Respiration and the activity of the respiratory
electron transport system in marine zooplankton’
AbstracLRespiratory oxygen consumption not been widely used as a11 index of plank-
and respiratory electron transport activity ton respiration. Since the electron transport
were measured for 15 species and several
mixed populations of marine zooplankton. A svstem ( ETS ) is more closely coupled to
high correlation ( r > 0.97 ) was found that the process of oxygen consumption, and
was only weakly affected by size of the ani- since the measurement of ETS activity is
mals and temperature. Regression equations simple and sensitive ( Packard 1971) , it has
are given for the calculation of respiration been used to provide estimates of oxygen
from electron transport activity.
consunlption in the deep sea (Packard et
al. 1971)) in phytoplankton (Packard 1971),
Although plankton respiration as a pa- and in zooplankton (Packard et al. 1974).
rameter in ecosystem models is not as im-
\Ve present data here on the calibration
portant as primary productivity, it never-
of the ETS assay with 15 species and sev-
theless must be considered if these models
eral mixed populations of zooplankton col-
are to attain predictive capability. Pres-
lected from the surface waters of Puget
ently, respiration methodology lags produc- Sound, the eastern North Atlantic Ocean,
tivity methodology because rapid direct
and the eastern tropical North Pacific
methods for measuring the respiration of
Ocean. 1Ve thank J. Boucher and H. J.
natural phytoplankton or zooplankton com-
Slinas for the respiration measurements
munities are nonexistent and because indi-
with Calanoicles carinatus and for the op-
rect methods are lengthy, insensitive, and
portunity to work on board the RV Jean
inaccurate. The use of specific enzyme re-
Charcot. We also thank G. Friederich, D.
actions as rate indices offers the advantage
Harmon, T. Moore, and J. Vidal for assist-
of speed and facility (Packard et al. 1974).
ing with the experiments on some of the
The utility of this approach depends on
Puget Sound species, R. Fernald for the
either proper calibration or knowledge of
use of the facilities at the Friday Harbor
the regulatory mechanisms of the enzyme
_\larine Laboratory, and C. Johnson and W.
reaction. Since our knowledge of enzyme
\lcCarthy for aid in preparing this manu-
regulation has not developed to the point
where an in vivo reaction rate can be pre-
The organisms were collected by bucket
dicted from measurements of in vitro en-
from the pier of the Friday Harbor hiarine
zyme activity, calibration is necessary. As
Laboratory, by net from Puget Sound, or
with ATP or nutrient analyses, this is ac-
by net aboard the RV T. G. Thompson
complished by demonstrating a high cor-
(Cruise 66) and the RV Jean Charcot
relation between the easily quantified in-
( CINECA II). Respiration rates were mea-
dex (ATP, diazo dye, etc.) and the direct
sured at in situ temperature by the method
measurement of, for example, living carbon,
of Conover ( 1960). The reagents for the
nitrite, etc. A correlation has been found
\1’inkler oxygen determination were pre-
between respiration and succinate dehy-
pared according to Carpenter ( 1965). Fil-
d rogenase activity (SDH) in the fish
tered air-saturated seawater was used in all
Menidia rneniclia (Curl and Sandberg 1961)
experiments. The bottle size and the num-
and the brine shrimp Artemia salimz (Pack-
ber of organisms were selected to ensure a
ard and Taylor 1968). However, because
final oxygen concentration in excess of 50%
of its lack of sensitivity the SDH assay has
of saturation at the end of the 24-h incuba-
’ Contribution No. 820 from the Department of tion. ETS activity was then determined at
Oceanography, C’niversity of Washington. This in situ temperature by a tetrazolium reduc-
research was supported by Office of Saval Re- tion method (Packard 1971; Packard et al.
search contract N-00014-67-0103-00014 and by
National Science Foundation grants GA 34165Al 1974). The ETS activities of Calanus pacif-
and GX 33502 ( CVEA-12). icus were measured on one group of animals
Table 1. Respiration and ETS acticities in marine zooplankton. The number of experiments with
each species as uxll as the incubation temperature used in each series of experiments are tabulated
under N and T. All the data are expressed as mean values; the ETS and respiration data are given in
~1 0, h-’ and each value is accompanied by its standard deviation. The letter associated with each or-
fianism identifies its location in Fig. 1. The copepodid stages of Calanus pacificus are indicated paren-
thetically. Stage I rulnplii are indicated (WI).
Organism N ETS Respiration Respiration
(per animal) (per animal) :ETS
Tomopteris septent2fonaZis (a) 8 5 6.7% i- 2.24' 6.15 i 1.82 0.95 ? 0.29
Sagitta eZegnns (b) 8 3 0.70% + 0.016 0.896 + 0.117 1.25 2 0.16
Parathemisto ?aciSiea (C) 10 7 1.52 F 0.6% 2.49 i 1.08 1.67 i 0.24
CaZanoides carinatus (d) 16 13 0.255 k 0.187 0.472 k 0.324 1.98 + 0.69
CaZanus pucificus (e9 ) 3 0.376 t 0.020 0.590 2 0.019 1.57 * 0.05
CaZanus pacificus (eV) E 0.093 ? 0.010 0.259 k 0.050 2.79 k 0.31
CaZanus pa~ific2.4~ (eIV) 15 3" 0.050 k 0.005 0.086 _" G.007 1.71 I 0.19
CaZanus pacificus (eI1) 15 2 0.019 + 0.000% 0.044 2 0.004 2.24 + 0.28
CaZams pacificus (eNI) 15 2 0.003 2 0.0003 0.004 t- 0.001 1.79 f 0.69
CaZanus sp. (f) 16 3 0.733 + 0.252 0.876 5 0.105 1.27 ? 0.43
Epitabidocera amphitrites (9) 10 4 39.4 k 20.8* 52.6 I- 17.2" 1.45 t 0.49
Mixed copepods (h) 27 6 11.1 + 13.8* 20.9 i 21.2* 2.16 i 0.40
Brachyuran larvae (megalops) (i) 16 2 1.05 t 0.17 1.45 i- 0.19 1.3% t 0.04
PZeuroncodes pkznipes (j) 23 5 117.0 ? 18.8 183.0 i 12.4 1.59 ? 0.18
Euphausiu pacifica (k) 5 5.84 + 3.04' 7.57 I 2.55 1.35 f 0.42
NfzmatoseeZis atZantica (1) 1: 8 3.47 + 4.41 4.78 5 5.31 1.47 -c 0.42
Fleurotraehia bachcii (m) 13 15 1.57 i: 1.04 2.19 YY 1.46 1.44 z! 0.41
Leuekartiara oetona (n) 10 3 3.56 k 0.64 2.89 k 1.34 0.79 t 0.23
PhiaZidium gregariwn (0) 13 9 2.20 +_ 0.38 1.94 + 0.17 0.91 + 0.18
Stomotoea artra (p) 13 36 20.1 k 8.8 10.0 + 2.9 0.54 i 0.12
Mixed zooplankton (q) 24 7 21.0 t 14.4* 31.9 + 22.2* 1.53 + 0.59
* Computed on a per assemblage basis.
' ETS activity was assayed at 35°C and corrected to 8°C using the Arrhenius equation
and an energy activation of 15 Kcal mole-l.
and the respiration rates on another, both significantly lower (P < 0.05) than that for
from the same population. This procedure the other groups. At the high end of the
permitted dry weight measurements after range fall some of the copepods: C. cari-
the respiration determinations. natus, C. pacificus (stages II and V) and
The respiration rates and ETS activities an assemblage of mixed copepods.
of zooplankton from five phyla are pre- The data from Table 1 are plotted on a
sented in Table 1. The ratio of the respira- log-log scale in Fig. 1. The regression lines
tion rate to the ETS activity ranges from were calculated by two different methods :
0.54 to 2.16; the three medusoid species fall the broken line is the result of a least
into the lower part of this range, with ratios squares regression analysis on a logarithmic
ETS ACTIVITY (A liters o2 h -‘animal-’ )
Fig. 1. Respiration rate vs. ETS activity. The data represent 15 species from five phyla of marine
zooplankton; the letter beside each point identifies the associated organism in Table 1. The dashed
lines were calculated from a least squares analysis on the logarithmically transformed data; the solid
lines were constructed from the mean ratio of respiration to ETS activity.
transformation of the data; the solid line is groups is further demonstrated in the log
based on Snedecor’s (1956) model 1A re- transformed data (Table 2, Fig. 1) by a
gression analysis in which the regression 1arge displacement of the y-intercept, as
coefficient is determined by calculating the well as by a significantly lower ( P < 0.01)
mean ratio between respiration and ETS regression coefficient for the medusae. For
activity (R : ETS ) . The data on medusae the medusae, the log-log equation (log R
were treated separately in both regression = 0.728 log ETS + 0.057) describes the
analyses, because the mean ratio of R to data better than does the linear equation.
ETS was significantly lower ( P < 0.01) The higher (P < 0.01) correlation coeffi-
for medusae than for the non-medusoid cients for the log-log equation attest to this.
species. The difference between the two Comparison of the correlation coefficients
Table 2. Regression equations for the relation-
ship between respiratory oxygen consumption (R)
and ETS actkity (ETS). N is the number of ex-
periments, Sb is the standard error of the regres-
sion coefficient and r is the correlation coefficient,
The standard errors of estimate (Sy) for the log-
log equations are 0.075 for the medusae and 0.138
for the non-medusoid organisms.
equation s 33 r
Non- R=1.64 ETS 98 0.058 0.986
Medusae R=0.953 logETS-tO.202 98 0.014 0.989
Medusae Rz0.62 ETS 48 0.029 0.898
R=0.728 logETS+O.O57 48 0.026 0.972
-4 -3 -2 -1 0 1 2 3 4 5
for the non-medusoid organisms (Table 2) LOG DRY WEIGHT (mg animal-‘) $5
indicates that both equations describe the
data equally well. The linear equation, Fig. 2. The effects of temperature (h) and
however, is preferred for its simplicity. The \\eight (B) on the ratio of respiration to ETS ac-
error of a respiration prediction based on tiv ity ( solid lines ) . The data for temperature and
\\eight were taken from Tables 1 and 3. The
this equation is *34%, calculated from the clashed lines superimposed on Fig. .2B, representing
coefficient of variation of the R : ETS ratio the data of Ikeda ( 1970 ), show the weight de-
(CV = SD/mean x 100 = 0.57/1.64 X 100). pendence and the temperature dependence of
The effect of size on the relationship be- \\Jei,ght specific respiration in marine zooplankton
tween ETS activity and respiration in the from three regions : Tropical ( line I ) , temperate
(line II), and boreal (line III). Respiration was
non-nledusoid group is small, as can be in- measured at 30°, l(ic, aud 8OC, respectively, for
ferred from Fig. 1A and the magnitude of the zooplankton from each of these three regions.
Table 3. Zooplankton dry zaeights based on direct mcasrlrements, prlblished data, or conz;ersions
Species Dry Weight Source
Tomopteris septentrionaEis 5.61 Ikeda (1970).
Sagitta elegans 1.43 Omori (1969).
Parathemisto pacifica 1.65 Hoos (1970).
CaZanoides carinatus 0.13 Converted from mean wet Formalin weight using a
dry weight:wet weight ratio of 0.13 (Banse 1962).
CaZanus pacificus (9) 0.179 Measured in this study.
Calanus pacificus (V) 0.044 Measured in this study.
CaZanus pacificus (IV) 0.026 Measured in this study.
CaZanus pacificus (II) 0.010 Measured in this study.
CaZanus pacificus (N I) 0.001 Measured in this study.
EpiZabidocera amphitrites 0.50 Converted from mean length (Davis 1949) using
equation of Fulton(1968).
Brachyuran larvae (megalops) 1.17 Converted from mean wet Formalin weight using
dry weight:wet weight ratio of 0.13 (Banse 1962).
Pleuroncodes planipes 432 T. Whitledge (Personal communication).
Euphausia pacifica 6.36 Hoos (1970).
NematosceZis atlantica 0.91 Converted from mean wet Formalin weight using
a dry weight:wet weight ratio of 0.13 (Banse 1962).
Pleurobrachia bach.eii 11.4 Converted from mean wet volume using dry weight:
wet weight ratio of 0.04 (Cooper 1939; Raymont
and Krishnaswamy 1960).
Table 4. The regression equations describing ture are given in Table 4. The temperature
the dependence of the ratio of R to ETS (Y) on effect alone is negligible (P > 0.10). Al-
dry weight ( W ) and temperature ( T ) and the
m&linear regression equation describing the de- though the combined effect of temperature
pendence on both variables are given below. Sy and weight is statistically significant (P <
is the standard error of log R : ETS and r is the 0.01)) thi use of size and temperature cor-
correlation coefficient. rected R : ETS ratios rather than a single
mean ratio provides only negligible im-
Independent Equation SY r provement in respiration estimates from
ETS activities. Neither weight nor temper-
None logY=O. 190 0.148 - ature, nor a combination of the two param-
Weight logy=-0.0485 1ogW 0.137 -0.387 eters, accounts for an appreciable amount
Temp logY=0.0128T+0.016 0.141 0.327 of the total variation of R : ETS. The total
Weight & lpgY=-0.491 1ogw unexplained standard deviation of log R :
temp +0.0130T+0.014 0.129 0.511
ETS, Sy = 0.148 (Table 4), is reduced by
only 7.4%, 4.7%, and 12.8% when the ef-
the regression coefficients of the log-log
fects of size, temperature, and both size
equation. The closeness of the regression
and temperature are considered,
coefficient to 1 (0.953) for a suite of data
that spans a size range of five orders of Frederick D. King2
magnitude (1 pg animal-l for C. pacificus Theodore T Packard3
stage 1 nauplii, to 0.5 g animal-l for PZeur-
oncodes plunipes) suggests that either the Department of Oceanography
size dependence of both ETS activity and University of Washington
respiration are mathematically equivalent Seattle 98195
or that the two processes are coupled. Re- References
gardless of the explanation, the ratio R :
BANSE, K. 1962. Net zooplankton and total
ETS for the non-medusoid organisms ap- zooplankton. Rapp. P.-V., Cons. Int. Explor.
pears to be affected only weakly by size. Mer 153: 211-215.
To investigate the size effect more directly, CARPENTER, J. H. 1965. The Chesapeake Bay
we plotted the ratio of respiration to ETS Institute technique for the Winkler dissolved
oxygen method. Limnol. Oceanogr. 10: 141-
activity against dry weight (Fig. 2B), us-
ing weights both directly measured and CONOVER, R. J. 1960. The feeding behavior and
taken from the literature (Table 3). The respiration of some planktonic crustacea.
regression line fitted to the data reveals a Biol. Bull. 119: 399415.
small decrease (P < 0.05) in the ratio: a COOPER, L. H. N. 1939. Phosphorous, nitrogen,
iron and manganese in marine zooplankton.
40% change as the dry weight increases J. Mar. Biol. Assoc. U.K. 23 : 387-390.
over five orders of magnitude. Superim- CURL, H., AND J. SANDBERG. 1961. The mea-
posed on Fig. 2B are the regression lines surement of dehydrogenase activity in marine
describing the dependence of weight-spe- organisms. J. Mar. Res. 19: 123-138.
DAVIS, C. C. 1949. The pelagic copepods of the
cific respiration as measured by Ikeda
northeastern Pacific Ocean. Univ. Wash.
(1970). At any one temperature the weight- Publ. Biol. 14: 1-118.
specific respiration can decrease by more FULTON, J. 1968. A laboratory manual for the
than an order of magnitude for a dry identification of British Columbia marine zoo-
weight increase of 104. This variation, in plankton. Fish. Res. Bd. Can. Tech. Rep. 55.
Hoos, R. A. W. 1970. Distribution and physiol-
addition to the temperature dependence, ogy of zooplankton in an oxygen minimum
complicates predictions of respiration from layer. M.S. thesis, Univ. Victoria. 113 p.
dry weight; a prediction from ETS activity IKEDA, T. 1970. Relationship between respira-
would be simpler. The regression equation tion rate and body size in plankton animals
for the size effect on the ratio R : ETS and
the equation for the temperature effect and ’ Present address: Graduate School of Oceanog-
raphy, Univ. R.I., Kingston 02881.
the multiple regression equation for the ’ Present address: Bigelow Laboratory for Ocean
combined effect of both size and tempera- Science, West Boothbay Harbor, Maine 04575.
as a function of the temperature of habitat. ity and oxygen consumption in the brine
Bull. Fat. Fish., Hokkaido Univ. 21: 91-112. shrimp, Artemia salina. Limnol. Oceanogr.
PACKARD, T. T. 1971. The measurement of res- 13 : 552555.
piratory electron-transport activity in marine OhiORI, M. 1969. Weight and chemical compo-
phytoplankton. J. Mar. Res. 29: 235-244. sition of some important oceanic zooplankton
~ D. HARMOK, ASD J. BOUCHER. 1974. in the North Pacific Ocean. Mar. Biol. 3:
Rekpiratory electron transport activity in 4-10.
plankton from upwelled waters. Tethys 6: RAYMOST, J. E. G., ASD S. KRISHSASWAMY. 1960.
213-222. Carbohydrates in some marine planktonic ani-
-, M. L. HEALY, AND F. A. RICHARDS. 1971. mals. J. Mar. Biol. Assoc. U.K. 39: 239-248.
Vertical distribution of the activity of the res- SSEDECOR, G. W. 1956. Statistical methods.
piratory electron transport system in marine Iowa State.
plankton. Limnol. Oceanogr. 16: 60-70.
---, AND P. B. TAYLOR. 1968. The relation- Submitted: 10 October 1974
ship bet\veen succinate dehydrogenase activ- Accepted: 8 April 1975
The relationship between temperature and the development of life stages
of the marine copepod Acartia clausi Giesbr?
Ab.stract--The durations of life stages of stant. Further, Munro (1974) found a
the marine copepod Acartia cluusi relative to broad temperature-independent plateau in
egg development time are consistently main-
tained when these animals are cultured with
the development of some stages of the
excess food at 10, 15, and 20°C. Seasonal ac- freshwater cyclopoid copepod, Cyclops
climation effects, lvhich have been shown to vicinus. Both of these papers are conspicu-
affect the egg development of A. clausi, are ously detailed with respect to the develop-
carried through an entire generation. Gen- ment of many life stages, involving observa-
eration time or the development time of any
postembryonic stage can be calculated from
tions of numerous animals at four different
life history data at one temperature and the temperatures. In contrast, Corkett and Mc-
relationship between egg development at Laren (1970) studied three species (Pseu-
other temperatures regardless of the effect of docalanus minutus, Eurytemora hirundoi-
dxzs, and Temora longicornis) but only in
the most superficial way (2 stages/species
Corkett and McLaren (1970) proposed -eggs and CI, based on the observations of
that under optimal food conditions cala- 3 (range l-6) individual copepodids at
noid copepods molt at intervals which each temperature).
maintain a constant relative relationship to I have re-examined the proposal of Cor-
the duration of the egg stage regardless of kett and McLaren (1970) for 6-10 life
temperature. If true, this would allow cal- stages of the marine copepod Acnldia clausi
culation of development time of any stage reared at three temperatures. Temperature
at any temperature from life history data acclimation affects the egg development of
at one temperature and egg development A. clausi by causing the eggs from winter-
times throughout the copepod’s tempera- acclimated females ( 10°C ) to develop sig-
ture range. The general applicability of nificantly faster under sullmler conditions
this relationship was challenged by Geiling (20°C) than eggs from summer-acclimated
and Campbell ( 1972)) who observed that animals (Landry 1975) ; the effect of accli-
the freshwater Calanoid copepod Diapto- mation on the development of advanced
mus did not follow a simple developmental life stages of this copepod is also investi-
pattern with temperature and that the rela- gated.
tionship between stages did not remain con- I gratefully acknowledge the assistance
of B. Frost in preparing and reviewing the
1 Contribution No. 845 from the Department of manuscript. This study was carried out at
Oceanography, University of Washington. This
study was supported by NSF grant DES 74-22640
the University of \Vashington Friday Har-
to B. W. Frost. bor Laboratories. I thank the director and