Respiration and the activity of the respiratory electron transport system in marine zooplankton
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1 Notes 549 Respiration and the activity of the respiratory electron transport system in marine zooplankton AbstracLRespiratory oxygen consumption and respiratory electron transport activity were measured for 15 species and several mixed populations of marine zooplankton. A high correlation ( r > 0.97 ) was found that was only weakly affected by size of the animals and temperature. Regression equations are given for the calculation of respiration from electron transport activity. Although plankton respiration as a parameter in ecosystem models is not as important as primary productivity, it nevertheless must be considered if these models are to attain predictive capability. Presently, respiration methodology lags productivity methodology because rapid direct methods for measuring the respiration of natural phytoplankton or zooplankton communities are nonexistent and because indirect methods are lengthy, insensitive, and inaccurate. The use of specific enzyme reactions as rate indices offers the advantage of speed and facility (Packard et al. 1974). The utility of this approach depends on either proper calibration or knowledge of the regulatory mechanisms of the enzyme reaction. Since our knowledge of enzyme regulation has not developed to the point where an in vivo reaction rate can be predicted from measurements of in vitro enzyme activity, calibration is necessary. As with ATP or nutrient analyses, this is accomplished by demonstrating a high correlation between the easily quantified in- dex (ATP, diazo dye, etc.) and the direct measurement of, for example, living carbon, nitrite, etc. A correlation has been found between respiration and succinate dehyd rogenase activity (SDH) in the fish Menidia rneniclia (Curl and Sandberg 1961) and the brine shrimp Artemia salimz (Pack- ard and Taylor 1968). However, because of its lack of sensitivity the SDH assay has Contribution No. 820 from the Department of Oceanography, C niversity of Washington. This research was supported by Office of Saval Research contract N and by National Science Foundation grants GA 34165Al and GX ( CVEA-12). not been widely used as a11 index of plankton respiration. Since the electron transport svstem ( ETS ) is more closely coupled to the process of oxygen consumption, and since the measurement of ETS activity is simple and sensitive ( Packard 1971), it has been used to provide estimates of oxygen consunlption in the deep sea (Packard et al. 1971)) in phytoplankton (Packard 1971), and in zooplankton (Packard et al. 1974). \Ve present data here on the calibration of the ETS assay with 15 species and several mixed populations of zooplankton collected from the surface waters of Puget Sound, the eastern North Atlantic Ocean, and the eastern tropical North Pacific Ocean. 1Ve thank J. Boucher and H. J. Slinas for the respiration measurements with Calanoicles carinatus and for the opportunity to work on board the RV Jean Charcot. We also thank G. Friederich, D. Harmon, T. Moore, and J. Vidal for assisting with the experiments on some of the Puget Sound species, R. Fernald for the use of the facilities at the Friday Harbor _\larine Laboratory, and C. Johnson and W. \lccarthy for aid in preparing this manuscript. The organisms were collected by bucket from the pier of the Friday Harbor hiarine Laboratory, by net from Puget Sound, or by net aboard the RV T. G. Thompson (Cruise 66) and the RV Jean Charcot ( CINECA II). Respiration rates were measured at in situ temperature by the method of Conover ( 1960). The reagents for the \1 inkler oxygen determination were prepared according to Carpenter ( 1965). Filtered air-saturated seawater was used in all experiments. The bottle size and the number of organisms were selected to ensure a final oxygen concentration in excess of 50% of saturation at the end of the 24-h incubation. ETS activity was then determined at in situ temperature by a tetrazolium reduction method (Packard 1971; Packard et al. 1974). The ETS activities of Calanus pacificus were measured on one group of animals
2 Notes 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 orfianism identifies its location in Fig. 1. The copepodid stages of Calanus pacificus are indicated parenthetically. Stage I rulnplii are indicated (WI). Organism N ETS Respiration Respiration (per animal) (per animal) :ETS Annelida Tomopteris septent2fonazis (a) % i- 2.24' 6.15 i ? 0.29 Chaetognatha Sagitta ezegnns (b) % Arthropoda Amphipoda Parathemisto?aciSiea (C) 10 7 Copepoda CaZanoides carinatus (d) CaZanus pucificus (e9 ) 3 CaZanus pacificus (ev) E CaZanus pa~ific2.4~ (eiv) 15 3" CaZanus pacificus (ei1) 15 2 CaZams pacificus (eni) 15 2 CaZanus sp. (f) 16 3 Epitabidocera amphitrites (9) 10 4 Mixed copepods (h) 27 6 Decapoda Brachyuran larvae (megalops) (i) 16 2 PZeuroncodes pkznipes (j) 23 5 Euphausiacea Euphausiu pacifica (k) 5 NfzmatoseeZis atzantica (1) 1: F 0.6% k t ? k % k 20.8* * 1.05 t ? ' i k k _" G t I- 17.2" 20.9 i 21.2* 1.45 i i I i * k I f ? t i % t ? f c 0.42 Ctenophora Fleurotraehia bachcii (m) i: YY z! 0.41 Coelenterata Leuekartiara oetona (n) 10 3 PhiaZidium gregariwn (0) 13 9 Stomotoea artra (p) k _ k k t i 0.12 Mixed zooplankton (q) t 14.4* * * 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 from the same population. This procedure permitted dry weight measurements after the respiration determinations. The respiration rates and ETS activities of zooplankton from five phyla are presented in Table 1. The ratio of the respiration rate to the ETS activity ranges from 0.54 to 2.16; the three medusoid species fall into the lower part of this range, with ratios significantly lower (P < 0.05) than that for the other groups. At the high end of the range fall some of the copepods: C. carinatus, C. pacificus (stages II and V) and an assemblage of mixed copepods. The data from Table 1 are plotted on a log-log scale in Fig. 1. The regression lines were calculated by two different methods : the broken line is the result of a least squares regression analysis on a logarithmic
3 Notes 851 A 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 1 arge 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 = log ETS ) 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 coeffifor 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
4 s52 Notes Table 2. Regression equations for the relationship between respiratory oxygen consumption (R) and ETS actkity (ETS). N is the number of experiments, Sb is the standard error of the regression coefficient and r is the correlation coefficient, The standard errors of estimate (Sy) for the loglog equations are for the medusae and for the non-medusoid organisms. - Group Regression equation s 33 r Non- R=1.64 ETS Medusae R=0.953 logets-to Medusae Rz0.62 ETS R=0.728 logets+o.o ~~-r- for the non-medusoid organisms (Table 2) indicates that both equations describe the data equally well. The linear equation, however, is preferred for its simplicity. The error of a respiration prediction based on this equation is *34%, calculated from the coefficient of variation of the R : ETS ratio (CV = SD/mean x 100 = 0.57/1.64 X 100). The effect of size on the relationship between ETS activity and respiration in the non-nledusoid group is small, as can be inferred from Fig. 1A and the magnitude of LOG DRY WEIGHT (mg animal- ) Fig. 2. The effects of temperature (h) and \\eight (B) on the ratio of respiration to ETS activ ity ( solid lines ). The data for temperature and \\eight were taken from Tables 1 and 3. The clashed lines superimposed on Fig..2B, representing the data of Ikeda ( 1970 ), show the weight dependence and the temperature dependence of \\Jei,ght specific respiration in marine zooplankton from three regions : Tropical ( line I ), temperate (line II), and boreal (line III). Respiration was measured at 30, l(ic, aud 8OC, respectively, for the zooplankton from each of these three regions. $5 5 Table 3. Zooplankton dry zaeights based on direct mcasrlrements, prlblished data, or conz;ersions as indicated. Species Dry Weight (mg animal-l) 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) Measured in this study. CaZanus pacificus (9) Calanus pacificus (V) Measured in this study. CaZanus pacificus (IV) Measured in this study. CaZanus pacificus (II) Measured in this study. CaZanus pacificus (N I) 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).
5 Notes 853 Table 4. The regression equations describing the dependence of the ratio of R to ETS (Y) on dry weight ( W ) and temperature ( T ) and the m&linear regression equation describing the dependence on both variables are given below. Sy is the standard error of log R : ETS and r is the correlation coefficient. Independent variable None Weight Equation SY r logy=o logy= ogW Temp logy=0.0128t Weight & lpgy= ogw temp T the regression coefficients of the log-log equation. The closeness of the regression coefficient to 1 (0.953) for a suite of data that spans a size range of five orders of magnitude (1 pg animal-l for C. pacificus stage 1 nauplii, to 0.5 g animal-l for PZeuroncodes plunipes) suggests that either the size dependence of both ETS activity and respiration are mathematically equivalent or that the two processes are coupled. Regardless of the explanation, the ratio R : ETS for the non-medusoid organisms appears to be affected only weakly by size. To investigate the size effect more directly, we plotted the ratio of respiration to ETS activity against dry weight (Fig. 2B), using weights both directly measured and taken from the literature (Table 3). The regression line fitted to the data reveals a small decrease (P < 0.05) in the ratio: a 40% change as the dry weight increases over five orders of magnitude. Superimposed on Fig. 2B are the regression lines describing the dependence of weight-specific respiration as measured by Ikeda (1970). At any one temperature the weightspecific respiration can decrease by more than an order of magnitude for a dry weight increase of 104. This variation, in addition to the temperature dependence, complicates predictions of respiration from dry weight; a prediction from ETS activity would be simpler. The regression equation for the size effect on the ratio R : ETS and the equation for the temperature effect and the multiple regression equation for the combined effect of both size and tempera- ture are given in Table 4. The temperature effect alone is negligible (P > 0.10). Although the combined effect of temperature and weight is statistically significant (P < 0.01)) thi use of size and temperature corrected R : ETS ratios rather than a single mean ratio provides only negligible improvement in respiration estimates from ETS activities. Neither weight nor temperature, nor a combination of the two parameters, accounts for an appreciable amount of the total variation of R : ETS. The total unexplained standard deviation of log R : ETS, Sy = (Table 4), is reduced by only 7.4%, 4.7%, and 12.8% when the effects of size, temperature, and both size and temperature are considered, Frederick Theodore T Department of Oceanography University of Washington Seattle References D. King2 Packard3 BANSE, K Net zooplankton and total zooplankton. Rapp. P.-V., Cons. Int. Explor. Mer 153: CARPENTER, J. H The Chesapeake Bay Institute technique for the Winkler dissolved oxygen method. Limnol. Oceanogr. 10: CONOVER, R. J The feeding behavior and respiration of some planktonic crustacea. Biol. Bull. 119: COOPER, L. H. N Phosphorous, nitrogen, iron and manganese in marine zooplankton. J. Mar. Biol. Assoc. U.K. 23 : CURL, H., AND J. SANDBERG The measurement of dehydrogenase activity in marine organisms. J. Mar. Res. 19: DAVIS, C. C The pelagic copepods of the northeastern Pacific Ocean. Univ. Wash. Publ. Biol. 14: FULTON, J A laboratory manual for the identification of British Columbia marine zooplankton. Fish. Res. Bd. Can. Tech. Rep. 55. Hoos, R. A. W Distribution and physiology of zooplankton in an oxygen minimum layer. M.S. thesis, Univ. Victoria. 113 p. IKEDA, T Relationship between respiration rate and body size in plankton animals Present address: Graduate School of Oceanography, Univ. R.I., Kingston Present address: Bigelow Laboratory for Ocean Science, West Boothbay Harbor, Maine
6 854 Notes as a function of the temperature of habitat. Bull. Fat. Fish., Hokkaido Univ. 21: PACKARD, T. T The measurement of respiratory electron-transport activity in marine phytoplankton. J. Mar. Res. 29: ~ D. HARMOK, ASD J. BOUCHER Rekpiratory electron transport activity in plankton from upwelled waters. Tethys 6: , M. L. HEALY, AND F. A. RICHARDS Vertical distribution of the activity of the respiratory electron transport system in marine plankton. Limnol. Oceanogr. 16: , AND P. B. TAYLOR The relationship bet\veen succinate dehydrogenase activ- ity and oxygen consumption in the brine shrimp, Artemia salina. Limnol. Oceanogr. 13 : OhiORI, M Weight and chemical composition of some important oceanic zooplankton in the North Pacific Ocean. Mar. Biol. 3: RAYMOST, J. E. G., ASD S. KRISHSASWAMY Carbohydrates in some marine planktonic animals. J. Mar. Biol. Assoc. U.K. 39: SSEDECOR, G. W Statistical methods. Iowa State. Submitted: 10 October 1974 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 the marine copepod Acartia cluusi relative to egg development time are consistently maintained when these animals are cultured with excess food at 10, 15, and 20 C. Seasonal acclimation effects, lvhich have been shown to affect the egg development of A. clausi, are carried through an entire generation. Generation time or the development time of any postembryonic stage can be calculated from life history data at one temperature and the relationship between egg development at other temperatures regardless of the effect of acclimation. Corkett and McLaren (1970) proposed that under optimal food conditions calanoid copepods molt at intervals which maintain a constant relative relationship to the duration of the egg stage regardless of temperature. If true, this would allow calculation of development time of any stage at any temperature from life history data at one temperature and egg development times throughout the copepod s temperature range. The general applicability of this relationship was challenged by Geiling and Campbell ( 1972)) who observed that the freshwater Calanoid copepod Diaptomus did not follow a simple developmental pattern with temperature and that the relationship between stages did not remain con- 1 Contribution No. 845 from the Department of Oceanography, University of Washington. This study was supported by NSF grant DES to B. W. Frost. stant. Further, Munro (1974) found a broad temperature-independent plateau in the development of some stages of the freshwater cyclopoid copepod, Cyclops vicinus. Both of these papers are conspicuously detailed with respect to the development of many life stages, involving observations of numerous animals at four different temperatures. In contrast, Corkett and Mc- Laren (1970) studied three species (Pseudocalanus minutus, Eurytemora hirundoidxzs, and Temora longicornis) but only in the most superficial way (2 stages/species -eggs and CI, based on the observations of 3 (range l-6) individual copepodids at each temperature). I have re-examined the proposal of Corkett and McLaren (1970) for 6-10 life stages of the marine copepod Acnldia clausi reared at three temperatures. Temperature acclimation affects the egg development of A. clausi by causing the eggs from winteracclimated females ( 10 C ) to develop significantly faster under sullmler conditions (20 C) than eggs from summer-acclimated animals (Landry 1975) ; the effect of acclimation on the development of advanced life stages of this copepod is also investigated. I gratefully acknowledge the assistance of B. Frost in preparing and reviewing the manuscript. This study was carried out at the University of \Vashington Friday Harbor Laboratories. I thank the director and
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