where [/max is the specific growth rate in doublings per day and T is ..... by the Gerson Meyerbaum fund for oceanography from the Hebrew. University of ...
Polar Biol (1982) 1:33 - 38
© Springer-Verlag1982
Effect of Temperature on Rate of Photosynthesis in Antarctic Phytoplankton A. Neori and O. Holm-Hansen Scripps Institution of Oceanography, University of California, San Diego, La Jolla, Cal 92093, USA Received 2 October 1981; accepted 10 March 1982
Summary. The rate of photosynthesis of marine antarctic phytoplankton (western Scotia Sea and Bransfield Strait) was determined as a function of temperature, from ambient ( - 0 . 8 ° C to 1.0°C) to 28°C. Photosynthetic rates, based on radiocarbon incorporation during half-day incubations, were increased by as much as 2 × with temperatures up to 7 °C; at higher temperatures the rates decreased rapidly, so that at 28°C the rates were only 3 % of that at ambient temperatures. In antarctic surface waters during the austral summer the rate of photosynthesis by phytoplankton thus is limited by thermodynamic effects on metabolic reactions, in spite of high nutrient concentrations and saturating light levels. The observed rates were in agreement with thermodynamic models of the dependence of phytoplankton growth rate on temperature.
Introduction Antarctic waters south of the Polar Front (Antarctic Convergence) are sufficiently high in nutrients (E1-Sayed 1968; Holm-Hansen et al. 1977) that nutrient concentrations would not be expected to limit phytoplankton growth rates. In spite of high nutrient concentrations and ample light (Franceschini 1978; Holm-Hansen et al. 1977) during at least 6 months each year, phytoplankton biomass is fairly low (0.1 to 1.0 I.tg chlorophyll a/liter) and algal growth rates have been reported to be in the range of 0.05 to 0.5 divisions per day (Bunt and Lee 1970; Holm-Hansen et al. 1977). Although the Antarctic is often thought of as being rich in regard to biological production, primary production rates are moderate, with most investigators estimating rates of approximately 130 to 450 mg C/m2/day (Holm-Hansen et al. 1977; E1Sayed 1970). During the R/V Melville cruise in the Scotia Sea in J a n u a r y - M a r c h of 1981, we had a multi-disciplinary team of investigators studying the distribution of plank-
ton in regard to the physical mixing processes in the upper water column (Holm-Hansen and Foster 1981) and the metabolic activity of plankton as influenced by environmental conditions. One of our objectives was to determine whether the low temperatures prevailing in antarctic waters are important in limiting phytoplankton growth rates, and what effect increased water temperatures would have on primary production. The specific questions of interest to us include: (1) Are Antarctic phytoplankton obligate psychrophiles, or can they also thrive at temperatures not encountered in antarctic waters? (2) How does the rate of photosynthesis respond to moderate increases in temperature? (3) Are cells genetically adapted so that their growth rates are high, in spite of low temperatures, or are their growth rates lower than those of mesophilic organisms in accordance with van't Hoff temperature relationships? In this paper we will be using the term "Antarctic phytoplankton" to apply to phytoplankton populations found south of the Antarctic Convergence (AC). Nutrient and temperature conditions south of the AC are fairly uniform (nitrate, for instance, rarely is less than 20 IxM in surface waters, and surface water temperatures range from about + 5 °C to - 1 . 8 ° C ) as contrasted to much greater variations in nutrient concentrations and temperature north of the AC (Holm-Hansen et al. 1977). The distribution of both zooplankton and phytoplankton species seems to have circumpolar continuity south of the AC (Hardy 1967), with considerable endemism in antarctic waters of phytoplankton and micro-zooplankton (Balech 1970). As the zones of distribution of many planktonic organisms are limited by either the AC or the Subtropical Convergence, most investigators distinguish between Antarctic waters (south of the AC) and Subantarctic waters (between the AC and the Subtropical Convergence); the Antarctic province comprises a relatively uniform biogeographic region as compared to the Subantarctic region (Hedgpeth 1969). It thus seems reasonable to assume (as a working hypothesis) that phyto0722-4060/82/0001/0033/$01.20
34
plankton south of the AC will react fairly similarly to changes in temperature. All available data on phytoplankton growth rates in antarctic waters support this view (Bunt and Lee 1970; Holm-Hansen et al. 1977). Thus, even though the phytoplankton samples used in our investigation were from a limited geographical area, our conclusions regarding phytoplankton response to changes in temperature most likely can be applied to all antarctic waters south of the AC for the Austral summer season.
Materials and Methods Water samples were obtained from 7, 10, or 20 m depths with 30-1 Niskin bottles or f r o m 1 m with a bucket. Three light and one dark bottle (borosilicate glass, 125 ml, with teflon-lined screw caps) were filled and injected with 0.5 or 0.6 ml of 10 ~tCi/ml NaH14CO3 solution. All light bottles were placed in three clear plexiglass cylinders of diameter slightly larger t h a n the bottles. Each cylinder was equipped with water-tight end caps containing hose couplings. Surface sea water was passed through the control cylinder, and temperature-controlled water f r o m two thermostated water baths was passed t h r o u g h the other two cylinders. The entire incubation unit was placed on the open fantail o f the ship. O n s u n n y days the unit was covered with a neutral density screen which attenuated the light reaching the bottles by 45%. A t the beginning o f each experiment the incubation unit was covered with a sheet of black plastic for at least 30 m i n to allow the samples to equilibrate with the experimental temperature. The black plastic sheet was then removed (generally a r o u n d 11.00 local time) to start the light incubation period. The dark bottles were maintained at the appropriate temperatures in a bucket with the outflow of surface water or in the reservoirs of the temperature baths. Temperatures in the incubators were monitored continuously using mercury thermometers in the outflows. At the end of the incubation period samples were filtered t h r o u g h 24 m m glass fiber filters ( W h a t m a n G F / C ) . The filters were exposed to concentrated HC1 fumes in a closed container overnight and the fixed
radiocarbon then measured in a liquid scintillation counter on board ship. Dark values have been subtracted from the corresponding light values in calculation o f photosynthetic rates. Chlorophyll a was determined by filtration of 100 ml of sample through G F / C glass fiber filters, extraction in 7 ml o f absolute methanol ( H o l m - H a n s e n and R i e m a n n 1978), and m e a s u r e m e n t of fluorescence ( H o l m - H a n s e n et al. 1965). Incident light q u a n t a were recorded continuously with an integrating scalar irradiance q u a n t u m meter (models QSR 240 and 250, Biospherical Instruments, Inc., San Diego, California). Light attenuation with depth in the water column was recorded with an underwater quant u m scalar irradiance sensor (model QSP 200). In vivo chlorophyll fluorescence as a function of temperature was measured with a Turner Instruments fluorometer (model 111) equipped with a flow-through door. A closed system was used, with a peristaltic p u m p circulating the sample t h r o u g h a temperature-controlled glass heat exchanger. All components o f this system were covered with a l u m i n u m foil and a black cloth.
Results
Rates of CO 2 assimilation, together with other related data, are shown in Table 1. The assimilation numbers (AN) are comparable with previous data (Burkholder and Mandelli 1965; Bunt 1964; Bunt and Lee 1970; Holm-Hansen et al. 1977). The photosynthetic rates as a function of temperature for all six experiments are shown in Fig. 1A (assimilation numbers) and 1B (rates relative to sample at ambient water temperature). Both these methods of representation show that an increase of temperature from ambient ( - 0 . 8 to + 1.0°C) to somewhere between 4.5 to 7 °C results in a significant increase of CO2 assimilation rates, while above 9 °C the rates are much reduced.
Table 1. Effects of temperature on carbon fixation in antarctic phytoplankton. The lowest temperature in each experiment is the ambient water temperature Experiment
Water sample
Sample incubation
14C fixation
(CPM)
Assimilation no. (~tg C/~tg chla/h)
Depth (m)
Chl. a (gg/1)
Light H o u r s of ( E / m 2 / h ) a light
Average light (E/m2/h)
Temp. (°C)
Dark
Light _+SD
I~g C / 1 / h
1
20
0.6
0.3
6.5
1.7
2
10
0.6
1.3
6.5
3.6
3
1
0.32
0.7
4.3
1.2
4
10
0.45
0.7
7.0
1.8
5
7
0.4
0.7
6.0
1.5
6
20
0.4
0.5
5.8
2.6
1 12 -0.8 7 15 1 4.5 9 0 3.5 17.5 0.7 2.3 28 0.7 3.3
60 73 73 67 113 62 87 81 101 85 142 406 418 359 513 530
1379+ 45 1069+ 19 1797+ 22 3587_+ 12 1036+ 86 1167+ 69 1594___ 12 1301+ 68 2057 _+ 165 2448 _+ 166 1342_+ 135 1984_+ 83 2494 + 266 419 + 9 1954_+ 77 2553 _+ 186
0.55 0.43 0.72 1.46 0.38 0.68 0.93 0.69 0.75 0.91 0.46 0.71 0.93 0.03 0.56 0.79
a This is the average light intensity to which the cells would have been exposed at that depth during the incubation period
0.91 0.71 1.19 2.44 0.64 2.13 2.91 2.16 1.68 2.03 1.03 1.78 2.34 0.07 1.41 1.98
35
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B
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8
12
16
20
24
28
I
I
I
I
I
a
8
12
16
20
24
28
0,0
TEMPERATURE
(°C)
Fig. 1 A , B . Effects of temperature on rates of photosynthesis in antarctic phytoplankton, expressed either as Assimilation numbers (A) or as fixation rates relative to the sample at ambient temperature in each experiment ( B )
It should be noted that both light intensity and ambient water temperature varied considerably from day to day, and hence also between experiments. As both these factors can influence the measured rates of photosynthesis, the assimilation numbers for all samples maintained at ambient temperatures are shown as a function of ambient light intensity (Fig. 2A) and ambient water temperature (Fig. 2B). The decrease in AN at ambient temperatures with increased light intensity (Fig. 2A) indicates that light levels were above the saturating light intensity. Although the decrease in AN from 2.1 at the lowest light intensity to 1.2 at the .highest light intensity suggests marked photoinhibition, this possibility must be tempered with the fact that the AN increased with temperature (Fig. 2B) and that samples exposed to high light intensities were at low temperatures, and vice-versa. One can conclude from these data that the light intensities for all samples (1.15 to 3.6 E/m2/h) were above the saturating light intensity and that there was some photoinhibition with the higher light intensities. This is also in agreement with results of studies by Sakshaug and HolmHansen (in preparation), which show that the saturating light intensity for antarctic phytoplankton is approximately 200 ~t Einsteins/m2/s, which is equivalent to approximately 0.7 E/mE/h. From theoretical analysis of pigment fluorescence (Butler 1978) as well as experimental applications (Fork
CO 2
1976), it appears that chlorophyll a fluorescence is lowest at temperatures where photosynthetic efficiency is highest. We thus attempted to ascertain the optimum temperature for photosynthesis in antarctic phytoplankton by studying in situ chlorophyll a fluorescence over the temperature range of - 0.35 to + 60 °C. In vivo fluorescence decreased about 11% from ambient ( - 0 . 3 5 °C) to +4.5 °C; between 4.5 °C and 60°C, fluorescence remained at a fairly uniform level. This kind of measure-
.c
A
A
B
2 []
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W ~n
EXP NO.
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o
Z 0 J 0 0
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LIGHT INTENSITY
I 2
4 3 (Einsteins/m2/hr)
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o
3 4 5 6
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o
t
~
0
I
TEMPERATURE
(°C)
Fig. 2 A , B. Assimilation numbers for phytoplankton samples incubated at ambient conditions of light (A) and temperature ( B )
36
ment can indicate not only the temperature of highest photosynthetic efficiency but also the cellular system responsible for the changes in efficiency with temperature. Discussion When temperature limits growth by determining metabolic rates, an increase in temperature should result in increased metabolic rates and growth within the temperature range that can be endured by the cells. Data in Table 1 and Fig. 1 show that temperature effects described by the van't H o f f equation may apply to antarctic phytoplankton. It is of interest to examine these photosynthetic rates in terms which permit comparison with phytoplankton from other oceans. In a summary of temperature and growth-rate data with laboratory cultures, Eppley (1972) suggested that upper limits for maximal growth rates were described by the equation [/max = 0 . 8 5 1 ( 1 . 0 6 6 )
T
(1)
where [/max is the specific growth rate in doublings per day and T is degrees centigrade. At 0 °C, gmaxwould thus be 0.851. Holm-Hansen et al. (1977) and Olson (1980) calculated actual g values ([.tact) for antarctic phytoplankton (using 14C and 15N assimilation data, respectively) by use of the equation: [/act
=
1/tl°g2 (CO + AC) Co
(2)
where C O = phytoplankton carbon or nitrogen at start of incubation period, AC = increase in phytoplankton carbon or nitrogen during incubation, and t = fraction of light day. Their calculated values for [/act at sub-zero temperatures were about half of that predicted by applying Eq. 1. It should be noted, however, that Eq. 1 assumes continuous illumination, whereas most field samples have less than 24 hours of illumination per day; the [/act values for natural samples thus have to be increased to compensate for true illumination period in order to allow a comparison with [/maxvalues. When this is done, the ~act values reported by Holm-Hansen et al. (1977) and Olson (1980) come close to (but still slightly below) the values predicted by Eq. 1. We are henceforth using t in Eq. 2 to mean number of light incubation hours divided by 24. It thus seems that specific growth rates of antarctic phytoplankton at ambient temperatures can be approximated by applying Eq. 1 with the appropriate lightperiod corrections. In order to see if the observed photosynthetic rates at elevated temperatures also fit Eq. 1, we have calculated gact at the elevated temperatures with respect to the rate at ambient temperature for each experiment. We are thus assuming that the growth rate for
the ambient temperature lies on the curve predicted by Eq. 1 (~act = mmax) and then seeing how the growth rates ([/act) at higher temperatures agree with that equation. In order to calculate experimental [/act values at the elevated temperatures by use of Eq. 2 it is necessary to know the value of C O(A C is obtained from the radiocarbon data). By assuming that [/act at ambient temperature equals gmax, we can calculate the value for C Oby Eq. 3, which is a rearrangement of Eq. 2: Co -
AC 2 ~maxt -
1
(3)
where [/max is the maximal growth rate for the sample at ambient temperature (in each of the six experiments) as calculated by Eq. 1. The C Ovalues calculated for experiments 2 and 5 are 28 and 26 [/g carbon per liter, as compared to total particulate organic carbon (POC) values of 70 and 50 [/g carbon per liter, respectively (POC was determined in a Hewlett-Packard CHN analyzer on samples concentrated onto Whatman GF/C glass fiber filters). These Co values are reasonable as total microbial biomass-carbon usually accounts for 50°7o- 9 0 % of the POC values (Holm-Hansen and Paerl 1972), and phytoplankton biomass usually accounts for 70% - 90% of the total microbial biomass. The calculated C O values also seem reasonable when compared to estimates based on chlorophyll concentrations (36 and 24 gg C/1 for Exp. 2 and 5, respectively) and on ATP values for Exp. 2 (45 [/g C/1 for total microbial biomass). These latter calculations assume a carbon/Chlorophyll ratio of 60 and a carb o n / A T P ratio of 250 (based on actual determinations of cultures maintained on shipboard at ambient water temperatures). POC data were available only for experiments 2 and 5, and ATP was measured only for experiment 2. The resulting growth rates at all elevated temperatures are shown in Fig. 3, line A. More recently, Goldman and Carpenter (1974) derived a model (Eq. 4) of temperature-limited growth which predicts lower rates than Eq. 1: ~l,max = (5.35 X 109) × e -6472/T°K .
(4)
If this equation is used to derive the [/maxvalues for insertion into Eq. 3, the estimated C Ovalues for Exp. 2 and 5 are 97 and 83 gg C per liter, respectively. The POC, chlorophyll, and ATP data thus indicate that Eq. 1 approximates the actual growth rates in our samples much better than Eq. 4. Line B, Fig. 3, shows the growth rates of samples at elevated temperatures according to the model of Goldman and Carpenter. It is seen from Fig. 3 that the photosynthetic response to elevated temperatures agrees well with both models (compare slopes and Qa0 values of lines A and B) up to 7°C; at higher temperatures the growth rates decrease in an exponential fashion, indicating thermally-induced cell damage or death. The major difference between the two models is in relating growth rates to initial phytoplankton carbon
37 I0 --
-
LINE A p.= 0 . 8 5 1 ( 1 . 0 6 6 ) T * C
~
CO ~K I 1.0 (.9 /
-
~.:(535xl 0 9 ) e - ~
-
Qio = 2 . 0 9 UNE B
o
o-o.o
o _ ~
_~
~
O3
A
A ~AA
A
Z _J rn
A'Z~
A A
0
::k
AMBIENT TEMPERATURE i
I
I
I
I
I
I
I
I
3.33
3.38
3.43
3.48
3.53
3.58
3.63
3.68
0.01
I/T°K
I 28
°
(xlO -3)
I
I
I
I
I
I
I
I
I I II
25 °
20 °
17.5 °
15 °
12 °
9o
6o
4.5 °
2 ° IO0=-I °
TEMPERATURE
(°C)
Fig. 3. Effects of temperature on specificgrowth rates as predicted by Eppley (line A and experimental points, 0) and by Goldman and Carpenter (line B and experimentalpoints, A). See text for details
values. Thus, if our estimates of Co are in error by any significant amount, the effect will be to displace the line vertically, with only a small change in slope. Although temperatures above 7 °C cause a decrease in photosynthetic rates (data in Table 1), it is interesting to note that CO2 incorporation continues at measurable rates up to the highest temperature used in our experiments (28 ° C). We cannot say if this is caused by a general reduction in photosynthetic rates by all the phytoplankton species in our samples, or if various species have different temperature responses. Additional experimental methods, particularly long-term culture experiments, are needed in order to document which species, if any, can grow at elevated temperatures. It is also possible that some species have the capacity to adapt to higher temperatures, which means they would be facultative psychrophiles. Our short-term radiocarbon data eventually should be reconciled with the demonstration that some antarctic fresh water (Holm-Hansen 1964) and marine phytoplankton (Gillan 1981) species can be maintained in cultures at approximately 20 ° C. The decrease of in vivo fluorescence of chlorphyll a with increasing temperature from ambient to 4.5 °C may be an indication that the increased efficiency of photosynthesis originates in the light reaction site (Butler 1978; Fork 1976; Schreiber et al. 1976). The stability of the in vivo fluorescence with further temperature increases indicates stability of the photosystems at those elevated
temperatures and implies that the decreased efficiency of photosynthesis at high temperatures in our samples originated in other processes in the cells not affecting the light reactions. It is of interest to compare the response of antarctic phytoplankton to elevated temperatures with other types of organisms. Eq. 1 predicts that the growth rate at - 0 . 8 ° C will be 25% of that at 20°C. Bacterial growth rates at - 0.8 °C in the Antarctic were 50% of the growth rates determined at 20 °C in waters of California, corresponding to Q10 values of about 1.4 (Farooq Azam, personal communication). Bacteria in the Antarctic thus appear to have smaller Qa0 values from 20°C to - 1 °C as compared to phytoplankton. In marine fish, the level of liver protein synthesis follows a curve with a Qa0 of 2.5, but in antarctic fishes the activity is 2 - 3 times higher than predicted by such a curve, as are other metabolic rate measurements (Smith and Haschmeyer 1980). There are reports on comparable growth rates between related benthic organisms in antarctic and temperate seas which are living at widely different temperatures (George 1977). It thus seems that phytoplankton as a group is unique in its genetic inability to compensate for the growth-inhibiting effects of low temperatures. As found in other cold water habitats (Sorokin and Konovalova 1973; Bunt 1968; Bunt and Lee 1970; Olson 1980) and as is generally the case in most phytoplankton habitats (Eppley 1972), we find that maximal growth rates were measured at temperatures a few degrees higher than the ambient temperature. In fact, this is common to many groups of organisms. Growth or activity curves versus temperature for bacteria (Hodson et al. 1981; Morita et al. 1977) and animals (Haschemeyer 1980) from Antarctica follow the same pattern as phytoplankton data. It is interesting to compare this temperaturephotosynthesis response to the temperature regime in the Southern Ocean. Most of the surface water south of the AC has an eastward and northward component to its flow. Although the classical textbook diagrams depict this north-easterly moving water as downwelling at the AC to form the Antarctic Intermediate Water, such a flow pattern is not necessarily continuous, but may be sporadically interrupted. At such times, antarctic surface waters might flow "across" the usual convergence zone, and eventually mix with Subantarctic water, thus exposing the entrapped planktonic organisms to temperatures between 6 °C and 10 ° C. Phytoplankton cells thus might normally be exposed to temperatures in the range of - 1 . 8 ° C (found at stations close to the continent) to about 5°C (at the Antarctic Convergence) and occasionally to up to 10 °C when they are transported north of the AC. Such a mixing of antarctic and subantarctic surface waters might account for the distribution of some phytoplankton species both north and south of the AC (Balech et al. 1968; Cassie 1963). Further studies are required to determine if such species are actively growing in subantarctic waters, or if they merely represent vestigial populations from colder waters.
38
If temperature is the main limiting factor for rate of photosynthesis in antarctic phytoplankton in summer, one would expect to find an increase in assimilation numbers in the warmer waters closer to the Antarctic Convergence. Data in the literature support this view, as HolmHansen et al. (1977) report an average A N of 0.77 at subzero temperatures and 1.02 at 3 ° C - 4 ° C . Also, Saijo and Kawashima (1964) report an average A.N. of 1.14 at sub-zero temperatures, and 1.66 at 2 ° C - 4 ° C . Such temperature effects on photosynthetic rates will also affect the magnitude of primary production available to the rest of the food chain. The result on net primary production would depend upon the effect that elevated temperatures have on respiration rates and on nutrient supply as affected by water column stratification. During the Melville cruise, T. Ikeda measured oxygen uptake rates in the Scotia Sea at a station where the phytoplankton biomass was high (5 txg chlorophyll a/liter). His measured rate of 0.05 Ixl O2/~g C / d a y at 1.0°C indicates a Qa0 of approximately 2.17 in comparison to the average respiration rate for phytoplankton of 0.25 ~tl O2/~g organic C / d a y at 2 2 ° C (Hobbie et al. 1972). It thus seems that temperature effects on photosynthesis and respiration are more or less parallel, so that a doubling of phytoplankton growth rates will also double the amount of net primary production available to herbivorous zooplankton. Such temperature effects on photosynthesis and respiration must be incorporated into any mathematical models of the dynamics of the food web in the Southern Ocean. Acknowledgements. We thank C. A. Paden, T. Ikeda, and D. Long for valuable help on board ship. This work was supported by National Science Foundation Grant DPP79-21295. Amir Neori was supported by the Gerson Meyerbaum fund for oceanography from the Hebrew University of Jerusalem, and by the Solar Energy Research Institute, Contract No. XK-0-9111-1 (W. H. Thomas, P. I.).
References Balech E, E1-Sayed SZ, Hasle G, Neushnl M, Zaneveld JS (1968) Primary productivity and benthic marine algae of the antarctic and subantarctic. American Geographical Society, New York (Antarctic Map Folio Series, Folio 10) Balech E (1970) The distribution and endemism of some antarctic microplankters. In: Holdgate MW (ed) Antarctic ecology, vol 1. Academic Press, New York, pp 143 - 147 Bunt JS (1964) Primary productivity under sea ice in antarctic waters. I. Concentrations and photosynthetic activities of microalgae in the waters of McMurdo Sound, Antarctica. In: Lee MO (ed) Biology of the antarctic seas (Antarctic research series 1). American Geophysical Union, Washington DC, pp 1 3 - 26 Bunt JS (1968) Some characteristics of microalgae isolated from antarctic sea ice. In: Llano GA, Schmitt WL (eds) Biology of the antarctic seas (Antarctic research series II). American Geophysical Union, Washington DC, pp 1 - 14 Bunt JS, Lee CC (1970) Seasonal primary production in antarctic sea ice at McMurdo Sound in 1967. J Mar Res 28:304-320 Burkholder PR, Mandelli EF (1965) Carbon assimilation of marine phytoplankton in Antarctica. Proc Natl Acad Sci USA 54:437- 444 Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Ann Rev Plant Physiol 29:345 - 378 Cassie V (1963) Distribution of surface phytoplankton between New Zealand and Antarctica, December 1957. Sci Rep Commonw Transantarctic Exped 1955 - 1958 7:1 - 11
E1-Sayed SZ (1968) On the productivity of the southwest Atlantic Ocean and the waters west of the Antarctic Peninsula. In: Llano GA, Schmitt WL (eds) Biology of the antarctic seas III (Antarctic research series 11). American Geophysical Union, Washington DC, pp 15 - 47 E1-Sayed SZ (1970) On the productivity of the Southern ocean (Atlantic and Pacific sectors). In: Holdgate AW (ed) Antarctic ecology, vol 1. Academic Press, New York pp 119- 135 Eppley RW (1972) Temperature and phytoplankton growth in the sea. Fish Bull 70:1063 - 1085 Fork DC (1976) Temperature dependence of chlorophyll a fluorescence in algae and higher plants in relation to changes of state in the photosynthetic apparatus. Carnegie Institute Year Book 75:472-477 Franceschini GA (1978) Solar radiation over the Weddell and Ross Seas. Antarct J US 13:172- 173 George RY (1977) Dissimilar and similar trends in antarctic and arctic marine benthos. In: Dunbar MJ (ed) Polar oceans. Arctic Institute of North America, Calgary, Alberta, pp 391-407 Gillan FT (1981) Lipids of aquatic ecosystems. PhD Thesis, University of Melbourne, Australia Goldman JC, Carpenter EJ (1974) A kinetic approach to the effect of temperature on algal growth. Limnol Oceanogr 19:756- 766 Hardy A (1967) Great Waters. Harper and Row, New York, pp 494 - 496 Haschemeyer AEV (1980) Temperature effects on protein metabolism in cold-adapted fishes. Antarct J US 15:147-149 Hedgpeth JW (1969) Distribution of selected groups of marine invertebrates in waters south of 35 °S latitude. Antarctic Map Folio Series, Folio 11. American Geographical Society, New York, pp 1 - 9 Hobbie JE, Holm-Hansen O, Packard TT, Pomeroy IR, Sheldon RW, Thomas JP, Wiebe WJ (1975) A study of the distribution and activity of microorganisms in ocean water. Limnol Oceanogr 17:544- 555 Hodson RE, Azam F, Carlucci AF, Fuhrman JA, Karl DM, HolmHansen O (1981) Microbial uptake of dissolved organic matter in McMurdo Sound, Antarctica. Mar Biol 61:89- 94 Holm-Hansen O (1964) Isolation and culture of terrestrial and freshwater algae of antarctica. Phycologia 4:43- 51 Holm-Hansen O, Lorenzen CJ, Holmes RW, Strickland JDH (1965) Fluorometric determination of chlorophyll. J Cons, Cons Perm Int Explor Mer 30:3 - 15 Holm-Hansen O, Paerl HW (1972) The applicability of ATP determinations for estimation of microbial biomass and metabolic activity. Mem Ist Ital Idrobiol Dott Marco de Marchi Pallanza Italy 29 (Suppl): 149-168 Holm-Hansen O, El-Sayed SZ, Franceschini GA, Cuhel RL (1977) Primary production and the factors controlling pbytoplankton growth in the Southern Ocean. In: Llano GA (ed) Adaptations within antarctic ecosystems. Gulf Publishing Co, Houston, Texas, pp 1 1 - 5 0 Holm-Hansen O, Riemann B (1978) Chlorophyll a determination: improvements in methodology. Oikos 30:438- 447 Holm-Hansen O, Foster TD (1981) A multidisciplinary study of the Eastern Scotia Sea. Antarct J US (in press) Morita RY, Griffiths RP, Hayasaka SS (1977) Heterotrophic activity of microorganisms in Antarctic waters. In: Llano GA (ed) Adaptations within antarctic ecosystems. Gulf Publishing Co., Houston, Texas, pp 9 9 - 113 Olson RJ (1980) Nitrate and ammonium uptake in antarctic waters. Limnol Oceanogr 25:1064- 1074 Saijo Y, Kawashima T (1964) Primary production in the Antarctic Ocean. J Oceanogr Soc Jpn 19:22-28 Schreiber U, Colbow K, Vidaver W (1976) Analysis of temperaturejump chlorophyll fluorescence induction in plants. Biochem Biophys Acta 428:249 - 263 Smith MAK, Haschemeyr AEV (1980) Protein metabolism and cold adaptation in Antarctic fishes. Physiol Zool 53:373- 382 Sorokin YI, Konovalova IW (1973) Production and decomposition of organic matter in a bay of the Japan Sea during the winter diatom bloom. Limnol Oceanogr 18:962-967
