Biomass and respiratory ETS activity of microplankton in the Barents Sea ROSA MARTINEZ Martinez. R. 1991: Biomass and respiratory ETS activity of microplankton in the Barents Sea Pp. 193- 200 in Sakshaug. E . , Hopkins. C. C . E. & 0ritsland. N. A. (cds.): Proccedings of the Pro Mare Symposium on Polar Marine Ecology, Trondhcim, 12-16 May 1990. P d u r Research l o ( / ) . The activity of the respiratory electron transport system (ETS) of microplankton was measured in the Central Barents Sea during summer 1988. I n vitro ETS activity increased with assay temperature between 0 and 12°C. as reported for other enzyme systems in plankton. The higher in situ activities were observed near the surface (upper 10-25 m) and werc associated with chlorophyll o maxima. Respiratory activity in the upper 60 m accounted for 4&W% of the total column respiration. The activities (&lo0 m) were lower than oxygcn consumption rates reported in the Canadian Arctic, mainly due to lower phytoplankton biomass. They were higher than ETS activity measured in the Weddcll Sea (Antarctic Ocean). A high detrital versus total microplankton mass accounted for the low activity related to particulatc organic carbon (POC). In general. the levels of respiratory ETS activity were in the range reported for temperate oligotrophic oceanic regions. ''@poLAR\~S<'' Rosa Martinez. Departurnento d e Ciencias v T k n i c a s del A g u a . Uniuersidad d e Canrabria. E-39005 Sarrtander, Spain (revised June 1991). Introduction Direct measurements of respiration are scarce compared with the wealth of data on primary production. In contrast to photosynthesis, res- piration is a process common to all organisms, and occurs throughout the whole water column. The microplankton fraction has been shown t o be the most metabolically active in different ocean regions (Williams 1981; Packard & Williams 1981; Mann 1982; Williams 1984; Packard 1985a). Oxygen consumption by respiration is mostly due to oxidative phosphorylation, driven by the respiratory electron transport system (ETS), and the measurement of the activity of this system yields the maximum potential respiration (Pack- ard 1971, 1985a). Data for real-time instan- taneous rates of respiratory activity in ocean regions can be obtained through measurement of ETS activity. This method facilitates the measure- ment of large numbers of samples and the deter- mination of very low respiration rates, while avoiding the need for incubations (Packard 1985b). Both growth and metabolic rates in plankton are limited by low temperatures (Packard et al. 1975; Neori & Holm-Hansen 1982). Adaptation of organisms to low temperatures can be achieved through biochemical mechanisms. Somero (1969) decrease in the Ea at near-zero temperatures in cold-adapted marine organisms. Chabot (1979) postulated an increase in mitochondria1 oxidation under lower growth temperature, involving enzyme increase. There is no conclusive evidence of these mechanisms in microplankton (Packard et al. 1975; Li et al. 1984; Tilzer et al. 1986). and there are no published data on ETS-temperature relationships in Arctic microplankton, that could contribute to clarify this question. The Central Barents Sea experiences during the summer oligotrophic conditions, i.e. low chlorophyll a concentrations and nutrient recyc- ling (Rey & Loeng 1985; Wassmann 1989; Wassmann et al. 1991). Therefore, low biomasses and metabolic rates are to be expected. This study was undertaken during the R/V (3.0. SARS cruise to the Central Barents Sea in July 1988. Its main objective was to provide data on respiratory ETS activity in Arctic microplankton that can be com- pared with ETS activity and respiration rates reported from polar and other latitudes, and with primary production and other metabolic rates. Study area Three stations were chosen which represent three and Hochachka & Somero (1971, 1973) found a zones in the area: Station 1 (73.5"N.. lYE), situ- 194 Rosa M a r t i n e z ated in Atlantic Water. close to the southern edge of the Polar Front, with temperatures ranging from -1°C t o 7°C and salinities from 34.5 t o 3 5 ; Station 2 (76.7"N, 32.5"E). located at the Polar Front. in Arctic Water. with temperatures from -2°C to 1 .@C and salinity from 32.5 to 3 s ; Station 3 (72.3"N. 30.5"E), well south of the Polar Front. perature, T,,, is t h e assay temperature (both in degrees K ) and R is the gas constant. Depth-integrated biomass and E T S activity were calculated by integration of single depth values according to the equation: " T ( X ) = E [ c x l i- xl+l)/2] * ('I+{ - '1) in Atlantic Water. with coastal water influence (temperature 3°C to 8.2"C, salinity 34.5 t o 34.8). where X, = v a l u e of the variable a t the depth zi. Material and methods Results Microplankton samples were taken at three sta- Enzyme kinetics tions with Niskin bottles at 12 to 16 depths, from surface to about 300 m. T h e water samples were screened through a 240 pm net t o eliminate larger zooplankters. Filtration was d o n e o n Whatman G F / F glass fiber filters. T h e filters with cells were frozen in liquid nitrogen until assaying. 5 to 10- liter samples were filtered for E T S assays, and 290 ml for particulate organic carbon ( P O C ) and nitrogen (PON). Chlorophyll a was measured o n board with a Turner Designs fluorometer using acetone as extractant. Nitrate and ammonium were measured on board with a Technicon Autoan- Respiratory ETS activity increased from 0 to 12°C in the two experiments. T h e mean activation energy for this temperature range, calculated from an Arrhenius plot of the results, was 11.5 ? 0.6 Kcal mole-'. and this was t h e value used to calculate in situ respiratory rates of all the samples that were routinely assayed at 10°C. Q l o for the 0 to 10°C range was 1.6. T h e reaction was linear with time for the first 15min. of incubation a t all incubation tem- peratures. Consequently, the time used for all the sample incubations was 15 min. alyser, and particulate organic carbon a n d nitro- gen were measured with a Carlo E r b a C H N - Biomass and actiuity elemental analyser. The respiratory E T S activity of the samples was analyzed with the Packard (1971) and Kenner & Ahmed (1975) enzyme assay. A time and tem- perature kinetics study was performed on two occasions prior to assaying. For this. a large water sample (60 I) was taken from the chlorophyll maximum layer, thoroughly mixed and fractioned in 6 aliquots of 10 1 each, that were subsequently filtered and frozen in the same way as t h e samples. Assays were run in duplicate for each aliquot, at 6 different temperatures: 1. 5. 7 , 8, 10 and 12°C. Several incubation times were used for each assay: 5, 10, 15, 20 and 2 5 m i n . This was done t o cal- culate the enzyme activation energy that should be used when converting activities from a single incubation temperature at which t h e assays were run to in situ activity, according t o the equation Table 1 summarises t h e results of biomass and activity variables at t h e three stations. Fig. 1 represents the vertical distribution of the biomass variables. T h e M o m zone was considered as the euphotic zone according t o the chlorophyll a distribution. Nitrate and ammonium profiles at Stations 1 and 2 are shown in Fig. 2 (nitrate and ammonium data were unavailable a t Station 3). A strong nitracline developed a t 2 M 0 m depth, where nitrate concentrations ranged from zero to 10 mmole Nitrate was exhausted at the surface of Atlantic as well as Arctic waters. Chlorophyll concentrations a t Stations 1 and 3 were low, corresponding t o the post-bloom stage. The peak of Station 1 was situated at the nitra- cline, about 25 m , and amounted t o 0.3 mg m-3. Station 2 showed t h e features of a bloom situation (Rey et al. 1987) with t h e chlorophyll peak located ETS(in situ) = ETS(assay) at 12 m depth, just above t h e nitracline, although I t represented only 3 mg m-3. Mean chlorophyll exp[Ed'l'Tds' - l'T's)'R1 a concentration was a n o r d e r of magnitude higher where E, is the activation energy of the enzyme at Station 2 (0.58 mg m-3) than Station 1 reaction (in Kcal mole-'). T,, is the in situ tern- (0.059 mg IT-^). Biomass and respiratory E T S activity of microplankton in the Barents Sea 195 Table 1. Mean values of biochemical variables f o r the three stations. Variable Station Mean S . D . Min. M a x . n POC (mg m3) PON (mg m - I ) Chla (mg m - 3 ) ETS (ml 0 2 m - 3 h-I) POC/Chla (w/w) (0-100 m) ETSIChla (m102 mg-' h - ' ) (0-100 m) C/N (at/at) C-SP. ETS (d-') 1 2 3 All 1 2 3 All 1 2 3 All 1 2 3 All 1 2 3 All 1 2 3 All 1 2 3 All 1 2 3 All 113 142 233 155 13.4 16.7 23.4 17.2 0.06 0.60 0.20 0.29 0.25 0.47 0.51 0.40 2536 342 1404 1424 5.11 0.87 2.39 2.69 12.1 11.4 12.7 12.0 0.027 0.033 0.030 0.030 69 127 106 111 10.8 16.4 10.9 13.4 0.06 0.94 0.22 0.60 0.25 0.78 0.37 0.5 2103 222 I I46 1097 4.01 0.55 0.52 2.50 3.7 2.0 1.4 2.7 0.013 0.020 0.017 0.017 49 54 70 49 4.1 5.5 6.1 4.1 0.01 0.02 0.01 0.01 0.05 0.06 0.17 0.05 1179 105 365 105 0.85 0.23 I .60 0.23 7.4 7.7 10.4 7.4 0.008 0.01 1 0.010 0.008 235 499 41 1 499 39.7 64.2 40.0 64.2 0.20 3.26 0.61 3.26 0.87 3.10 1.23 3.10 6780 814 3406 6780 14.50 2.00 3.12 14.50 19.6 15.8 15.6 19.6 0.048 0.068 0.056 0.068 16 1s 1 1 42 I 6 1s I 1 42 16 IS 11 42 16 15 1 1 42 8 9 6 25 8 9 6 25 16 15 11 42 16 15 I 1 42 POC and PON distributions (Fig. 1) varied among the stations. At Station 1 they showed peaks in the upper 5 0 m , just above the ammonium peaks, with concentrations of 236 and 40mg m-3, respectively. Increases i n POC and PON did not show any correspondence with increases in chlorophyll, which implies that they were probably related mainly to microhetero- trophs and/or detrital matter. Station 2 exhibited the highest single-depth POC and PON maxima, 499 and 64 mg m-3, corresponding to the chloro- phyll maximum. Maximum POC and PON con- centrations at Station 3 were 410 and 19 mg m-3, respectively, at 50 m depth, clearly below the chlorophyll maximum, which was located at 20 m. Fig. 3 shows in situ ETS activity and carbon- specific ETS activity. The activity was highest in the chlorophyll maximum at the three stations. suggesting that most of the microplankton meta- bolic activity takes place in the upper 40 m and is mainly due to phytoplankton (and possibly also to micrograzers). Maximum values were 0.9, 1.3 and 3 . l m l O2 m-3 h-', at Stations 1, 2 and 3, respectively. Minimum activities occurred at intermediate depths (about 100 m) and a slight increase was observed at Station 1 near the bottom, probably due to an increase of bacterial biomass. At Station 1, ETS activity showed good cor- relations with POC, PON and chlorophyll (r2 > 0.6). The correlations were highest at Sta- tion 2: r2 = 0.7 for POC; r' = 0.8 for PON and r' = 0.9 for chlorophyll. At Station 3, the activity was only correlated with chlorophyll (r2 = 0.9) and not with POC or PON. (All correlations had P < 0.001). POC and PON were strongly 196 Rosa M a r t i n e z 0 1w h E f u ,"m D 300 FIR I . Depth profiles of the hiomass variahlcs. POC. PON and chloroph!il u ' U = Station 1 ; X - X = Station 2; A-A = Station 3 . correlated at this station (r' = 0.97) and chloro- phyll-independent, which further indicates that an important proportion of the particulate organic matter was detrital or microheterotrophic. C,/N (at/at) ratios had a mean value of 12. T h e ratios were highest at Station 3 . suggesting the existence of more detrital material. Significant differences ( P c O . 0 5 ) were found for the C/N ratio between Station 3 (all values) and the other two stations. POC/Chl ratios were high d u e to the pre- dominance of heterotrophic organisms and detritusduring summer. as compared with a POC/ Chl ratio of 59 for phytoplankton during the spring bloom (Rey unpubl. obser.). In the chloro- phyll maximum at Station 2. the ratio had a mini- Fig. -7. Dcpth profiles of nitrate and ammonium at Stations 1 and 2: C. = Station I : X - x = Station 2 Biomass and respiratory ETS actiuity of microplankton in the Barenrs Sea 197 a iaa - E v r c n 8 200 Fig. 3. Depth profiles of ETS activity (ETSA) and carbon-specific ETS activity (C-specific ETSA): x-x = Station 2; A-A = Station 3. 0-4 = Station 1; 300 E T S activity, rnl.02rn-’h-’ C-specific E T S activity, h-] mum value of 105, which indicates a moderately high proportion of phytoplankton in the total microplankton biomass. ETS activity was converted to carbon units (mg C m-3 h-l), using a respiratory quotient RQ = 1 (Packard 1979; Simpkins 1986; Shaffer 1987). The result was divided by POC con- centration to find the (potential) carbon-specific respiratory rate, or carbon respiratory turnover, in (time)-‘ units. The carbon respired ranged from 0.02 to 1.4 mg C m-3 h-l (mean = 0.22 mg C m - 3 h-l). The carbon-specific rate (Fig. 3) ranged from 0.01 to 0.07 h-l and was highest in the chlorophyll maximum, as were both biomass and absolute ETS, suggesting that at that depth the living biomass was both more abundant and more metabolically active. Depth-integrated values of biomass and actiuity Integral column values for the biomass and activity variables are summarised in Table 2. Sta- tion 1 showed the lowest depth-integrated chloro- phyll and ETS activity. POC and PON were similar at Stations 1 and 2 (26 and 23 g C rn-2; 3 and 2.6 g N m-*) and higher at Station 3: 43.4 g C m-2 and 4 g N m-?. Chlorophyll a was highest at Station 2: 61 mg m-2. ETS activity showed an increase in the Stations 1-2-3 sequence: 0.7, 0.8 and 1.1 g C m-* d-I. C/N ratio (atoms) of the integrated water column was 9 for Stations 1 and 2 and 11 for Station 3. Table 2 also shows the integral values for the 0-60 m water column, and the percentage of the total column contained in it. The distributions of biomass and activity at Station 2 were different from Stations 1 and 3, Table 2. Depthintegrated values of biochemical variables. In parentheses. percentage of the total column value contained in the upper 60 m. ~ STA Depth POC Chl a ETSA C/N C/Chl ETS/Chl c - s p ( m ) d-I) d-I) ( d - l ) no. range (g m-’) (mg m - l ) (gC m - ? (at/at) (w/w) (gCgChl-’ ETS ~ 1 &60 9.3 (35%) 5.5 (52%) 0.27 (39%) 8.2 206 49.0 0.03 0-340 26.4 10.6 0 . 6 9 8.8 2480 62.8 0 . 0 3 2 0-60 9.8 (42%) 54.5 (90%) 0.51 (62%) 7.6 1 80 9.4 0.05 &250 23.3 60.8 0.82 8 . 8 383 14.0 0.04 0-255 43.4 4 . 0 1.10 10.9 1685 42.7 0.03 3 0-60 17.3 (40%) 20.6 (79%) 0.49 (44%) 13.6 840 23.8 0.03 198 Rosa Martinez which exhibited strongly stratified water masses, and where 45% of POC. 73% of P O N . 89% of chlorophyll and 62% of E T S activity took place above 60 m. Ratios between depth-integrated variables (Table 2) were calculated for the 6 0 upper m and the total column. T h e euphotic zone of Station 2 had the lowest C/N ratio ( 7 . 6 a t / a t ) , chlorophyll- specific P O C (180 g/g), P O N (43 g/g) and E T S activity (9.4 g C g Chla-' d-I) and the highest carbon-specific E T S activity (5.2% d-I). indi- cating that this water mass was the richest in phytoplankton and protein. and the most meta- bolically active. Discussion The in vitro E T S activity increased with tem- perature in the assayed interval (0-12"C), showing a similar effect to that reported for other enzyme systems in cold-water organisms. Activation energy (E,) was 11.5 Kcal m o l e - ' , similar to the E, = 12 reported by Neori & Holm-Hansen (1982) for photosynthesis of Antarctic phyto- plankton at near-zero temperatures, and lower than the mean value (E, = 16 Kcal mole-') found by Packard et al. (1975) for E T S activity in mic- roplankton from several latitudes. However, tem- peratures in their study ranged between 9 and 28°C and did not include polar zones. E, in t h e present study falls in lower part of their range. This suggests that E, in cold-water microplankton is at the lower end of responses t o naturally occur- ring temperatures, as postulated for photo- synthesis and growth of polar phytoplankton (Neori & Holm-Hansen 1982; Li et al. 1984; Harrison & Platt 1986; Tilzer et al. 1986). However, bacterial growth in the Antarctic ocean was double of that predicted and had lower Q l o than phytoplankton (1.4 versus 2) for the -1- 20°C temperature interval (Neori & Holm-Han- sen 1982). In this study. Q I , , = 1.6 (G12"C) poss- ibly reflects a variety of responses in the populations that compound the microplankton. The ETS activity measured is a potential res- piration rate. and can be converted to actual oxygen consumption ( R ) by applying a factor derived from simultaneous R and E T S activity measurements done on mixed plankton popu- lations. Some calibrations (Packard & Williams 1981: Williams 1984; Packard 1985a; Vosjan & Nieuwland 1987) yield values of about 3 for the ETS/R ratio. However, these studies have been made on temperate microplankton from eutrophic surface waters. Although E T S activity and respiration a r e usually well correlated in a given area or plankton community (Packard & Williams 1981), R / E T S ratio can vary with dif- ferent plankton contributions or seasons (see Hobbie et al. 1972). R / E T S ratios increase with increased bacterial contribution to overall res- piration since bacteria a r e usually more meta- bolically active than o t h e r organisms (Williams 1984; Azam & Fuhrman 1984; Harrison 1986). Also. organisms in cold environments seem to use a larger proportion of their ETS for actual respiration (Jansky 1963). Additional problems relate to the long incubations needed to determine oxygen consumption with the micro-Winkler technique (Williams & Jenkinson 1983): this could promote bacterial growth inside the incu- bation bottles, causing an apparent increase in respiration. These a r e reasons why E T S activity results have been directly reported here without conversion t o oxygen consumption. The E T S activities found in this study for the 100 upper m range between 0.5 to 100 mg 0 2 m - 3 d - ' (mean value 13 mg O2 m-' d-I), which is in the range found for oligotrophic oceanic regions (Williams 1984). Integrated daily rates for the upper lOOm were 1 . 7 g O2 m - ? d-I and 2 . 7 g O2 m-? d-I for the whole water column. Williams (1984) quoted respiration rates in Antarctic mic- roplankton (0-100 m) ranging from 0 t o 16 mg O 2 m - 3 d - I , but FTS activity in the Weddell Sea (Martinez & Estrada 1991) was higher: 0.2 t o 5 3 m g O2 m-3 d - I . These values would range between o n e and three-fold those quoted by Wil- liams, when applying an ETS/R ratio of l to 3. Vosjan & Olanczuk-Neyman (1991) reported ETS activity of 2-200 mg O 2 m - 3 h-' in Admiralty Bay, Antarctica. Harrison (1986) found in the High Canadian Arctic (0-100 m ) a mean value of 60 mg O 2 m-3 d-I and integrated values (100 m) of 4-9g O2 m - ? d - ' . E T S activity in this study was higher than in the Weddell Sea and lower than respiration in the Canadian Arctic. Harrison's (1986) results were five-fold higher than in the present study, the main reason prob- ably being the higher living biomass in the Canadian Arctic samples. Chlorophyll u in the surface ( M o m ) waters of the Canadian Arctic ranged from 0.74 to 8 m g r K 3 , whereas at the Barents Sea stations they ranged from 0.05 to 3.3 mg m3. Respiration/Chl ratio in the Canadian Arctic (calculated from data from Harrison 1986) Biomass and respiratory ETS activity of microplankton in the Barents Sea 199 was 1.7mg O 2 mg Ch1-l h-l, and ETS/Chl in this study was similar, 1.9mg 0 2 mg Chl-' h-l. However, assuming that respiration is lower than ETS activity, the calculated ratio sets an upper limit for the R/Chl a ratio in the Barents Sea. ETS/Chl ratios reflect the relative contribution of autothrophs to total microplankton respiration. In phytoplankton-dominated zones, such as upwelling systems, ocean fronts or chlorophyll maximum layers, the ratio is low, and increases away from these zones. The ratio was 0.7 mg O2 mg Chl-I h-' at the chlorophyll maximum at Station 2, and increased to 2 mg O 2 mg Chl-' h-' at the bottom of the euphotic zone at the same station. The range of this ratio was similar in the Weddell Sea during spring (Martinez 1989; Martinez & Estrada 1991). In the Western Med- iterranean Sea the ETS/Chl ratio ranged from 0.3 mg O2 mg Chl-I h-l (chlorophyll maximum and Almeria-Oran Front) and 5 mg 0 2 mg Chl-' h-' (oligotrophic central basin) (Martinez et al. 1990; Martinez unpubl. data). The ETS activity, converted t o carbon and day units, had a mean value of 5 mg C m-3 d-', with a range of 0.6-33.6mg C m-3 d-l. The carbon- specific rate, or (potential) respiratory carbon turnover, was 0.01-0.07 d-' with a mean value of 0.03 d-', and the integral column value ranged between 0.03 and 0.04 d-l. This means that 3 to 4% of the POC present is potentially consumed each day by respiration. This rate is in the same range as the rate observed in sediment trap material in the same region during the same cruise, between 40 and 300 m depth (Wassmann et al. 1991). C/N ratios were similar: 11 in sedi- menting versus 12 in suspended matter, indicating similar organic matter. This is in agreement with the characteristics of recycled production in sum- mer in the region (Wassmann 1989; Wassmann et al. 1991). Respiratory turnover rate of carbon in Barents Sea microplankton in summer was a fifth of the rates found in the Weddell Sea in spring: 0.02 to 0.05d-' with a mean of 0.17d-I (Martinez & Estrada 1991), in spite of lower temperatures (-1.7 to 2°C). The reasons probably are the high living/dead organic matter ratio and high bac- terial contribution in the Weddell Sea (Boldrin pers. comm.; Delille 1989), with C/N ratios of 6.5, close to C/N = 5.7 reported for marine bac- teria (Mann 1982). Vosjan & Nieuwland (1987) found rates of 0.12 d-' in Antarctic waters, and 0.3 d-' in the North Atlantic during the spring bloom, and much higher values, averaging 0.9 d-I, in tropical waters at temperatures between 10 and 27°C. High detrital/living ratios together with low temperatures account for the low carbon-specific enzyme activity found i n the Barents Sea during summer. Respiratory ETS activity of microplankton can be compared with existing data on primary pro- duction by phytoplankton in the Barents Sea by Rey et al. 1987. Their estimation of annual pro- duction was 69 g C m-2, taking place only during six months. We can assume that the ETS activities measured in this study are maintained during the same six months (a low estimation), and that respiration in the colder months is negligible. On basis of data from the more pelagic Stations 1 and 2, the carbon potentially respired would average 140 g C m-2 for the six-month period. Using the R/ETS = 0.3 ratio, this would correspond to 47 g C m-2. Assuming that the numbers given by Rey et al. estimate net production of the micro- plankton community, then gross production, by adding microplankton respiration, would be between 116 (taking R = 0.3 ETS) and 209 g C m-2 (taking R = ETS). This means a respiration of between 40% and 70% of gross primary pro- duction. Although this is a rough estimate, it provides an approach to estimate the range and order of magnitude of the production-respiration relationship in microplankton in the Barents Sea. These results show that most of the respiratory activity of microplankton in the Barents Sea occurred in the upper layers (<60m) and was correlated with phytoplankton biomass. Ranges of respiratory ETS activity, as well as column- integrated values, were higher than those reported from the Antarctic (Williams 1984; Mar- tinez & Estrada 1991) and lower than respiration in other Arctic regions (Harrison 1986). It has been postulated that Arctic microplankton res- piration may be substantially higher than that in the Antarctic. The results of this study do not support this hypothesis. My results rather provide evidence of the similarity of function between microplankton communities of Arctic and tem- perate oceanic areas. Acknowkdgernenrs. - I am indebted to E. Sakshaug for the opportunity to participate in a Pro Mare cruise. H . R. Skjoldal, as the cruise leader, provided logistic support and cooperation. and allowed me to use the chlorophyll and nutrient data measured on board. The help provided by the staff at the Institute of Marine Research in Bergen is appreciated. Thanks are extended to the Department of Microbiology, University of Bergen, for allowing me to use their CHN-analyzer. Comments 200 Rosn Martinez and suggestion5 o f E Srikshdiig. T T. Pdckard a n d 1 5 5 0 anon!- rnous r e \ i c u c r \ are appreci.itcd. 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