Respiration and the activity of the respiratory electron transport

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					                                                              Notes                                       549

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
                                                Notes                                               851


                             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
s52                                                                           Notes

   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.

    Group           Regression
                     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
as indicated.

      Species                                           Dry Weight                                              Source
                                                       (mg animal-l)

      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).
                                                       Notes                                                        853

   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.
854                                                              Notes

     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