._ 0.042 0.053 0.76
0.010 0.042 0.0070 0.044
NH&-N PO*-P .._-_l"."-~.
.”..-..
1.25 0.057 0.076 0.090 0.14
._ 0.0010 0.00059 0.011
NHJ-N Qz _.__~_ .-_-. ... -__lll
_.-.
and excretion rate of the zooplankton
2390
4120
12870
8040
16340
Dry weight/ sample Wug)
IV of the zooplankton.
14.7
11.0
24.6
13.5
653.6
Dry weight/ animal @B)
community.
0.0065 0.00057 0.00017 0.00049 -
Pod-P
Respiration and excretion rate P (mg body dry wt)- ’ . day- ’ /
Oxygen consumption
Acartiu tumida 13.5 % P~e~docalanlls ~tin~[tL/s 9.8 %
100%
Calanus pac$cus
Species
_-_-__l_l-~~ -_..
experiment
No.
No. of experiment
TABLE
Chemical composition
6.0 1.2
441 184
-.-_ NIP
5.07
5.19
5.16
5.40
5.46
_. 73.6 153 12.9
Atomic ratio ~~~~_~ O/N
1.26
0.91
2.05
1.15
63.0
(Pg)
Nitrogen/ animal
199 100
02
I-. O/P
6.39
4.72
10.5
6.26
344. I
W
Carbon/ animal
FILTRATION
RATE
Values for ammonia were not obtained. monia
increased
FILTRATION
Table
OF
ZOOPLANKTON
for Experiments
During
the peak
from 0.042-0.053
DURING
SPRlNG
1 and 2 and of phosphate of the spring
bloom
1.53
BLOOM
for Experiment
the excretion
to 0.76 pg-at. N. (mg dry wt))‘.
5
rate of am-
day-‘.
RATE
VI summarizes
the filtration
rates
of the zooplankton
community
as cal-
culated on three different bases. The filtration rates ‘varied’ widely, depending upon the measure used. That of C. pac$cus (Exp. 1) ranged from 13.46-5 1.60 ml. animalday- ‘. In Experiments 2 to 5, the filtration rate based upon cell count was the highest and ranged from 1.04-9.32 ml.animal-‘.dayI. The filtration rate based upon seston carbon was the lowest and ranged from 0.20-1.33 ml.animal-l.day‘.
r.
TABLE VI
Comparison of filtration rates calculated from logarithmic decreases on three different bases, namely, chlorophyll u, seston carbon, and cell count: filtration rate is I/nt In (CJC,), where n is number of animals per litre, I the time of feeding, Co the initial concentration of food, and C, concentration of food at time t. No. of experiment
Filtration ml. Chl. a
I 2 3 4 5
51.60 6.13 0.99 0.45 1.20
animal-’
. day-’
rate ml
Carbon
Cell
16.08 1.33 0.20 0.36 0.69
13.46 7.96 9.32 1.58 1.04
pg animal
C- ’
day-
’
Chl. LI
Carbon
Cell
0.150 0.948 0.0936 0.0953 0.185
0.047 0.206 0.0189 0.0763 0.106
0.039 I .23 I 0.88 I 0.335 0.161
In studying size-selectivity in grazing, we measured the maximum length of cells or chains when the cells formed chains. Fig. 3 shows the size-distribution of phytoplankton cells in experimental bottles and in the control bottle before and after the experiments.
In Experiment
1, the initial
size-range
of cells from 20-I 10 /*m constituted
over 92.7 % and in the control the size-range of cells from 20-190 pm was > 90.3 “,,. As shown in Table VII, C. paciJicus ingested phytoplankton cells which ranged in size from 30-200 pm. Table VII also summarizes the size-range of phytoplankton utilized and size-range of animals which constituted > 90 y0 of the total in each of the experiments. The size-range of cells utilized is seen to depend on that of the animals utilizing them; in other words, if grazer body size decreases C. pacz~cus --f Acartia tumida -+ Pseudocalanus minutus --f Acartia longiremis, the size range of cells mostly grazed decreases. ECOLOGICAL
RELATIONS
The assimilation of food by zooplankton was calculated assuming two levels of the assimilation efficiency, either 70 or 90 y0 (Corner, 1961) except in Experiment 1, in
154
SATORU
CONTROL
TAGUCHI
132,500CELLS
AND MITSUO
FUKUCHI
I-’
EXP. N0.2-FEi3.23/71 EXPERlMENTAL294,SOOCELLS
I-’
Fig. 3. Size distribution of phytoplankton cells: Exp. 1; 6.9pg Chl. a 1-l and 31O/*g C I-’ for initial, 7.9 /dg Chl. a 1-l and 31Opg C I-’ for control, 4.1 pg Chl. a 1-l and 246,ug C 1-l for experimental bottle: Exp. 2; 7.3 ,ug Chl. a 1-l and 293 ,ug C 1-l for initial, 8.0 pg Chl. a I-’ and 307 pg I-’ for control, 1.3 ,ug Chl. a I-’ and 206 pg C 1-l for experimental bottle: Exp. 3; 10.5 ,ug Chl. a 1-l and 418pg C 1-l for initial, 12.6yg Chl. u 1-l and 410,ug C 1-l for control, 9.7,ug Chl. a 1-l and 408,ug C 1-l for experimental bottle: Exp. 4; 12.Opg Chl. a 1-l and 635,ug C I-’ for initial, 11.9 fig Chl. a 1-l and 676pg C 1-l for control, 10.9,~g Chl. u 1-l and 632 ILg C I-’ for experimental bottle: Exp. 5; 8.Opg Chl. a 1-l and 451 /lg C 1-l for initial, 8.9 pug Chl. o 1-l and 428yg C I-’ for control, 8.Opg Chl. a I-’ and 405 @g C 1-l for experimental bottle.
which it was estimated by the difference between the ingested food and faecal pellets. According to Mayzaud (unpubl. obs.), the O/N ratios of Experiments 3 and 4 (73.6 and 153) in Table V suggest either carbohydrate or fat metabolism. Experiment 5
30-200
20-l 70
30-160
40-130
30-50
1
2
3
4
5
_-
Size range of cell utilized (Pm)
No. of experiment --hyafinu
aurita
grauida (5.0)
(32.6)
graoida hyafina
Tftalassiosira
Thafassiosira Thafassiosira ityalinu
hyalina grauida
Thafassios~rfJ hyalina Thalass~osfra graaida
Thalassiosira Thalassiosira
(93.9)
(71.8) (23.9)
(81.6) ( 14.9)
(48.3) (42,5)
(Lyng.) Brebisson & Godey
Biddulphia
Cleve
Thafassiosira
(Grunow) Giran
Thafassiosira
(53.3)
of phytoplankton
Species composition of phytoplanktoR utilized (%) __.._.~ --
Size relationship
TABLE VII
-~.-
0.80-1.15
Acartfa fongiremis Pseudoea~anus minutus Acurtia tumida
Pseudacalanus minutus Acartia iongiremis
0.75-l
.0.5
Pseudacaian~ minutus Acartia fang~re~lis
0.80-1.05
Caianus pacificus
Pseudocalanus minutus Acartia longiremis
--.--
Species composition of zooplankton incubated (“/,)
0.75-l .05
1.90
-I_-.-
Size-range of animals incubated (mm)
and zooplankton.
2 EJ 0 E
(9.7) (4.2)
,”
; 2
2
B
$
I’ 8 t?
9
(80.6)
(49.0) (44.8)
(76.5) (20.4)
(10.0)
(89.3)
(loo)
$ 2
2
P P ti
2
ZI
VI! i
17.47 2.96 14.85 13.59
4.53 22.46 3.81 19.09 17.47
TABLE
._I -- --.I- -. “-- . ~.
Assimilated ‘AE==70 _~_ AE = 90
-
tx
6.99
2.t4 4.64 3.26 8.62
Secondary production mgC.day-’ -.-._ll-,, _^ ~~__ AE = 0.7 AE = 0.9
13.50 &I7 7.48 6.60
2.70
Ii.72 lo.48
1.02
IS.49
._-~,~-“--
Mean _, ,_Iestimated growth AE-70 AE-90
, ,‘._....__, .
Net @kTldry production my C*day-”
per mZ during spring bloom,
1.52 3.30 2.32 6.12
-_ _.___
Respired __I- .~-__ RQ :: &EC RQ = 1.00
.-. 1__1-~4. .- ~__~_,
- ~~... RQ = 0.71
Standing stock, secondary and primary production
-_
2.18 -
TABI&
all vatues are expressed in ilg C * (mg dry wt)-’ . day-“: mean RQ used ta calculated mean ~st~rn~t~d growth.
I_- ^-~__. ‘_..
Faecal pellets
community:
Standing stock “_._,__^ I ^_~ _ -_ ._~_ - ._____.l___ Zooplankton P~ytop~ai~k~o~ mg dry wt mgC: my CM LI gc
”
* Observed on 23.ii.1972.
Date
2 3 4 .5
~-.
6.71 24.95 4.23 21.21 19.41
1
Ingested
_~_h~.
No. of experiment
Carbon budget of zooplanktan
FILTRA’I-ION
RATE OF ZOOPLANKT~N
showed an O/N of 12 which according nant metabolism. during
to Mayzaud
An RQ of 0.8 might be assumed
the time of the experiment.
IlURING
is an indicator if no synthesis
The amount
of carbon
15-l
SPRING BLOOM
of a protein-domiof protein
respired
took place
was estimated
from the rate of oxygen consumption, assuming the RQ to be either 0.71 (fat metabolism) or 1.00 (carbohydrate metabolism) (Conover, 1962). The growth was calculated
from the difference
between
the assimilated
and the respired
carbon
(Table
VIII). The growth rate estimated for CaZanuspaciJicus, 1.79 ,u.g C.animal-‘.day‘, is similar to I .57 /Lg C.animal-‘. day-’ for C. plurnchr~s (Taguchi & Ishii, 1972). The ecological efficiency between the primary and the secondary production was calculated as the ratio of net primary production determined by an in situ 14C method to net growth rate of zooplankton community without any estimation of mortality (Table IX). DISCUSSION
The respiration rate of C. pacificus was 0.89 1.11oxygen. (mg body dry wt)-‘.day - ’ ( = I .92 fig-at.oxygen. (mg dry wt)- ’ .day-‘), considerably lower than 4.90 ~1 oxygen. (mgdrywt)-“.day-’ formale C.paciJicltsreported by Ikeda (1970)in Mutsu Bay. This difference is probably due to the fact that our experimental temperature ranged from 5 6 ‘C in contrast to 17 “C in his experiments, and that the dry weight of our animals (average 653 pg) was higher than his animals (90 pg). The respiration rates of the smaller copepods fall into the range found by previous workers (Conover. 1959: Marshall & Orr, 1962). Compared with data of Harris (1959) obtained on a mixed population (mainly Aeartia clattsi) during April to June in Long Island Sound, our excretion rate is relatively low; however, our excretion rates on the smaller copepods are similar to those of other workers (Hargrave & Geen, 1968; Butler, Corner & Marshall, 1969). The filtration rate for Calanus pac$cus is of a similar magnitude to the range of values found for C. plumchrus by Taguchi & Ishii (1972). Even though the species were sometimes different, our filtration rates for the smaller copepods are also similar to those of previous workers (Gauld, 1951; Marshall & Qrr, 1962; Anraku, 1964). The filtration rate of zooplankton has been shown to be related to developmental stage of ~~~~/7~~, or to body weight (Gauld 1951; Marshall & Orr, 1956; Mullin & Brooks, 1970; Paffenhofer, 1971). In Fig. 4, filtration rates~anima~~day are plotted against body weight (log-log scale) together with data on C. cristatus and C. piumchr~rs from Taguchi & l’shii (1972). The correlation between filtration rate and body weight is relatively high for each method used to estimate the former and there is no significant difference in the slope of the regression equations between chlorophyll and cell count. The slope of regression equation based on seston carbon is, however, significantly greater (P < 0.05), which might be related to selectivity by the animals based on more than size alone i.e., the smaller Pseudocalanus minutus and Acartia sp. might utilize chlorophyll more efficiently while larger animals such as Calanus cristafus utilize other seston components in addition to chlorophyii.
SATORU TAGUCHl
AND MITSUO FUKUCHI
CHLOROPHYLL c7 SESTON CARBON
0.1 I
I
I 1111111 IO
I
BODY
Fig. 4. Relationship
0 Q
100
WEIGHT
IN t.i.9 CARBON
between filtration rate and body weight; data on filtration and C. p~u~chr~s (Taguchi & Ishii, 1972) are added.
rate for Caking
~~is~a~~s
Earlier workers (e.g., Fuller 1937; Gauld, 1951; Richman, 1958) found little relation between the concentration of phytoplankton cells and the filtration rate of zooplankton, but it is now well known that filtration rate depends upon the concentration of food (Ryther, 1954; Marshall & Orr, 1955; Conover, 1956; Rigler, 1961; Mullin, 19’63; Anraku, 1964; Adams & Steele, 1966; Paffenhofer, 1971). In Fig. 5 filtration rates are plotted against the initial concentration of chlorophyll a with additional data on Acartia clausi from Kawamura et al. (1968) and for CuEanus cristatus and C.~~~~c~r~~from Taguchi &Ishii (1972). Mullin (1963) showed that there was negative
FILTRATION
RATE OF ZOOPLANKTON
o n D v
PRESENT ACARTlA CALANUS CALANUS
DURING
SPRING
BLOOM
159
STUDY CLAUSI (KAWAMURA et al, 1968) CRISTATUS (I-AGUCHI & ISHll,l972) PLUMCHRUS (TAGUCHI 81 ISHll,l972)
0 0
0
0.11
0.1 INITIAL
I I llllll
1 I lllllll I
CONCENTRATION
Fig. 5. Filtration
OF
I llll
IO
CHLOROPHYLLo
rate and initial concentration
100
IN pg/i
of chlorophyll (1.
linear relation between filtration rate and ~oucentration of cells for C. ~y~e~~~~ez~~ at least to a certain level. Anraku (1964) also showed the same relation in C.~nmarc~~cus and Pseudo~alanus m~nutus. Adams & Steele (I 966) and Parsons, LeBrasseur & Fulton (1967) observed that grazing by zooplankton did not occur below a certain critical food level (2.5 pg chl. a 1-l for Calanusfinmarchicus and 58 ,ug C 1-r for Pseudocaianus minutus, respectively). The latter value could be converted to 1.9 pg ch1.a I-’ with an assumption of a carbon/chlorophyll ratio of 30. In Fig. 5, however, at 2.75 pgch1.a 1-l the filtration rate of Acartia clausi did not decrease,ranging from 26.2-35ml.animal- ‘. day- I. Calanus cristatus showed maximum filtration rates, ranging from 132.2165.5ml.animal-‘.day-‘at0.5 ~gchl.alW1, but below that concentration the filtration rate of C. ~lumchras decreased and ranged from 11.6-13.8 ml. animal-‘.day-” at 0.3 fcg ch1.a I- ‘. Our result shows’ that zooplankton can utilize food below the critical
SATORU
160
concentrations
TAGUCHI
given by Adams
AND
MlTSUO
FUKUCHI
& Steele (1966) and Parsons,
LeBrasseur
& Fulton
(1967). It is certain that the portion of food which is retained by zooplankton depends upon the size of food. In order to calculate ingestion rate the efficiency of filtration has been assumed to be 100 “/, by some previous workers (see Paffenhafer, 1’971). Such an assumption might be true when the size of all food particles is the same, which is not the case in natural sea water. The size of food varies from 2-500 Zeitzschel, 1970). From this wide range of food sizes, that utilized
CHLOROPHYLL Fig. 6. Relationship A, 2. = -1.851-3.90X
u (ug
/tm (Fig. 3 and by zooplankton
I-‘)
between index of filtration efficiency and at 5-8.5 “C (the present results): B, (Kawamura et trl., 1968).
concentration of chlorophyll f = 3.38-1.86X at 16-18
(I: C
depends in part on the size of zooplankton (Table VII). The filtration efficiency may be defined as the ratio of the volume containing the amount of food ingested to total volume containing food particles passed through the animal’s feeding appendages at present an unmeasurable quantity. Even so, there is no ‘mechanical’ loss of oxygen in the respiratory process. The ratio of the rate of oxygen consumption ( IO3 ml oxygen. (mg dry wt)-‘.day-‘) to the product of filtration rate (ml.(mg dry wt)-‘.day-’ ) x dissolved oxygen (ml oxygen) gives an estimate of respiration efficiency. Because the filtration efficiency should be related to the respiration efficiency, we have adopted this ratio as an index of filtration efficiency. This index has no dimensions and is similar to the measure of “filtering effectiveness” proposed by Ivanova (1970). The index of filtration efficiency increases with an increase in concentration of food (Fig. 6). To eliminate any temperature effect on the index of filtration efficiency, we have calculated the correlation between the index of filtration efficiency and food concentration
TABLE
X
10.16
2.42
23.iii.7 1
21.iv.71
* Observed on 23.ii.1972.
78.50* 8.05 (79.3 %) X7.24 (35.60 “/)
6.67
IS.02
22.91*
__-.
3.05 (45.7 ;A)
4.24 (18.5 %,)
26000
22700
2240*
I630
1420
140*
_.__
Ammonia Phosphate /‘g-at. N or P me2 ’ day- ’
Ammonia Phosphate [‘g-at. N or P me2 . day.-’
Ammonia Phosphate /Lg-at. N or P rns2
__
Requirement for primary production (PR)
community during spring bloom: figures in parentheses in standing stock.
Excretory rate (ER)
and excretory rate of the zooplankton
Standing stock
23.ii.71
Date
Standing stock ofnutrients
0.80
0.035
_
Ammonia
0.2:
3.03
Phosphate
ER/PR (7:)
indicate % of excretory rate
SATORU
162
TAGUCHI
for spring and summer
based on estimates
food from Kawamura
rt a/. (1968).
AND
MITSUO
of respiration.
FUKUCHI
grazing, and concentration
For each set of data the correlation
of
is significant
(P < 0.05). Although there is a relatively narrow range of food concentration in our experiments, the index of filtration efficiency varies 20-fold. This might be due to a in the size-range of the phytoplankton cells utilized because the size-range of the zooplankton varied within narrow limits (Table VII ). In other words, when the
difference
size range of phytoplankton is relatively small, the filtration ef%ciency, may increase. This suggestion is supported by an increase in chlorophyll a concentration as the sizerange of phytoplankton decreased during the time course of the spring bloom (Tables VII, rx). There are many interesting aspects to the relation between filtration efhciency, growth rate, and primary and secondary production. The estimated growth rate of zooplankton decreased gradually with the time course of the spring bloom if we ignore the extremely low growth rates in Experiment 3 (Table VIII). Even though the zooplankton community has a relatively low filtration efficiency. the growth rate of the zooplankton community is high. There is no reason why high filtration efficiency should automatically induce high growth rate since growth rate depends upon the quality of the food while filtration efficiency depends only upon the size spectrum of food. assuming that oxygen is never limiting. At the maximum of the spring bloom the ecological efficiency was lowest and subsequently increased to a level about one-tenth of that before it. While the ~ltratio~l efficiency is high at the maximum of the spring bloom, the ecological efhciency is still low. The standing stock of phytoplankton may be controlled when the grazing by, zooplankton is sufficiently high (Martin, 1968; Butler, Corner & Marshall. 1969. 1970): however, in the present work the loss by grazing of phytoplankton is extremely low (Table IX), so there is a low ecological efficiency compared with that in the open ocean (McAllister, 1969). Furthermore, only 1 “d of the nutrients required for primary production is supplied by the excretion of ammonia by the zooplankton community (Table X). If our assumptions are essentially correct, grazing and excretion by zooplankton have little effect on phytoplankton in Akkeshi Bay at the time of the spring bloom,
perhaps
because it is a highly eutrophic
area.
ACKNOWLEDGEMENTS
We are grateful to A. Koyama for identifying of zooplankton species and measuring of their body length. We would like to thank Professors T. Kawamura and S. Nishizawa for their continuing encouragement and Dr R. J. Conover and Dr P. Mayzaud for constructive criticisms.
FILTRATION
RATE
OF
ZOOPLANKTON
DURING
SPRING
BLOOM
I63
REFERENCES J. A. & J. H. STEELE, 1966. Shipboard experiments on the feeding of Ctrlnnrrs finr~zcrrchicus (Gunnerus). In, Son?e confemportrrJ studies in nznrine science, edited by H. Barnes, George Allen and Unwin Ltd, London, pp. 19-35. ANRAKU, M., 1964. Influence of the Cape Cod Canal on the hydrography and on the copepods in Buzzards Bay and Cape Cod Bay, Massachusetts. II. Respiration and feeding. Li~nnol. Occ~~~oyr.. Vol. 7, pp. 195-206. BURNS, C’. W. & F. H. RIGLER, 1967. Comparison of filtering rates of Dophnilr TOS(YIin lake \\ater and in suspension of yeast. Limnol. Oceonogr., Vol. 12, pp. 492-502. BUTLER, E. I., E. D. S. CORNER & S. M. MARSHALL, 1969. On the nutrition and metabolism of zooplankton. VI. Feeding efficiency of Cokrnrrs in terms of nitrogen and phosphorus. J. mar. biol. Ass. U.K., Vol. 49, pp. 977-1001. BUTLER, E. I., E. D. S. CORNER & S. M. MARSHALL, 1970. On the nutrition and metabolism of zooplankton. VII. Seasonal survey of nitrogen and phosphorus excretion by Ctrlrrrrrls in the Clyde sea-area. J. ,?1(lr. hiol. Ass. U.K., Vol. 50, pp. 525-560. CONOVER, R. J., 1956. Oceanography of Long Island Sound, 1952-1954. VI. Biology of Actrrtitr cltrusi and A. tonsa. Bull. Binghtrm Ocrmogr. Coil., Vol. 15, pp. 156-233. CONOVER, R. J., 1959. Regional and seasonal variation in the respiratory rate of marine copepods. Limnol. Ocemogr., Vol. 4, pp. 259-268. CONOVER, R. J.. 1962. Metabolism and growth in C’alnnlrs hFperboreu.9 in relation to its life cycle. Rtrpp. P.-c. R&n. Cons. perrn. in?. Esplor. Mer, Vol. 153, pp. 190-197. CORNER, E. D. S., 1961. On the nutrition and metabolism of zooplankton. I. Preliminary observations on the feeding of the marine copepod Calmus he/,yolundicus (Calanus). J. ,?l(,r. biol. Ass. U.K., Vol. 41, pp. 5-16. FULLER, J. L.. 1937. Feeding rate of Co/onus finnzcrrchicrrs in relation to environmental conditions. Biol. Bull. mar. biol. Lob., Woods Hole, Vol. 72, pp. 233-246. GAIJLD, D. T., 195 I. The grazing rate of planktonic copepods. J. mar. hiol. Ass. U.K., Vol. 19, pp. 695-706. GLIWI~Z, G. M., 1969. The share of algae, bacteria and trypton in the food of the pelagic zooplankton of lakes with various trophic characteristics. Bull. Actrd. pal. Sri. CI. /I Sdr. Sri. Biol.. Vol. 17, pp. 159-165. HAR~~RAVE, 9. T. & G. H. GEEN, 1968. Phosphorus excretion by zooplankton. Linrnol. Owrrwrgr.. Vol. 13, pp. 332-355. HARRIS, E., 1959. The nitrogen cycle in Long Island Sound. Bull. Binghom Oceanogr. Co/l., Vol. 17. pp. 31-65. IKEDA, T., 1970. Relationship between respiration rate and body size in marine plankton animals as a function of the temperature of habitat. Bull. For. Fish. Hohkaido (/nil?., Vol. 21, pp. 91-l 12. IVAN~VA, M. B., 1970. Relations between the food concentration, filtration rate and effectiveness of oxygen utilization by Clodocern. PO/. Arch. HJ’drobiol., Vol. 17, pp. 161-168. KAWAIMURA, T., S. NISHIZAWA, H. ISHII,T. TANAKA & S. UNO, 1968. Excretion, respiration and grazing of zooplankton community. Progress Report, 1967. In, Studies on rhe productiriries of biocoenoses in northern cold wirer, Akkeshi Bay Research Group, edited by S. Motoda, Faculty of Fisheries, Hokkaido University, pp. 21-26 (in Japanese). MARSHALL, S. M. & A. P. ORR, 1955. On the biology of Calmus finmarchicus. VIII. Food uptake. assimilation and excretion in adult and stage V Calm~rs. J. mar. biol. Ass. U.K.. Vol. 23, pp. 495-529. MARSHALL, S. M. & A. P. ORR, 1956. On the biology of Cnltrnrrs fin,nnrchicus. IX. Feeding and digestion in the young stages. J. Inor. biol. Ass. U.K., Vol. 35, pp. 587-603. MARSHAL.L, S. M. & A. P. ORR, 1962. Food and feeding in copepods. Rtrpp. P.-c. Rim. Cms. perru. int. Explor. Mer, Vol. 153, pp. 93-97. MARTIN, J. H., 1968. Phytoplankton-zooplankton relationships in Narragansett Bay. 111. Seasonal changes in zooplankton excretion rates in relation to phytoplankton abundance. Lirnnol. Oceonogr.. Vol. 13, pp. 63-67. MCALLISTER. C. D., 1969. Aspects of estimating zooplankton production from phytoplankton production. J. Fish. Res. Bd Can., Vol. 26, pp. 119-220. ADAMS,
164
SATORU
TAGUCHl
AND
MITSUO
FUKUCHI
MULLIN, M. M., 1963. Some factors affecting the feeding of marine copepods of the genus Calunus. Limo/. Oceunogr., Vol. 8, pp. 239-250. MULLIN, M. M. & E. R. BROOKS, 1970. Growth and metabolism of two planktonic, marine copepods as influenced by temperature and types of food. In, Marine .food -hoins, edited by J. H. Steele, Oliver and Boyd, Edinburgh, pp. 74-95. NAKAJIMA, K., 1969. Suspended particulate matter in the waters on both sides of Aleutian Ridges. J. oceanogr. Sor. Japun, Vol. 25, pp. 17-26. OMORI, M., 1969. Weight and chemical composition of some imporlant oceanic zocplankton in the north Pacific Ocean. Mar. Biol., Vol. 3, pp. 4-10. PAFFEN~~BFER, G.-A., 1971. Grazing and ingestion rates of nauplii, copepodites, and adults of the marine planktonic copepod C&anus helgolandicus. Mar. Biol., Vol. 11, pp. 386-298. PARSONS, T. R., R. J. LEBRASSEUR & J. D. FULTON, 1967. Some observations on the dependence of zooplankton grazing on the cell size and concentration of phytoplankton blooms. J. Oce~nogr. Sot. Japan, Vol. 23, pp. 1 I-18. RICHMAN, S., 1958. The transformation of energy by Dnphnirr pulex. Ecol. .Monogr., Vol. 2X. pp. 273-29 I. RIGLER, F. H., 1961. The relation between concentration of food and feeding rate of Dnphnia mugnu Straus. Corn. J. Zool., Vol. 39, pp. 857-868. RY~HER, J. H., 1954. Inhibitory effects of phytoplankton upon the feeding of Duphniu mcrgntr with reference to growth, reproduction and survival. Ecology, Vol. 33, pp. 522-535. SAIJO, Y. & S. NLSHIZAWA, 1969. Excitation spectra in the fluorometric determination of chlorophyll-u and pheophytin-a. Mur. Biol., Vol. 2, pp. 135-136. SOL~)RZANO, L., 1969. Determination of ammonia in natural waters by the phenol-hypochlorite method. Limnol. Oceunogr., Vol. 14, pp. 799-801. STRICKLAND, J. D. H. & T. R. PARSONS, 1968. A practical handbook of seawater analysis. B/r//. Fish. Res. Bd Can., No. 167, 3 I1 pp. TAGLJCHI, S. & H. ISHII, 1972. Shipboard experiments on respiration, excretion, and grazing or Cnlmus cristatw and C. plurnchrus (Copepoda) in the northern North Pacific. In, Biologiccd oceanography of the northern North Pacific Oceun, edited by A. Y. Takenouti et trl.. ldemitsa Shoten, Tokyo, pp. 419431. ZEITZSCHEL, B., 1970. The quantity, composition and distribution of suspended matter in the Gulf of California. Mar. Biol., Vol. 7, pp. 305-318.
Publishing Company
FILTRATlON RATE OF ZOOPLANKTON COMMUNITY DURING SPRING BLOOM IN AKKESHI BAY ’ SATORU TAGUCHI’ Faculty qf‘ Fisheries,
and MITSUO FUKUCHI
Hokkaido Unicersit_r, Hakodnte, Jopun
Abstract: The filtration
rate of a natural zooplankton community at the time of the spring bloom in Akkeshi Bay was estimated using changes in concentration of chlorophyll a, of particulate carbon, and changes in cell numbers. The size range of phytoplankton cells utilized indicated that the maximum length of chain consumed depended upon the size-range of the zooplankton community. Evidence for size-selection of food by animals is presented. The possible explanation of relation between the filtration efficiency - the ratio of respiration rate to the product of filtration rate and dissolved oxygen - and the quantity and quality of food is discussed. When there is a wide range of phytoplankton sizes or a small amount of phytoplankton, the filtration efficiency decreases.
Most estimations of filtration rates have been made for single species of zooplankton in an experimental container. In the natural marine environment, however, the community structure of zooplankton is so complicated that few have tried to determine the relationships between filter-feeders and their food. In the freshwater environment, Richman (1958), Burns & Rigler (1967), Ghwicz (t969), and Ivanova (1970) have tried to establish the relationship between the filtration rate of zooplankton community and size of food. In the present study we report observations on the filtration rate and selectivity by a natural zooplankton community cles during the spring bloom.
caught with net as it fed on naturally
occurring
parti-
MATERIALS AND METHODS
Five experiments
were carried
out on the zooplankton
community
in Akkeshi
Bay
(Fig. I) on 23rd February, 23rd March, and 21st April, 1971 at the central station (42”58.5’N: 143”49.4’E). Experimental animals were caught with a conical plankton net (30 cm in mouth diameter, 100 cm Tong, 0.35 mm mesh apertures) towed for 10 min about noon. The animals were acclimatized in a IO-1 bucket in the dark for z 8 h. For each experiment, surface water was sampled with a plastic bucket and passed through 0.35 mm mesh net to remove large planktonic animals. All of the experiments ’ Contribution from JIBP-PM. ’ Present address: Fisheries & Marine Service, Marine Ecology Laboratory, Oceanography, Dartmouth, Nova Scotia, Canada. 145
Bedford Institute of
146
SATORU
TAGUCHI
AND
MITSUO
FUKUCHI
were begun at 20.00 h and lasted for 24 h. The experimental than the in situ temperature
at which the animals
temperatures
were collected
were higher
by 4.30 “-7.15 ‘C
(Table I), but varied less than +0.5 “C during the experiments. In the first experiment 25 healthy individual Calanuspacijhs were transferred to 2-l dark bottles filled with net (0.35 mm mesh) moved and 15 animals
filtered
surface
water.
After incubation,
were frozen for chemical
analysis
the animals
were re-
and 10 were fixed in formalin
43=‘N
43ON
I
I
I
144O5O’E Fig. 1. Map
of location
of experimental
station.
for identification of stage. Weight was measured after the frozen samples were dried at 60 “C for 1 h. The organic carbon and nitrogen of animals were measured with a Hitachi CHN Analyser. In the Experiments 2 to 5, the same procedure was followed except that mixed populations of zooplankton rather than a single species were used. Before and after incubation, subsamples of water, excluding faecal pellets, were taken to determine oxygen, chlorophyll, phytoplankton cells, total seston carbon, and nutrients.
HLTRATION
RATE OF ZOOPLANKTBN
DURING
SPRING BLOOM
147
tninutus
Kr0yer
Thompson
ptrciJiw.7 Brodski
Crdtnus
Total
Uitlruno
sintilis
Ciaus
Tt,rfrrtzusdisc~tt{d~~tiis Thompson
pctcijfcn
Brodski
he~dftz~t~ii
Willey
Metriditr
Euryte,norri
Acctrticr turmdu
Acurtiu lungirewzif (Lillijeborg)
Pseudoculunus
_ -_ _.-._-. ..-l__-_l-.
Species
& Scott
& Scott
II--.--
-..
Species composition
V IV
Female Malt
Copepodid
Ii
Copepodid V Copepodid IV Copepodid I1I
Female Copepodid Copepodid
Female Male Copepodid
Female Male
Female Male Copepodid
Female Male Copepodid
-..-_. ._. ._
Stage
of the rooplankton
25
(4) 113) (8)
_. _
_ -.
_
._
-
1
591
I
I
^...
5
523
I
^_
372
I
__
162
13 ^.
-
-.
-
-
.-
__
-. i_
_.
5
13 5
96 21 2
12 2 2
3
2
__
-_
2
1
IO
_ -
123 38 4
160 4 22
1
2
“,.
I 3 4
._
-
2 ._
85 21
375 I 14
4
_ ~.-...__--- .___ ”
number
__~__.
3
3 2
_
Experiment
1
.-
50 8
490 9 22
2
incubated during the experiments.
E
FILTRATION
RATE
The rate of respiration experimental determined excretion
OF
ZOOPLA~KTON
was obtained
and control by the Winkler
rate was obtained
bottles method
DURING
from the difference
after 24 h incubation. as described
SPRlNG
in oxygen concentr~~tion Oxygen
by Strickland
from the difference
between
I49
BLOOM
concentrations
& Parsons
ammonia-N
in
were
(1968). The concentration
and phosphate-phosphorus concentration in experimental and control suspensions after incubation. Ammonia-nitrogen was determined by the method of Solorzano (1969), and phosphate-phosphorus by the one-solution method of Murphy & Riley (see Strickland &Parsons, 1968). The filtration rate was obtained from the calculated rates of decrease of three different values: chlorophyll a concentration, phytoplankton cell numbers, and particulate organic carbon concent~tion. chlorophyll a concentration was measured by the method of Saijo & Nishizawa (1969). Phytoplankton ceils were counted under an inverted microscope. Size was measured for each phytoplankton ceil; in the case of chain-forming species, the maximum and minimum size of the chain was measured. Particulate organic carbon was determined by the method of Nakajima (1969). BODY STAGE COPEPODITE
DRY
Fig. 2. Size distribution
BODY
WEIGHT
of CWanw
!N
pncificus
m LEIN%H V IV
1.95 .-_2.45 190
ug
used for Experiment
I.
At the same station, vertical observations of temperature, ammonia-N, phosphate-P, chlorophyll a, and seston carbon, down to 20 m, were made. The standing stock of zooplankton community was obtained from a vertical tow with a 0.35-mm mesh net. A series of in situ primary production experiments was also carried out at this station by the method of Strickland & Parsons (1968).
150
SATORU
TAGUCHI
AND
MITSUO
FUKUCH1
RESULTS BODY SIZE,
WEIGHT
AND SPECIES COMPOSITION
Species and stage composition of zooplankton community is shown for each experiment in Table II. In Experiment 1,25 stage III, IV and V, C,paci$clrs were selected. Their weight distribution and length are shown in Fig. 2. In Experiment I, C. pacijicus with a body length of % 1.90 mm was assumed to be dominant. In Experiment 2, carried out in February, P.~eadoc~i~us rnj~a~~swith a body length of 0.70-f .25 mm was over 87.5 % of total number while Aearria Zo~g~re7nis,0.75-0.95 mm long, constituted only 9.7 % of the total number (Table III). In Experiment 3 in March the percentage of the two species changed to 75.704 for Pseudoculanus minutus (0.85-1.05 mm iong)and20.2~~ for Acartia ~o~giremjs~O.80-1.00 mm Iong). As the average body length of the two species increased from Experiment 2 to Experimelit 3, the average dry weight increased from 13.5 pg to 24.6 /lg. In Experiment 4, Pseuducalanus minurus (0.80-I .05 mm long) and Acartia longiremis (0.80-1.00 mm long) made up 50.0 ‘;i and 44.3 O,;, respectively of the total. The portion of smaller-sized A. Iongiremis more than doubled and consequently the average body dry weight decreased by one-half. In Experiment 5, A. lo~zgire~~is(0 X0-1.05 mm long) was 73.4 %, A. tumidu (0.95-1.35 mm long) 13.5 “/6,and Pseadocalun~~srn~n~~~.~ (O.SO-1.15 mm long) 9.8 :I:;of the total. In addition to the small-sized Acarfiu Iongjremjs, larger A. rumida occupied over lo:, of total number, which might have caused the increase of average body dry weight to 14.7 ,WJ. CHEMICAL
COMPOSITION
Chemical analyses for all experiments are summarized in Table IV. Average carbon and nitrogen content per body dry weight of CalanuspaciJicus was 52.6 “/, and 9.64 ‘;,;, respectively. These values are similar to 48.0 to 58.4 % for carbon content and 7.8 to 12.7 “/:,for nitrogen content for C. pacz@cus, collected in the northern North Pacific Ocean by Omori (1969). The carbon and nitrogen content varied with stage but for C. ~~~~~ci~~greater than 700 pg dry weight, carbon and nitrogen were constant at ?Z 54 ‘?Gand 9.12 %, respectively. For mixed populations, i.e., Experiments 2, 3, 4, and 5, carbon and nitrogen contents fell within a narrow range: 42.6-46.2 Y/i carbon and 8.25~8.50% nitrogen. Average dry weight per animal ranged from 1I .O-24.6 pg and the maximum dry weight was observed in March when primary production was at a peak. RESPIRATION
AND EXCRETION
RATES
Data from the respiration and excretion experiments are summarized in Table V. The respiration rate increased during the dev~iopment of the spring bloom from 1.92 to 4.20 jug-at. oxygen. (mg body dry wt)-‘. day-’ in February and to 9.79 pg-at. oxygen. (mg body dry wt)-‘. day-’ in April.
minutus
longiremis
similis
pacijica
herdmanii
3
tumida
tumida
Acartia
herdmanii
Total
~~erdl~laflii
tumida
Eurytemora
Acartia
It
I 30 I I 33
I 10
langiremis
Pse~o~alan~
Acartia
72
i~l~nlitas
20 48 3
15 25
L
83
1
45 37
133
43
I
22 20
70
4
19
110
40
2
2
1 2
61 6
fotai Experiment 5
Temora discaudatus
Oithona similis
Eurytemora
Calanus pacificus
longiremis
Acartia
Pseudacaianus
Total Experiment 4
ninutus
herdmanii
Oithona similis
Eurytemora
Calanus pacijicus
Acartia
minutus
longiremis
Acartia
Pseudocaianus
experiment
Total
Temora discaudatus
Oithora
Metridia
Eurytemora
Calanus pacijkus
Acartiu
Pseudacalanus
Experiment 2
-~----___
Species
of the zooplankton
51
1
3 47
59
28 31
81
69 21 1
128
2
113 13
-.-.._-__ ._.__ __... ~ --.~__.___. -r: 0.70 0.70- 0.75- MO- 0.8.5- 0.900.75 0.80 0.85 0.90 0.95 --1 .._,. ~__-_______~~______l^
Size distribution
TARLE III
18
I5 3
43
2
I
16
2
1
10
3
44
2
6
34
73
25 17
67
I
3
2
4
66
74
I
73
57 7
88
80 8
8
I
5
2
26
4
3
19
30
1
I
28
24
1
23
1 3
2
8
I
7
14
t
1
12
10
10
2 4
2
6
1 2
3
7
I I
5
6
2
4
1.20
7
5
5
5 2
2
2
4
1
3
3
i
2
2
2
1.25 _.
2
2
1
J
1.301.35 --
I
I
1
1
3
3
1.3% 1.401.40 1.45 .~--.. -~
-l-_.__-._ .---~--“.
1.251.30 . _-_~..
1.20-
_-
2, 3, 4, and 5.
--.. 1.1%
used for Experiments
__ ._.__ Size groups 0.95- I.Oo- l.OS- I.lO1.00 1,05 1.10 1.15
community
I
1
I
1
1
I
12
12
I
1
3
2
1
5
2
3
1.50
11_--1.4% 1.50
of
87.8 %
9.7 % 15.7 %
20.2 % 50.0 %
44.3 % 13.4 %
Pseudocalanus minutus
Acffrtia longiremis P~e~doc~lanus minutus
Acarfia longirem~s Pseudocalanus minutus
Acartia longiremis Acartin longiremis
__~ -...~_-__. 02
Icg-at. Oy, N
I 2 3 4 5
1.92 4.20 3.09 8.12 9.79
Or
162
372
523
593
25
No. individuals
3714
TABLE V
(42.6 %) 1034 (43.3 %I
(43.0 %I 1756
146.2 %, 5535
680.9
(8.56 %I
(8.25 %-t 204.5
(8.34 %I 399.9
(8.47 %, 1073
1575 (9.64 %)
Gig)
(E”g) 8603 (52.6 %)
Nitrogen/ sample
Carbon/ sample
__ .._ 0.042 0.053 0.76
0.010 0.042 0.0070 0.044
NH&-N PO*-P .._-_l"."-~.
.”..-..
1.25 0.057 0.076 0.090 0.14
._ 0.0010 0.00059 0.011
NHJ-N Qz _.__~_ .-_-. ... -__lll
_.-.
and excretion rate of the zooplankton
2390
4120
12870
8040
16340
Dry weight/ sample Wug)
IV of the zooplankton.
14.7
11.0
24.6
13.5
653.6
Dry weight/ animal @B)
community.
0.0065 0.00057 0.00017 0.00049 -
Pod-P
Respiration and excretion rate P (mg body dry wt)- ’ . day- ’ /
Oxygen consumption
Acartiu tumida 13.5 % P~e~docalanlls ~tin~[tL/s 9.8 %
100%
Calanus pac$cus
Species
_-_-__l_l-~~ -_..
experiment
No.
No. of experiment
TABLE
Chemical composition
6.0 1.2
441 184
-.-_ NIP
5.07
5.19
5.16
5.40
5.46
_. 73.6 153 12.9
Atomic ratio ~~~~_~ O/N
1.26
0.91
2.05
1.15
63.0
(Pg)
Nitrogen/ animal
199 100
02
I-. O/P
6.39
4.72
10.5
6.26
344. I
W
Carbon/ animal
FILTRATION
RATE
Values for ammonia were not obtained. monia
increased
FILTRATION
Table
OF
ZOOPLANKTON
for Experiments
During
the peak
from 0.042-0.053
DURING
SPRlNG
1 and 2 and of phosphate of the spring
bloom
1.53
BLOOM
for Experiment
the excretion
to 0.76 pg-at. N. (mg dry wt))‘.
5
rate of am-
day-‘.
RATE
VI summarizes
the filtration
rates
of the zooplankton
community
as cal-
culated on three different bases. The filtration rates ‘varied’ widely, depending upon the measure used. That of C. pac$cus (Exp. 1) ranged from 13.46-5 1.60 ml. animalday- ‘. In Experiments 2 to 5, the filtration rate based upon cell count was the highest and ranged from 1.04-9.32 ml.animal-‘.dayI. The filtration rate based upon seston carbon was the lowest and ranged from 0.20-1.33 ml.animal-l.day‘.
r.
TABLE VI
Comparison of filtration rates calculated from logarithmic decreases on three different bases, namely, chlorophyll u, seston carbon, and cell count: filtration rate is I/nt In (CJC,), where n is number of animals per litre, I the time of feeding, Co the initial concentration of food, and C, concentration of food at time t. No. of experiment
Filtration ml. Chl. a
I 2 3 4 5
51.60 6.13 0.99 0.45 1.20
animal-’
. day-’
rate ml
Carbon
Cell
16.08 1.33 0.20 0.36 0.69
13.46 7.96 9.32 1.58 1.04
pg animal
C- ’
day-
’
Chl. LI
Carbon
Cell
0.150 0.948 0.0936 0.0953 0.185
0.047 0.206 0.0189 0.0763 0.106
0.039 I .23 I 0.88 I 0.335 0.161
In studying size-selectivity in grazing, we measured the maximum length of cells or chains when the cells formed chains. Fig. 3 shows the size-distribution of phytoplankton cells in experimental bottles and in the control bottle before and after the experiments.
In Experiment
1, the initial
size-range
of cells from 20-I 10 /*m constituted
over 92.7 % and in the control the size-range of cells from 20-190 pm was > 90.3 “,,. As shown in Table VII, C. paciJicus ingested phytoplankton cells which ranged in size from 30-200 pm. Table VII also summarizes the size-range of phytoplankton utilized and size-range of animals which constituted > 90 y0 of the total in each of the experiments. The size-range of cells utilized is seen to depend on that of the animals utilizing them; in other words, if grazer body size decreases C. pacz~cus --f Acartia tumida -+ Pseudocalanus minutus --f Acartia longiremis, the size range of cells mostly grazed decreases. ECOLOGICAL
RELATIONS
The assimilation of food by zooplankton was calculated assuming two levels of the assimilation efficiency, either 70 or 90 y0 (Corner, 1961) except in Experiment 1, in
154
SATORU
CONTROL
TAGUCHI
132,500CELLS
AND MITSUO
FUKUCHI
I-’
EXP. N0.2-FEi3.23/71 EXPERlMENTAL294,SOOCELLS
I-’
Fig. 3. Size distribution of phytoplankton cells: Exp. 1; 6.9pg Chl. a 1-l and 31O/*g C I-’ for initial, 7.9 /dg Chl. a 1-l and 31Opg C I-’ for control, 4.1 pg Chl. a 1-l and 246,ug C 1-l for experimental bottle: Exp. 2; 7.3 ,ug Chl. a 1-l and 293 ,ug C 1-l for initial, 8.0 pg Chl. a I-’ and 307 pg I-’ for control, 1.3 ,ug Chl. a I-’ and 206 pg C 1-l for experimental bottle: Exp. 3; 10.5 ,ug Chl. a 1-l and 418pg C 1-l for initial, 12.6yg Chl. u 1-l and 410,ug C 1-l for control, 9.7,ug Chl. a 1-l and 408,ug C 1-l for experimental bottle: Exp. 4; 12.Opg Chl. a 1-l and 635,ug C I-’ for initial, 11.9 fig Chl. a 1-l and 676pg C 1-l for control, 10.9,~g Chl. u 1-l and 632 ILg C I-’ for experimental bottle: Exp. 5; 8.Opg Chl. a 1-l and 451 /lg C 1-l for initial, 8.9 pug Chl. o 1-l and 428yg C I-’ for control, 8.Opg Chl. a I-’ and 405 @g C 1-l for experimental bottle.
which it was estimated by the difference between the ingested food and faecal pellets. According to Mayzaud (unpubl. obs.), the O/N ratios of Experiments 3 and 4 (73.6 and 153) in Table V suggest either carbohydrate or fat metabolism. Experiment 5
30-200
20-l 70
30-160
40-130
30-50
1
2
3
4
5
_-
Size range of cell utilized (Pm)
No. of experiment --hyafinu
aurita
grauida (5.0)
(32.6)
graoida hyafina
Tftalassiosira
Thafassiosira Thafassiosira ityalinu
hyalina grauida
Thafassios~rfJ hyalina Thalass~osfra graaida
Thalassiosira Thalassiosira
(93.9)
(71.8) (23.9)
(81.6) ( 14.9)
(48.3) (42,5)
(Lyng.) Brebisson & Godey
Biddulphia
Cleve
Thafassiosira
(Grunow) Giran
Thafassiosira
(53.3)
of phytoplankton
Species composition of phytoplanktoR utilized (%) __.._.~ --
Size relationship
TABLE VII
-~.-
0.80-1.15
Acartfa fongiremis Pseudoea~anus minutus Acurtia tumida
Pseudacalanus minutus Acartia iongiremis
0.75-l
.0.5
Pseudacaian~ minutus Acartia fang~re~lis
0.80-1.05
Caianus pacificus
Pseudocalanus minutus Acartia longiremis
--.--
Species composition of zooplankton incubated (“/,)
0.75-l .05
1.90
-I_-.-
Size-range of animals incubated (mm)
and zooplankton.
2 EJ 0 E
(9.7) (4.2)
,”
; 2
2
B
$
I’ 8 t?
9
(80.6)
(49.0) (44.8)
(76.5) (20.4)
(10.0)
(89.3)
(loo)
$ 2
2
P P ti
2
ZI
VI! i
17.47 2.96 14.85 13.59
4.53 22.46 3.81 19.09 17.47
TABLE
._I -- --.I- -. “-- . ~.
Assimilated ‘AE==70 _~_ AE = 90
-
tx
6.99
2.t4 4.64 3.26 8.62
Secondary production mgC.day-’ -.-._ll-,, _^ ~~__ AE = 0.7 AE = 0.9
13.50 &I7 7.48 6.60
2.70
Ii.72 lo.48
1.02
IS.49
._-~,~-“--
Mean _, ,_Iestimated growth AE-70 AE-90
, ,‘._....__, .
Net @kTldry production my C*day-”
per mZ during spring bloom,
1.52 3.30 2.32 6.12
-_ _.___
Respired __I- .~-__ RQ :: &EC RQ = 1.00
.-. 1__1-~4. .- ~__~_,
- ~~... RQ = 0.71
Standing stock, secondary and primary production
-_
2.18 -
TABI&
all vatues are expressed in ilg C * (mg dry wt)-’ . day-“: mean RQ used ta calculated mean ~st~rn~t~d growth.
I_- ^-~__. ‘_..
Faecal pellets
community:
Standing stock “_._,__^ I ^_~ _ -_ ._~_ - ._____.l___ Zooplankton P~ytop~ai~k~o~ mg dry wt mgC: my CM LI gc
”
* Observed on 23.ii.1972.
Date
2 3 4 .5
~-.
6.71 24.95 4.23 21.21 19.41
1
Ingested
_~_h~.
No. of experiment
Carbon budget of zooplanktan
FILTRA’I-ION
RATE OF ZOOPLANKT~N
showed an O/N of 12 which according nant metabolism. during
to Mayzaud
An RQ of 0.8 might be assumed
the time of the experiment.
IlURING
is an indicator if no synthesis
The amount
of carbon
15-l
SPRING BLOOM
of a protein-domiof protein
respired
took place
was estimated
from the rate of oxygen consumption, assuming the RQ to be either 0.71 (fat metabolism) or 1.00 (carbohydrate metabolism) (Conover, 1962). The growth was calculated
from the difference
between
the assimilated
and the respired
carbon
(Table
VIII). The growth rate estimated for CaZanuspaciJicus, 1.79 ,u.g C.animal-‘.day‘, is similar to I .57 /Lg C.animal-‘. day-’ for C. plurnchr~s (Taguchi & Ishii, 1972). The ecological efficiency between the primary and the secondary production was calculated as the ratio of net primary production determined by an in situ 14C method to net growth rate of zooplankton community without any estimation of mortality (Table IX). DISCUSSION
The respiration rate of C. pacificus was 0.89 1.11oxygen. (mg body dry wt)-‘.day - ’ ( = I .92 fig-at.oxygen. (mg dry wt)- ’ .day-‘), considerably lower than 4.90 ~1 oxygen. (mgdrywt)-“.day-’ formale C.paciJicltsreported by Ikeda (1970)in Mutsu Bay. This difference is probably due to the fact that our experimental temperature ranged from 5 6 ‘C in contrast to 17 “C in his experiments, and that the dry weight of our animals (average 653 pg) was higher than his animals (90 pg). The respiration rates of the smaller copepods fall into the range found by previous workers (Conover. 1959: Marshall & Orr, 1962). Compared with data of Harris (1959) obtained on a mixed population (mainly Aeartia clattsi) during April to June in Long Island Sound, our excretion rate is relatively low; however, our excretion rates on the smaller copepods are similar to those of other workers (Hargrave & Geen, 1968; Butler, Corner & Marshall, 1969). The filtration rate for Calanus pac$cus is of a similar magnitude to the range of values found for C. plumchrus by Taguchi & Ishii (1972). Even though the species were sometimes different, our filtration rates for the smaller copepods are also similar to those of previous workers (Gauld, 1951; Marshall & Qrr, 1962; Anraku, 1964). The filtration rate of zooplankton has been shown to be related to developmental stage of ~~~~/7~~, or to body weight (Gauld 1951; Marshall & Orr, 1956; Mullin & Brooks, 1970; Paffenhofer, 1971). In Fig. 4, filtration rates~anima~~day are plotted against body weight (log-log scale) together with data on C. cristatus and C. piumchr~rs from Taguchi & l’shii (1972). The correlation between filtration rate and body weight is relatively high for each method used to estimate the former and there is no significant difference in the slope of the regression equations between chlorophyll and cell count. The slope of regression equation based on seston carbon is, however, significantly greater (P < 0.05), which might be related to selectivity by the animals based on more than size alone i.e., the smaller Pseudocalanus minutus and Acartia sp. might utilize chlorophyll more efficiently while larger animals such as Calanus cristafus utilize other seston components in addition to chlorophyii.
SATORU TAGUCHl
AND MITSUO FUKUCHI
CHLOROPHYLL c7 SESTON CARBON
0.1 I
I
I 1111111 IO
I
BODY
Fig. 4. Relationship
0 Q
100
WEIGHT
IN t.i.9 CARBON
between filtration rate and body weight; data on filtration and C. p~u~chr~s (Taguchi & Ishii, 1972) are added.
rate for Caking
~~is~a~~s
Earlier workers (e.g., Fuller 1937; Gauld, 1951; Richman, 1958) found little relation between the concentration of phytoplankton cells and the filtration rate of zooplankton, but it is now well known that filtration rate depends upon the concentration of food (Ryther, 1954; Marshall & Orr, 1955; Conover, 1956; Rigler, 1961; Mullin, 19’63; Anraku, 1964; Adams & Steele, 1966; Paffenhofer, 1971). In Fig. 5 filtration rates are plotted against the initial concentration of chlorophyll a with additional data on Acartia clausi from Kawamura et al. (1968) and for CuEanus cristatus and C.~~~~c~r~~from Taguchi &Ishii (1972). Mullin (1963) showed that there was negative
FILTRATION
RATE OF ZOOPLANKTON
o n D v
PRESENT ACARTlA CALANUS CALANUS
DURING
SPRING
BLOOM
159
STUDY CLAUSI (KAWAMURA et al, 1968) CRISTATUS (I-AGUCHI & ISHll,l972) PLUMCHRUS (TAGUCHI 81 ISHll,l972)
0 0
0
0.11
0.1 INITIAL
I I llllll
1 I lllllll I
CONCENTRATION
Fig. 5. Filtration
OF
I llll
IO
CHLOROPHYLLo
rate and initial concentration
100
IN pg/i
of chlorophyll (1.
linear relation between filtration rate and ~oucentration of cells for C. ~y~e~~~~ez~~ at least to a certain level. Anraku (1964) also showed the same relation in C.~nmarc~~cus and Pseudo~alanus m~nutus. Adams & Steele (I 966) and Parsons, LeBrasseur & Fulton (1967) observed that grazing by zooplankton did not occur below a certain critical food level (2.5 pg chl. a 1-l for Calanusfinmarchicus and 58 ,ug C 1-r for Pseudocaianus minutus, respectively). The latter value could be converted to 1.9 pg ch1.a I-’ with an assumption of a carbon/chlorophyll ratio of 30. In Fig. 5, however, at 2.75 pgch1.a 1-l the filtration rate of Acartia clausi did not decrease,ranging from 26.2-35ml.animal- ‘. day- I. Calanus cristatus showed maximum filtration rates, ranging from 132.2165.5ml.animal-‘.day-‘at0.5 ~gchl.alW1, but below that concentration the filtration rate of C. ~lumchras decreased and ranged from 11.6-13.8 ml. animal-‘.day-” at 0.3 fcg ch1.a I- ‘. Our result shows’ that zooplankton can utilize food below the critical
SATORU
160
concentrations
TAGUCHI
given by Adams
AND
MlTSUO
FUKUCHI
& Steele (1966) and Parsons,
LeBrasseur
& Fulton
(1967). It is certain that the portion of food which is retained by zooplankton depends upon the size of food. In order to calculate ingestion rate the efficiency of filtration has been assumed to be 100 “/, by some previous workers (see Paffenhafer, 1’971). Such an assumption might be true when the size of all food particles is the same, which is not the case in natural sea water. The size of food varies from 2-500 Zeitzschel, 1970). From this wide range of food sizes, that utilized
CHLOROPHYLL Fig. 6. Relationship A, 2. = -1.851-3.90X
u (ug
/tm (Fig. 3 and by zooplankton
I-‘)
between index of filtration efficiency and at 5-8.5 “C (the present results): B, (Kawamura et trl., 1968).
concentration of chlorophyll f = 3.38-1.86X at 16-18
(I: C
depends in part on the size of zooplankton (Table VII). The filtration efficiency may be defined as the ratio of the volume containing the amount of food ingested to total volume containing food particles passed through the animal’s feeding appendages at present an unmeasurable quantity. Even so, there is no ‘mechanical’ loss of oxygen in the respiratory process. The ratio of the rate of oxygen consumption ( IO3 ml oxygen. (mg dry wt)-‘.day-‘) to the product of filtration rate (ml.(mg dry wt)-‘.day-’ ) x dissolved oxygen (ml oxygen) gives an estimate of respiration efficiency. Because the filtration efficiency should be related to the respiration efficiency, we have adopted this ratio as an index of filtration efficiency. This index has no dimensions and is similar to the measure of “filtering effectiveness” proposed by Ivanova (1970). The index of filtration efficiency increases with an increase in concentration of food (Fig. 6). To eliminate any temperature effect on the index of filtration efficiency, we have calculated the correlation between the index of filtration efficiency and food concentration
TABLE
X
10.16
2.42
23.iii.7 1
21.iv.71
* Observed on 23.ii.1972.
78.50* 8.05 (79.3 %) X7.24 (35.60 “/)
6.67
IS.02
22.91*
__-.
3.05 (45.7 ;A)
4.24 (18.5 %,)
26000
22700
2240*
I630
1420
140*
_.__
Ammonia Phosphate /‘g-at. N or P me2 ’ day- ’
Ammonia Phosphate [‘g-at. N or P me2 . day.-’
Ammonia Phosphate /Lg-at. N or P rns2
__
Requirement for primary production (PR)
community during spring bloom: figures in parentheses in standing stock.
Excretory rate (ER)
and excretory rate of the zooplankton
Standing stock
23.ii.71
Date
Standing stock ofnutrients
0.80
0.035
_
Ammonia
0.2:
3.03
Phosphate
ER/PR (7:)
indicate % of excretory rate
SATORU
162
TAGUCHI
for spring and summer
based on estimates
food from Kawamura
rt a/. (1968).
AND
MITSUO
of respiration.
FUKUCHI
grazing, and concentration
For each set of data the correlation
of
is significant
(P < 0.05). Although there is a relatively narrow range of food concentration in our experiments, the index of filtration efficiency varies 20-fold. This might be due to a in the size-range of the phytoplankton cells utilized because the size-range of the zooplankton varied within narrow limits (Table VII ). In other words, when the
difference
size range of phytoplankton is relatively small, the filtration ef%ciency, may increase. This suggestion is supported by an increase in chlorophyll a concentration as the sizerange of phytoplankton decreased during the time course of the spring bloom (Tables VII, rx). There are many interesting aspects to the relation between filtration efhciency, growth rate, and primary and secondary production. The estimated growth rate of zooplankton decreased gradually with the time course of the spring bloom if we ignore the extremely low growth rates in Experiment 3 (Table VIII). Even though the zooplankton community has a relatively low filtration efficiency. the growth rate of the zooplankton community is high. There is no reason why high filtration efficiency should automatically induce high growth rate since growth rate depends upon the quality of the food while filtration efficiency depends only upon the size spectrum of food. assuming that oxygen is never limiting. At the maximum of the spring bloom the ecological efficiency was lowest and subsequently increased to a level about one-tenth of that before it. While the ~ltratio~l efficiency is high at the maximum of the spring bloom, the ecological efhciency is still low. The standing stock of phytoplankton may be controlled when the grazing by, zooplankton is sufficiently high (Martin, 1968; Butler, Corner & Marshall. 1969. 1970): however, in the present work the loss by grazing of phytoplankton is extremely low (Table IX), so there is a low ecological efficiency compared with that in the open ocean (McAllister, 1969). Furthermore, only 1 “d of the nutrients required for primary production is supplied by the excretion of ammonia by the zooplankton community (Table X). If our assumptions are essentially correct, grazing and excretion by zooplankton have little effect on phytoplankton in Akkeshi Bay at the time of the spring bloom,
perhaps
because it is a highly eutrophic
area.
ACKNOWLEDGEMENTS
We are grateful to A. Koyama for identifying of zooplankton species and measuring of their body length. We would like to thank Professors T. Kawamura and S. Nishizawa for their continuing encouragement and Dr R. J. Conover and Dr P. Mayzaud for constructive criticisms.
FILTRATION
RATE
OF
ZOOPLANKTON
DURING
SPRING
BLOOM
I63
REFERENCES J. A. & J. H. STEELE, 1966. Shipboard experiments on the feeding of Ctrlnnrrs finr~zcrrchicus (Gunnerus). In, Son?e confemportrrJ studies in nznrine science, edited by H. Barnes, George Allen and Unwin Ltd, London, pp. 19-35. ANRAKU, M., 1964. Influence of the Cape Cod Canal on the hydrography and on the copepods in Buzzards Bay and Cape Cod Bay, Massachusetts. II. Respiration and feeding. Li~nnol. Occ~~~oyr.. Vol. 7, pp. 195-206. BURNS, C’. W. & F. H. RIGLER, 1967. Comparison of filtering rates of Dophnilr TOS(YIin lake \\ater and in suspension of yeast. Limnol. Oceonogr., Vol. 12, pp. 492-502. BUTLER, E. I., E. D. S. CORNER & S. M. MARSHALL, 1969. On the nutrition and metabolism of zooplankton. VI. Feeding efficiency of Cokrnrrs in terms of nitrogen and phosphorus. J. mar. biol. Ass. U.K., Vol. 49, pp. 977-1001. BUTLER, E. I., E. D. S. CORNER & S. M. MARSHALL, 1970. On the nutrition and metabolism of zooplankton. VII. Seasonal survey of nitrogen and phosphorus excretion by Ctrlrrrrrls in the Clyde sea-area. J. ,?1(lr. hiol. Ass. U.K., Vol. 50, pp. 525-560. CONOVER, R. J., 1956. Oceanography of Long Island Sound, 1952-1954. VI. Biology of Actrrtitr cltrusi and A. tonsa. Bull. Binghtrm Ocrmogr. Coil., Vol. 15, pp. 156-233. CONOVER, R. J., 1959. Regional and seasonal variation in the respiratory rate of marine copepods. Limnol. Ocemogr., Vol. 4, pp. 259-268. CONOVER, R. J.. 1962. Metabolism and growth in C’alnnlrs hFperboreu.9 in relation to its life cycle. Rtrpp. P.-c. R&n. Cons. perrn. in?. Esplor. Mer, Vol. 153, pp. 190-197. CORNER, E. D. S., 1961. On the nutrition and metabolism of zooplankton. I. Preliminary observations on the feeding of the marine copepod Calmus he/,yolundicus (Calanus). J. ,?l(,r. biol. Ass. U.K., Vol. 41, pp. 5-16. FULLER, J. L.. 1937. Feeding rate of Co/onus finnzcrrchicrrs in relation to environmental conditions. Biol. Bull. mar. biol. Lob., Woods Hole, Vol. 72, pp. 233-246. GAIJLD, D. T., 195 I. The grazing rate of planktonic copepods. J. mar. hiol. Ass. U.K., Vol. 19, pp. 695-706. GLIWI~Z, G. M., 1969. The share of algae, bacteria and trypton in the food of the pelagic zooplankton of lakes with various trophic characteristics. Bull. Actrd. pal. Sri. CI. /I Sdr. Sri. Biol.. Vol. 17, pp. 159-165. HAR~~RAVE, 9. T. & G. H. GEEN, 1968. Phosphorus excretion by zooplankton. Linrnol. Owrrwrgr.. Vol. 13, pp. 332-355. HARRIS, E., 1959. The nitrogen cycle in Long Island Sound. Bull. Binghom Oceanogr. Co/l., Vol. 17. pp. 31-65. IKEDA, T., 1970. Relationship between respiration rate and body size in marine plankton animals as a function of the temperature of habitat. Bull. For. Fish. Hohkaido (/nil?., Vol. 21, pp. 91-l 12. IVAN~VA, M. B., 1970. Relations between the food concentration, filtration rate and effectiveness of oxygen utilization by Clodocern. PO/. Arch. HJ’drobiol., Vol. 17, pp. 161-168. KAWAIMURA, T., S. NISHIZAWA, H. ISHII,T. TANAKA & S. UNO, 1968. Excretion, respiration and grazing of zooplankton community. Progress Report, 1967. In, Studies on rhe productiriries of biocoenoses in northern cold wirer, Akkeshi Bay Research Group, edited by S. Motoda, Faculty of Fisheries, Hokkaido University, pp. 21-26 (in Japanese). MARSHALL, S. M. & A. P. ORR, 1955. On the biology of Calmus finmarchicus. VIII. Food uptake. assimilation and excretion in adult and stage V Calm~rs. J. mar. biol. Ass. U.K.. Vol. 23, pp. 495-529. MARSHALL, S. M. & A. P. ORR, 1956. On the biology of Cnltrnrrs fin,nnrchicus. IX. Feeding and digestion in the young stages. J. Inor. biol. Ass. U.K., Vol. 35, pp. 587-603. MARSHAL.L, S. M. & A. P. ORR, 1962. Food and feeding in copepods. Rtrpp. P.-c. Rim. Cms. perru. int. Explor. Mer, Vol. 153, pp. 93-97. MARTIN, J. H., 1968. Phytoplankton-zooplankton relationships in Narragansett Bay. 111. Seasonal changes in zooplankton excretion rates in relation to phytoplankton abundance. Lirnnol. Oceonogr.. Vol. 13, pp. 63-67. MCALLISTER. C. D., 1969. Aspects of estimating zooplankton production from phytoplankton production. J. Fish. Res. Bd Can., Vol. 26, pp. 119-220. ADAMS,
164
SATORU
TAGUCHl
AND
MITSUO
FUKUCHI
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