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Photosynthetic response to temperature of marine phytoplankton along a latitudinal gradient (16°N to 74°N)
I)ccp-Sca II.c',,caidl. Vol ),2, No. I I, pp. 1381 Io 1391. UI85. Ih'inlcd m (;rcal Brilain.
0198 1114~9/85$3 {111+ II.llll (~ 1985 Pergamon Press IAd.
Photosynthetic response to temperature of marine phytoplankton along a latitudinal gradient (16°N to 74°N) W. K. W. LI* (Received 1 April 1985; in revised form 3 June 1985;accepted 6 June 1985) Abstract--Photosynthesis-temperature relationships for natural phytoplankton assemblages were established by measuring the uptake of H ~4CO3in freshly collected seawater samples incubated for 2 h across a shipboard laboratory temperature gradient. The minimum, optimum and maximum temperatures for photosynthesis, as well as the extent of photosynthetic change per unit temperaturc change in the suboptimal range, all decreased from low to high latitude. The empirical mathematical model of RATKOWSKVetal, (1983, Journal of Bacteriology, 154, 1222-1226) provided a good fit to the data.
INTRODUCTION
FOR MANYplants, the response to changes in an environmental condition depends on both their genotype and phenotype. Thus the conditions prevailing in the natural habitat and during growth are important determinants of the response. For example, plants native to and growing in cold environments generally have minimum, optimum and maximum temperatures (so-called cardinal temperatures) for photosynthesis that are lower than the respective temperatures in plants native to and growing in warmer environments (BERRY and BJORKMAN, 1980). Additionally, plants may have the ability of acclimating (phenotypically) to different temperatures. Thus, the cardinal temperatures for photosynthesis of a cold-native may be increased if the plant is grown at a higher temperature. Conversely, the cardinal temperatures of a warm-native may be decreased if growth is at a lower temperature (BERRYand BJORKMAN, 1980). The extent to which such acclimation proceeds is itself genetically determined. In the case of unicellular algae, such features of temperature adaptation have been confirmed by experimentation with monoclonal laboratory cultures. Genotypic adaptation is evident when the temperature response is compared between warm-water and cool-water clones of given species (BRAARUD, 1961; GUILLARDand KILIIAM, 1977; ttULBURT, 1982; KRAWIEC, 1982). Phenotypic adaptation is evident when the temperature response for a given clone is compared at different acclimation (growth) temperatures (ARUGA, 1965; SHERIDANand ULIK, 1976; LI and MORRIS, 1982). The question to be considered in this paper is whether marine phytoplankton in nature also exhibit a photosynthetic response to temperature that is dependent on the temperature of their habitat. The answer to this cannot be directly derived from laboratory studies * Marine Ecology Laboratory, Bedford Institute of Oceanography, Department of Fisheries and Oceans, Dartmouth, Nova Scotia, Canada B2Y 4A2. 1381
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of cultured clones for various reasons. First, almost every sample of phytoplankton from the sea is a multispecies, muiticlonal assemblage. Since there is genetic variability in the response to temperature (BRANDetaI., 1981), the response exhibited by the assemblage as a whole may not resemble that of any particular clone. Second, there are many factors which can affect the temperature response that would have to be laboriously specified in culture studies (but that would be given in a fresh phytoplankton sample collected and assayed at sea). Such factors would include the conditions of light intensity, day length, salinity, nutrient supply and temperature during growth. In this paper 1 report the results of shipboard experiments in which photosynthesis-temperature relationships for natural phytoplankton assemblages were established by measuring the uptake of HHCO~ in freshly collected samples incubated for a short time across a shipboard laboratory temperature gradient. MATERIALS AND METIIODS
Experimental procedures" Experiments were conducted on board CSS Hudson in August and September 1983 during a cruise in the eastern Canadian arctic (cruise 83-023) and in December 1984 during a cruise in the Caribbean Sea and the Atlantic Ocean (cruise 84-049). Seawater was collected using a pump sampler system (HERMAN el al., 1984). The dates, locations and depths of sampling as well as the temperature and chlorophyll a content of the samples are given in Table 1. A major impediment to the field study of temperature responses in phytoplankton has been the difficulty of operating unwieldy temperature gradient incubators on research vessels. Most experimentors have therefore relied on separate thermostated water-baths, the number of which in any study is usually 3 or 4 (YENTSCHelaI.,1974; LI and PLA'Vr, 1982; NEORI and HOLM-HANSEN, 1 9 8 2 ; JACQUES, 1983; LI et al., 1984) and rarely exceeds 6 or 7 ( A R U G A , 1965; HARRISand PICCININ, 1 9 7 7 ; HARRIS, 1978). Obviously, the data resulting from these experiments are grossly inadequate to describe fully the response across the entire biokinetic range. We have recently overcome this problem by a combination of some simple modifications to a commercially available temperature gradient incubator and the downscaling of sample volume (to 1 ml) required to measure H t4CO~ uptake in this instrument ILl and DICKIE,1984). The measurement of light-dependent H ~4CO~ uptake (photosynthesis) as a function of Table 1. Descriptive information on phytoplankton samples
Date
7 Dec. 11 Dec. 14 Dec. 15 Dec. 10 Aug.
1984 1984 1984 1984 1983
23 A u g . 1983 I0 Sept. 1983
Latitude IN)
Longitude (W)
Depth (m)
Temperature (°C)
Chlorophyll a(~g I i)
I,,,(W
16o44.5 ' 29°50.0 ' 35°37.1 ' 36o54.5 ' 64°09.4 '
66"48.6' 77018.9 ' 75013.5 ' 74049.0 ' 57"12.6'
10 10 10 10 l0
27.5 22.6 15.9 14.4 3.5
(I.10 0.24 2.28 1.79 1.15
99 174 47
0.96 0.78 0.99
74°07.0 , 72003.6 '
81°54.0 ' 68018.4 '
25 28
0.0 -I. I
1.116 6.41
55 47
I).99 0.98
* See Methods for explanation.
m
-')*
P,~//',,,*
Photosyntheticresponseto temperatureof marinephytoplankton
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temperature has been described (LI and DICKIE, 1984). Briefly, 1.0 ml subsamples of seawater radiolabelled with NaHI4CO3 (47.1 mCi mmol -I, NEC-086H, New England Nuclear; final activity of about 5 to 50 laCi m1-1 seawater) were measured into optically clear, plastic incubation chambers (No. 4804 tissue culture chamber/slide, Lab-Tek Products) placed in a temperature gradient incubator (Model 675, Scientific Industries Inc.). A pair of cool-white fluorescent lamps provided 68 W m-2 of incident photosynthetically active radiation. Samples were incubated in the temperature gradient for 2 h. Radiolabelled plankton were collected by vacuum filtration onto 0.2 lam Nuclepore membranes using 3 filtration manifolds, each capable of handling 12 samples simultaneously (1225 Sampling Manifold, Millipore Corp., Bedford, MA). Each filter was rinsed twice with l0 ml of freshly filtered seawater (
To be assured that 68 W m -2 was appropriate for the measurement of light-saturated rates of photosynthesis (i.e. neither too low to be limiting nor too high to be inhibiting), the following analysis was done. In five out of seven experiments (Table 1), B. D. IRWIN (unpublished observations) measured HI4CO~ uptake as a function of irradiance at the in situ temperature in a shipboard laboratory light-gradient incubator (PtArr et al., 1980; PLATFand GALLEGOS,1980). The resulting data were fit by non-linear regression to the photosynthesis-light model of PLATret al. (1980). From this, it was possible to estimate the irradiance at which photosynthesis was maximum (/m), the rate of photosynthesis at 1,,, (P,,), and the rate of photosynthesis at 68 W m -2 (Pt,8). In these experiments, there was only one case (15 December, 1984) for which the ratio of Pt,~ to P,,, was slightly less than unity (Table l). Data analysis
Photosynthesis-temperature data were fit to the empirical mathematical model of RATKOWSKYet al. (1983) by non-linear regression according to the Gauss-Newton method (BARD,1974) using a computer: P = f(T) g(T),
(1)
f(T) = [[~(T- T~in)] 2
(2)
g(T) = [l - exp{~,(T- Tmax)}]2,
(3)
where and where P is the light-saturated rate of photosynthesis (units = lag C lag Chl a -~ h-l); T is the temperature (units = °C); Tm~. and Tm,~xare the minimum and maximum temperatures, respectively, at which P is zero; [3is a parameter related to the extent of change in P for unit change in T below the optimum temperature [units = (lag C lag Chl a -~ h-~) L/2 °C-I]; and ~, is a parameter related to the relative change in P for unit change in T above the optimum temperature (units = °C-~).
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Ll
Mathematically, P assumes positive finite values at values of T that are less than Tmi, or greater than Tm~x. This biological impossibility is of no concern if attention is restricted to Tmi. ~< T ~< Tm,x. Within this range, the temperature (T,,pt) at which P is optimum (Poor) is uniquely defined. RESULTS
The results of experiments conducted at the lower latitudes (cruise 84-049) and at the higher latitudes (cruise 83--023) are shown in Figs I and 2, respectively. In going from cold to warm waters, there was an incrcasc in all three cardinal tcmpcraturcs (Table 2, Fig. 3). In all cases, Toot was closer to Tmaxthan to Tmi,. For arctic phytoplankton, Toot was much higher than in situ temperature. There was an approximate I°C increase in Toot for every 2°C increase in the in situ temperature (Fig. 3) so that for Caribbean phytoplankton, Toot
/ 27"5° C 1.0
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22"6° C
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TEMPERATURE ("C) TEMPERATURE (*C) Fig. ]. Normalized photosynthesis--temperature curves from experiments performed on cruise 84-049. Numbers in panels indicate in situ temperature. Measurements of P within each experiment arc normalized to the value of Popt for that particular experiment. The curves represent the statistical best-fit of the Ratkowsky model to the data (see Methods). The model parameters arc given in Table 2.
;o
Photosyntheticresponse to temperature of marine phytoplankton
3.5oc
1385
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TEMPERATURE
2~
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3o'
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Fig. 2. Normalized photosynthesis-temperature curves from experiments performed on cruise 83-023. Numbers in panels indicate in situ temperatures. Refer to Fig. 1 legend for explanation of curves.
was the same as the in situ temperature. For Tmi,, there was an approximate I°C increase for every I°C increase in the in situ temperature (Fig. 3). The same was true for Tm~xbut only up to an in situ temperature of about 14°C. At temperatures above this, Tm,,x appeared to remain constant at about 35°C (Fig. 3). Values of 13 (Table 2) were positively correlated with in situ temperature (r -- 0.77, P < 0.05). For the sake of comparison against a more familiar measure of the degree to which a biological process depends on temperature, Table 2 also lists the Arrhenius activation energy, E,, (RABINOWITCH,1956). Values of E,, were estimated from the slope of the regression of lnP on I/T in the suboptimal temperature range of each experiment. Such regressions explained at least 76% of the variance. Although the relationship between 13 and E, is non-linear and temperature-dependent (13 ~ - ( T - T m i , ) -l [A exp(-Ea/RT)]ll2), the two parameters were correlated (r = 0.76, P < 0.05). Values of y (Table 2) were uncorrelated with in situ temperature (P > 0.6).
Photosynthetic response to temperature of marine phytoplankton
1387
The Arrhenius equation has been extensively used in phytoplankton research (GoLDMAN and CARPENTER, 1974) which has mainly been concerned with responses in the suboptimal temperature range. Originally developed from the chemical theory of absolute rates for elementary reactions, the model is only empirical when applied to a biological reaction sequence as complex as photosynthesis. Although the Arrhenius equations can be extended to cover the entire biokinetic range (JOHNSONet al., 1974; MOHRand KRAWIEC, 1980), the model of RATKOWSKVet al. (1983) was chosen in the present study for thc following reasons. Although strictly empirical in nature, the Ratkowsky model not only fits the data well (Figs 1 and 2), but it also is expressed in parameters which are easily identified with biological concepts. The exception is Tmin for psychrophiles (RA'rKOWSK¥ et al., 1982, 1983). In cases where Train is lower than the freezing point of seawater, Tm~n has to be regarded as a characteristic temperature of no metabolic significance. Due to mechanical problems with the incubator during the arctic cruise, the lowest temperatures achieved during measurements of photosynthesis were always a few degrees above in situ temperatures (Fig. 2). The values estimated for 13 and Train in thesc experiments must therefore be regarded as based on extrapolations (using the Ratkowsky model) of measurements at higher temperatures. In earlier work in which we measured photosynthesis of samples incubated in four water baths thermostated at separate temperatures +5°C from ambient, our best estimate for E, based on data pooled from 12 experiments was 16.9 kcal mol -I (LI et al., 1984). The values of 15.1 and 11.1 kcal mol -l for the samples of 23 August and 10 September, 1983 respectively (Table 2) were not greatly dissimilar to the earlier value. However, it is difficult to judge the reliability of the extrapolated low temperature response of the remaining arctic sample (10 August, 1983): the values of both E,, and Tmi, were very low (Table 2). In spite of the reservations with which values of 13and Tm~,,for arctic samples must be viewed, it is clear that Tmin, T,,pt and Tm~x all increased with in situ temperature (Fig. 3). For Toot, this adaptive nature was noted previously (LI, 1980). In particular, ARUGA(1965) demonstrated a seasonal covariation of T,,pt with water temperature for freshwater phytoplankton in a pond in the University of Tokyo campus. Furthermore, the seasonal data of ARU6A (1965) and the latitudinal data in this paper (Fig. 3) both indicate a close correspondence between Topt and in situ temperature when the latter is high, but a divergence between the two temperatures when in situ temperatures are low. In several species of higher plants, the change in Toot also does not fully match the change in growth temperature (BERRYand BJORKMAN,1980; BERRYand RAISON, 1981). The slope of about 0.5 for the Topt vs in situ temperature relationship in marine phytoplankton (Fig. 3) was the same as that in Alaskan mosses (OECHEL, 1976). Our results show that multispecies assemblages of phytoplankton in the ocean, like clonal isolates cultured in nutrient-replete media in the laboratory, have a photosynthetic response to temperature that is dependent on the temperature of growth. All P-T curves obtained so far have only one optimum each. It is therefore possible to consider the assemblage as a physiological unit in the way that it is done so when discussing photosynthesis-irradiance relationships. This contrasts with natural bacterioplankton assemblages, some of which display heterotrophic activity-temperature response curves that have more than a single optimum (ROMANENKO, 1982; LI and DICKIE, 1984). The temperature response of photosynthesis across the entire biokinetic range is not the result of a single chemical reaction (JOHNSONet al., 1974). Increasing temperature accelerates the reactions which both enhance and depress photosynthesis. At temperatures less than Toot, those reactions that enhance photosynthesis are dominant; at
1388
w.K.W. Lt
temperatures greater than Toot, those that depress photosynthesis are dominant. This overall process can be modeled simply by subtracting an Arrhenius equation for the photosynthetic-depressing processes from one for the photosynthetic-enhancing processes (DEAN and HINSHELWOOO,1966; MOHR and KRAWiEC, 1980). However, the Ratkowsky model is a multiplicative one. It is the result of multiplying a continually increasing function, i.e. f(T) (equation 2) with a continually decreasing function that is scaled from 0 to 1, i.e. g(T) (equation 3). As T---~ Train, g(T) --~ 1 so that P - * f ( T ) . An interesting feature of the Ratkowsky model is that Toot depends on Tmin, Tm,,xand 7 but not on 13.This is shown as dP - 2 13fU2(T)g(T) - 2"ff(T)gl/2(T) [1 - gl/2(T)], dT
(4)
when dP/dT = O, the factor 2132can be eliminated so that 0 = (Toot - Tmin)g(Topt) - ~'(Toot - Train)2gl/2(Topt)[1 - gl/2( Toot) ].
(5)
Although I have not been able to obtain an explicit analytical solution to Toot, it is clear from equation (5) that Topt depends on Tmin, Tmaxand ~,but not on 13.From this it is implied that changes in Top, come about, not by change in the suboptimal rates of photosynthesis [which are most likely under the control of rate-limiting enzymes such as ribulose-1, 5bisphosphate carboxylase (BJORKMANand PEARCY,1971; Ll et al., 1984)], but by changes in Train, Tma,, and 7. Recent reviews that discuss the factors controlling these three parameters include CHRISTOPHERSEN(1973), INGRAHAM(1973), INNISSand INGRAttAM(1978), AMELUNXENand MURDOCK(1978), BERRYand BJORKMAN(1980), ARAGNO(1981), BERRY and RAISON(1981), STEPONKUS(1981) and GRAHAMand PATI'ERSON(1982). It is only a mathematical feature of the empirical Ratkowsky model that 13has no influence on T,,pt; but it is an intriguing biological possibility worth pursuing. The parameter 13conveys information about the extent of photosynthetic change arising from an increase of temperature in the suboptimal range. It is correlated with E, which conveys the same information. For Phaeodactylum tricornutum, E,, of light-saturated photosynthesis was found to be the same whether cells were grown at 5, 10, 15 or 25°C (Ll and MORRIS, 1982). For freshwater phytoplankton assemblages in Lake Ontario, QI. (a measure similar to E~) was also found to be the same at different seasons (HARRISand PICCININ, 1977). However, for the marine phytoplankton studied here, 13 and E,, were correlated with in situ temperature (Table 2). Although the values of E,, for arctic phytoplankton (Table 2) were similar to those of many other plants (RABINOWITCIt, 1956; BJORKMANand PEARCY, 1971), the values of E,, for the lower latitude phytoplankton (Table 2) appeared quite large. In arctic phytoplankton, the E,, for P and ribulose-1, 5bisphosphate carboxylase (RUBPC) activity have been found to be similar, indicating that RUBPC may be important in controlling the rate of photosynthesis at suboptimal temperatures (Lt et al., 1984). In contrast, SMmt and PLAT1"(1985) found that the E,, for RUBPC activity was significantly lower in phytoplankton in the tropics than in the arctic. Thus, in tropical phytoplankton, the greatly dissimilar values of E,, for P (reported here) and for RUBPC activity (reported by Smith and Piatt) suggest that RUBPC may not be directly important in the photosynthetic response to temperature changes in the suboptimal range. Another feature sometimes observed in thermally adapted phytoplankton is that the light-saturated rate of photosynthesis remains constant over a range of growth tempera-
Photosynthctic rcsponsc to tclnpcraturc of nlarille phytoplankton
1389
tures. In other words, the P vs in situ temperature plot is a horizontal line (so-called perfect compensation). This was found to be the case in Phaeodactylum tricornutum at 10, 15 and 25°C (LI and MORRm, 1982). For natural asscmblagcs of phytophmkton, plots P vs in situ temperature seldom yield a horizontal line. This was also the case in the present set of experiments. This was most likely because P at any one temperature depends on the diel rhythm (MACCAULLand PLATr, 1977; HARDINGet al., 1982), light history (YENTSCItand LEe, 1966; BEARDALLand MORRIS, 1976), cell size and species composition (MALONE, 1971; DURBINet al., 1975; GLOVER, 1980; CO'rEand PLA'Fr, 1983) and nutrient conditions (T)toMAS, 1970; GLOVER, 1980). The ecological implications of this study appear straightforward. In terms of photosynthesis, phytoplankton at high latitudes are not sensitive to slight increases in their habitat temperature. They have relatively low 13values and live at temperatures far from Toot and Tm~,~. On the other hand, low latitude phytoplankton are relatively much more sensitive to any change in habitat temperature. As they are at or near Topt, a slight temperature increase will rapidly bring them near Tmax,while a temperature decrease will reduce P by a relatively large extcnt because of high 13values. Acknowledgements--I thank B. D. Irwin for unpublished information, P. M. Dickie for assistance in the experiments, Dr. E. P. W. Home for assistance in the mathematics, and D. Rudderham for assistance in computing. Drs T. Platt, J. C. Smith and W. G. Harrison read the manuscript. REFERENCES AMELUNXENand A. L. MURDOCK(1978) Microbial life at high temperatures: mechanisms and molecular aspects. In: Microbial life in extreme environments, D. J. KUSHNER,editor, Academic Press, New York, pp. 217-278. ARAGNOM. (1981) Responses of microorganisms to temperature. In: Physiologicalplant ecology, Vol. 1, O. L. LANGE, P. S. NOBEL, C. B. OSMONDand H. ZIEGLER, editors, Springer-Verlag, Berlin, pp. 339-369. ARUGA Y. (1965) Ecological studies of photosynthesis and matter production of phytoplankton 1. Scasonal changes in photosynthesis of natural phytoplankton. Botanical Magazine, Tokyo, 78,280--288. BARD Y. (1974) Nonlinear parameter estimation. Academic Press, New York, 332 pp. BEARDALLJ. and I. MORRIS(1976) The concept of light intensity adaptation in marine phytoplankton: somc experiments with Phaeodactylum tricornutum. Marine Biology, 37, 377-387. BERRY J. and O. B.IORKMAN(1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology, 31,491-543. BERRY J. and J. J. RAISON(1981) Responses of macrophytes to temperature. In: Physiologicalplant ecology, Vol. 1, O. L. LANGE,P. S. NOBEL, C. B. OSMONDand H. ZIEGLER, editors, Springer-Verlag, Berlin, pp. 277-338. BJORKMAN O. and R. W. PEARCY (1971) Effect of growth temperature on temperature dependence of photosynthesis in vivo and on CO2 fixation by carboxydismutase in vitro in C 3 and C4 species. Carnegie Institution of Washington Yearbook, 70, 511-520. BRAARUDT. (1961) Cultivation of marine organisms as a means of understanding environment influences on population. In: Oceanography, M. SEARS,editor, American Association for the Advancement of Scicnce, Washington, pp. 271-298. BRANDL. E., L. S. MURPHY,R. R. L. GUILLARDand H.-t. LEE ( 1981 ) Genetic variability and differentiation in the temperature niche component of the diatom Thalassiosira pseudonana. Marine Biology, 62, 103-110. C|IRISTOPHERSENJ. (1973) Basic aspects of temperature action on microorganisms, In: Temperature and life, H. PRECHT, J. CHRISTOPHERSEN,H. HENSELand W. LARCHER,editors, Springer-Verlag, Berlin, pp. 3--59. COT~ B. and T. PLATr (1983) Day-to-day variations in the spring-summer photosynthetic parameters of coastal marine phytoplankton. Limnology and Oceanography, 28, 320--344. DEANA. C. R. and C. HINSHELWOOD(1966) Growth, function and regulation in bacterial cells, Clarendon Press, Oxford. 439 pp. DURBIN E. G., R. W. KRAWIECand T. J. SMAYDA(1975) Seasonal studies on the relative importance of different size fractions on phytoplankton in Narragansett Bay (USA). Marine Biology, 32, 271-287. GLOVERH. E. (1980) Assimilation numbers in cultures of marine phytoplankton. Journal of Plankton Research, 2, 69-79.
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SMITHJ. C. and T. PLATr (1985) Temperature responses of ribulose bisphosphate carboxylase and photosynthetic capacity in arctic and tropical phytoplankton. Marine Ecology Progress Series, in press. STEPO_~:KUSP. L. (1981) Responses to extreme temperatures. Cellular and sub-cellular bases. In: Physiological plant ecology, Vol. 1, O. L. LANGE, P. S. NOBEL, C. S. OSMONDand H. Z1EGLER, editors, SpringerVerlag, Berlin, pp. 371--402. TtlOMAS W. H. (1970) On nitrogen deficiency in tropical Pacific oceanic phytoplankton: photosynthetic parameters in poor and rich water. Limnology and Oceanography, 15,380-385. YENTSCHC. S. and R. W. LEE (1966) A study of photosynthetic light reactions, and a new interpretation of sun and shade phytoplankton. Journal of Marine Research, 24,319-337. YENTSCH C, S., C. M. YENTSClt, C. M. STRUBEand I. Morris (1974) Influence of tcmpcraturc on thc photosynthetic efficiency in natural populations of marine phytoplankton. In: Thermal ecology, J. W. GIBBONSand R. R. SHARITZ,editors, Atomic Energy Commission, Oak Ridgc, Tennessee, pp. 508--517.
0198 1114~9/85$3 {111+ II.llll (~ 1985 Pergamon Press IAd.
Photosynthetic response to temperature of marine phytoplankton along a latitudinal gradient (16°N to 74°N) W. K. W. LI* (Received 1 April 1985; in revised form 3 June 1985;accepted 6 June 1985) Abstract--Photosynthesis-temperature relationships for natural phytoplankton assemblages were established by measuring the uptake of H ~4CO3in freshly collected seawater samples incubated for 2 h across a shipboard laboratory temperature gradient. The minimum, optimum and maximum temperatures for photosynthesis, as well as the extent of photosynthetic change per unit temperaturc change in the suboptimal range, all decreased from low to high latitude. The empirical mathematical model of RATKOWSKVetal, (1983, Journal of Bacteriology, 154, 1222-1226) provided a good fit to the data.
INTRODUCTION
FOR MANYplants, the response to changes in an environmental condition depends on both their genotype and phenotype. Thus the conditions prevailing in the natural habitat and during growth are important determinants of the response. For example, plants native to and growing in cold environments generally have minimum, optimum and maximum temperatures (so-called cardinal temperatures) for photosynthesis that are lower than the respective temperatures in plants native to and growing in warmer environments (BERRY and BJORKMAN, 1980). Additionally, plants may have the ability of acclimating (phenotypically) to different temperatures. Thus, the cardinal temperatures for photosynthesis of a cold-native may be increased if the plant is grown at a higher temperature. Conversely, the cardinal temperatures of a warm-native may be decreased if growth is at a lower temperature (BERRYand BJORKMAN, 1980). The extent to which such acclimation proceeds is itself genetically determined. In the case of unicellular algae, such features of temperature adaptation have been confirmed by experimentation with monoclonal laboratory cultures. Genotypic adaptation is evident when the temperature response is compared between warm-water and cool-water clones of given species (BRAARUD, 1961; GUILLARDand KILIIAM, 1977; ttULBURT, 1982; KRAWIEC, 1982). Phenotypic adaptation is evident when the temperature response for a given clone is compared at different acclimation (growth) temperatures (ARUGA, 1965; SHERIDANand ULIK, 1976; LI and MORRIS, 1982). The question to be considered in this paper is whether marine phytoplankton in nature also exhibit a photosynthetic response to temperature that is dependent on the temperature of their habitat. The answer to this cannot be directly derived from laboratory studies * Marine Ecology Laboratory, Bedford Institute of Oceanography, Department of Fisheries and Oceans, Dartmouth, Nova Scotia, Canada B2Y 4A2. 1381
1382
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of cultured clones for various reasons. First, almost every sample of phytoplankton from the sea is a multispecies, muiticlonal assemblage. Since there is genetic variability in the response to temperature (BRANDetaI., 1981), the response exhibited by the assemblage as a whole may not resemble that of any particular clone. Second, there are many factors which can affect the temperature response that would have to be laboriously specified in culture studies (but that would be given in a fresh phytoplankton sample collected and assayed at sea). Such factors would include the conditions of light intensity, day length, salinity, nutrient supply and temperature during growth. In this paper 1 report the results of shipboard experiments in which photosynthesis-temperature relationships for natural phytoplankton assemblages were established by measuring the uptake of HHCO~ in freshly collected samples incubated for a short time across a shipboard laboratory temperature gradient. MATERIALS AND METIIODS
Experimental procedures" Experiments were conducted on board CSS Hudson in August and September 1983 during a cruise in the eastern Canadian arctic (cruise 83-023) and in December 1984 during a cruise in the Caribbean Sea and the Atlantic Ocean (cruise 84-049). Seawater was collected using a pump sampler system (HERMAN el al., 1984). The dates, locations and depths of sampling as well as the temperature and chlorophyll a content of the samples are given in Table 1. A major impediment to the field study of temperature responses in phytoplankton has been the difficulty of operating unwieldy temperature gradient incubators on research vessels. Most experimentors have therefore relied on separate thermostated water-baths, the number of which in any study is usually 3 or 4 (YENTSCHelaI.,1974; LI and PLA'Vr, 1982; NEORI and HOLM-HANSEN, 1 9 8 2 ; JACQUES, 1983; LI et al., 1984) and rarely exceeds 6 or 7 ( A R U G A , 1965; HARRISand PICCININ, 1 9 7 7 ; HARRIS, 1978). Obviously, the data resulting from these experiments are grossly inadequate to describe fully the response across the entire biokinetic range. We have recently overcome this problem by a combination of some simple modifications to a commercially available temperature gradient incubator and the downscaling of sample volume (to 1 ml) required to measure H t4CO~ uptake in this instrument ILl and DICKIE,1984). The measurement of light-dependent H ~4CO~ uptake (photosynthesis) as a function of Table 1. Descriptive information on phytoplankton samples
Date
7 Dec. 11 Dec. 14 Dec. 15 Dec. 10 Aug.
1984 1984 1984 1984 1983
23 A u g . 1983 I0 Sept. 1983
Latitude IN)
Longitude (W)
Depth (m)
Temperature (°C)
Chlorophyll a(~g I i)
I,,,(W
16o44.5 ' 29°50.0 ' 35°37.1 ' 36o54.5 ' 64°09.4 '
66"48.6' 77018.9 ' 75013.5 ' 74049.0 ' 57"12.6'
10 10 10 10 l0
27.5 22.6 15.9 14.4 3.5
(I.10 0.24 2.28 1.79 1.15
99 174 47
0.96 0.78 0.99
74°07.0 , 72003.6 '
81°54.0 ' 68018.4 '
25 28
0.0 -I. I
1.116 6.41
55 47
I).99 0.98
* See Methods for explanation.
m
-')*
P,~//',,,*
Photosyntheticresponseto temperatureof marinephytoplankton
1383
temperature has been described (LI and DICKIE, 1984). Briefly, 1.0 ml subsamples of seawater radiolabelled with NaHI4CO3 (47.1 mCi mmol -I, NEC-086H, New England Nuclear; final activity of about 5 to 50 laCi m1-1 seawater) were measured into optically clear, plastic incubation chambers (No. 4804 tissue culture chamber/slide, Lab-Tek Products) placed in a temperature gradient incubator (Model 675, Scientific Industries Inc.). A pair of cool-white fluorescent lamps provided 68 W m-2 of incident photosynthetically active radiation. Samples were incubated in the temperature gradient for 2 h. Radiolabelled plankton were collected by vacuum filtration onto 0.2 lam Nuclepore membranes using 3 filtration manifolds, each capable of handling 12 samples simultaneously (1225 Sampling Manifold, Millipore Corp., Bedford, MA). Each filter was rinsed twice with l0 ml of freshly filtered seawater (
To be assured that 68 W m -2 was appropriate for the measurement of light-saturated rates of photosynthesis (i.e. neither too low to be limiting nor too high to be inhibiting), the following analysis was done. In five out of seven experiments (Table 1), B. D. IRWIN (unpublished observations) measured HI4CO~ uptake as a function of irradiance at the in situ temperature in a shipboard laboratory light-gradient incubator (PtArr et al., 1980; PLATFand GALLEGOS,1980). The resulting data were fit by non-linear regression to the photosynthesis-light model of PLATret al. (1980). From this, it was possible to estimate the irradiance at which photosynthesis was maximum (/m), the rate of photosynthesis at 1,,, (P,,), and the rate of photosynthesis at 68 W m -2 (Pt,8). In these experiments, there was only one case (15 December, 1984) for which the ratio of Pt,~ to P,,, was slightly less than unity (Table l). Data analysis
Photosynthesis-temperature data were fit to the empirical mathematical model of RATKOWSKYet al. (1983) by non-linear regression according to the Gauss-Newton method (BARD,1974) using a computer: P = f(T) g(T),
(1)
f(T) = [[~(T- T~in)] 2
(2)
g(T) = [l - exp{~,(T- Tmax)}]2,
(3)
where and where P is the light-saturated rate of photosynthesis (units = lag C lag Chl a -~ h-l); T is the temperature (units = °C); Tm~. and Tm,~xare the minimum and maximum temperatures, respectively, at which P is zero; [3is a parameter related to the extent of change in P for unit change in T below the optimum temperature [units = (lag C lag Chl a -~ h-~) L/2 °C-I]; and ~, is a parameter related to the relative change in P for unit change in T above the optimum temperature (units = °C-~).
1384
w.K.W.
Ll
Mathematically, P assumes positive finite values at values of T that are less than Tmi, or greater than Tm~x. This biological impossibility is of no concern if attention is restricted to Tmi. ~< T ~< Tm,x. Within this range, the temperature (T,,pt) at which P is optimum (Poor) is uniquely defined. RESULTS
The results of experiments conducted at the lower latitudes (cruise 84-049) and at the higher latitudes (cruise 83--023) are shown in Figs I and 2, respectively. In going from cold to warm waters, there was an incrcasc in all three cardinal tcmpcraturcs (Table 2, Fig. 3). In all cases, Toot was closer to Tmaxthan to Tmi,. For arctic phytoplankton, Toot was much higher than in situ temperature. There was an approximate I°C increase in Toot for every 2°C increase in the in situ temperature (Fig. 3) so that for Caribbean phytoplankton, Toot
/ 27"5° C 1.0
I
22"6° C
• •
•
•
•
~- 0.5
0
J
•
J
'.0 o
|
I
J
t
14,4°C
I
X
I
I
I
I
I
J
f ;o
o
,o
I
2o
I
~o
TEMPERATURE ("C) TEMPERATURE (*C) Fig. ]. Normalized photosynthesis--temperature curves from experiments performed on cruise 84-049. Numbers in panels indicate in situ temperature. Measurements of P within each experiment arc normalized to the value of Popt for that particular experiment. The curves represent the statistical best-fit of the Ratkowsky model to the data (see Methods). The model parameters arc given in Table 2.
;o
Photosyntheticresponse to temperature of marine phytoplankton
3.5oc
1385
O.O°C
I.O
n O.I
I
I
I
I
I
I
I
I
I
I n
i
o
'
,4
'
TEMPERATURE
2~
'
3o'
'
(*C)
Fig. 2. Normalized photosynthesis-temperature curves from experiments performed on cruise 83-023. Numbers in panels indicate in situ temperatures. Refer to Fig. 1 legend for explanation of curves.
was the same as the in situ temperature. For Tmi,, there was an approximate I°C increase for every I°C increase in the in situ temperature (Fig. 3). The same was true for Tm~xbut only up to an in situ temperature of about 14°C. At temperatures above this, Tm,,x appeared to remain constant at about 35°C (Fig. 3). Values of 13 (Table 2) were positively correlated with in situ temperature (r -- 0.77, P < 0.05). For the sake of comparison against a more familiar measure of the degree to which a biological process depends on temperature, Table 2 also lists the Arrhenius activation energy, E,, (RABINOWITCH,1956). Values of E,, were estimated from the slope of the regression of lnP on I/T in the suboptimal temperature range of each experiment. Such regressions explained at least 76% of the variance. Although the relationship between 13 and E, is non-linear and temperature-dependent (13 ~ - ( T - T m i , ) -l [A exp(-Ea/RT)]ll2), the two parameters were correlated (r = 0.76, P < 0.05). Values of y (Table 2) were uncorrelated with in situ temperature (P > 0.6).
Photosynthetic response to temperature of marine phytoplankton
1387
The Arrhenius equation has been extensively used in phytoplankton research (GoLDMAN and CARPENTER, 1974) which has mainly been concerned with responses in the suboptimal temperature range. Originally developed from the chemical theory of absolute rates for elementary reactions, the model is only empirical when applied to a biological reaction sequence as complex as photosynthesis. Although the Arrhenius equations can be extended to cover the entire biokinetic range (JOHNSONet al., 1974; MOHRand KRAWIEC, 1980), the model of RATKOWSKVet al. (1983) was chosen in the present study for thc following reasons. Although strictly empirical in nature, the Ratkowsky model not only fits the data well (Figs 1 and 2), but it also is expressed in parameters which are easily identified with biological concepts. The exception is Tmin for psychrophiles (RA'rKOWSK¥ et al., 1982, 1983). In cases where Train is lower than the freezing point of seawater, Tm~n has to be regarded as a characteristic temperature of no metabolic significance. Due to mechanical problems with the incubator during the arctic cruise, the lowest temperatures achieved during measurements of photosynthesis were always a few degrees above in situ temperatures (Fig. 2). The values estimated for 13 and Train in thesc experiments must therefore be regarded as based on extrapolations (using the Ratkowsky model) of measurements at higher temperatures. In earlier work in which we measured photosynthesis of samples incubated in four water baths thermostated at separate temperatures +5°C from ambient, our best estimate for E, based on data pooled from 12 experiments was 16.9 kcal mol -I (LI et al., 1984). The values of 15.1 and 11.1 kcal mol -l for the samples of 23 August and 10 September, 1983 respectively (Table 2) were not greatly dissimilar to the earlier value. However, it is difficult to judge the reliability of the extrapolated low temperature response of the remaining arctic sample (10 August, 1983): the values of both E,, and Tmi, were very low (Table 2). In spite of the reservations with which values of 13and Tm~,,for arctic samples must be viewed, it is clear that Tmin, T,,pt and Tm~x all increased with in situ temperature (Fig. 3). For Toot, this adaptive nature was noted previously (LI, 1980). In particular, ARUGA(1965) demonstrated a seasonal covariation of T,,pt with water temperature for freshwater phytoplankton in a pond in the University of Tokyo campus. Furthermore, the seasonal data of ARU6A (1965) and the latitudinal data in this paper (Fig. 3) both indicate a close correspondence between Topt and in situ temperature when the latter is high, but a divergence between the two temperatures when in situ temperatures are low. In several species of higher plants, the change in Toot also does not fully match the change in growth temperature (BERRYand BJORKMAN,1980; BERRYand RAISON, 1981). The slope of about 0.5 for the Topt vs in situ temperature relationship in marine phytoplankton (Fig. 3) was the same as that in Alaskan mosses (OECHEL, 1976). Our results show that multispecies assemblages of phytoplankton in the ocean, like clonal isolates cultured in nutrient-replete media in the laboratory, have a photosynthetic response to temperature that is dependent on the temperature of growth. All P-T curves obtained so far have only one optimum each. It is therefore possible to consider the assemblage as a physiological unit in the way that it is done so when discussing photosynthesis-irradiance relationships. This contrasts with natural bacterioplankton assemblages, some of which display heterotrophic activity-temperature response curves that have more than a single optimum (ROMANENKO, 1982; LI and DICKIE, 1984). The temperature response of photosynthesis across the entire biokinetic range is not the result of a single chemical reaction (JOHNSONet al., 1974). Increasing temperature accelerates the reactions which both enhance and depress photosynthesis. At temperatures less than Toot, those reactions that enhance photosynthesis are dominant; at
1388
w.K.W. Lt
temperatures greater than Toot, those that depress photosynthesis are dominant. This overall process can be modeled simply by subtracting an Arrhenius equation for the photosynthetic-depressing processes from one for the photosynthetic-enhancing processes (DEAN and HINSHELWOOO,1966; MOHR and KRAWiEC, 1980). However, the Ratkowsky model is a multiplicative one. It is the result of multiplying a continually increasing function, i.e. f(T) (equation 2) with a continually decreasing function that is scaled from 0 to 1, i.e. g(T) (equation 3). As T---~ Train, g(T) --~ 1 so that P - * f ( T ) . An interesting feature of the Ratkowsky model is that Toot depends on Tmin, Tm,,xand 7 but not on 13.This is shown as dP - 2 13fU2(T)g(T) - 2"ff(T)gl/2(T) [1 - gl/2(T)], dT
(4)
when dP/dT = O, the factor 2132can be eliminated so that 0 = (Toot - Tmin)g(Topt) - ~'(Toot - Train)2gl/2(Topt)[1 - gl/2( Toot) ].
(5)
Although I have not been able to obtain an explicit analytical solution to Toot, it is clear from equation (5) that Topt depends on Tmin, Tmaxand ~,but not on 13.From this it is implied that changes in Top, come about, not by change in the suboptimal rates of photosynthesis [which are most likely under the control of rate-limiting enzymes such as ribulose-1, 5bisphosphate carboxylase (BJORKMANand PEARCY,1971; Ll et al., 1984)], but by changes in Train, Tma,, and 7. Recent reviews that discuss the factors controlling these three parameters include CHRISTOPHERSEN(1973), INGRAHAM(1973), INNISSand INGRAttAM(1978), AMELUNXENand MURDOCK(1978), BERRYand BJORKMAN(1980), ARAGNO(1981), BERRY and RAISON(1981), STEPONKUS(1981) and GRAHAMand PATI'ERSON(1982). It is only a mathematical feature of the empirical Ratkowsky model that 13has no influence on T,,pt; but it is an intriguing biological possibility worth pursuing. The parameter 13conveys information about the extent of photosynthetic change arising from an increase of temperature in the suboptimal range. It is correlated with E, which conveys the same information. For Phaeodactylum tricornutum, E,, of light-saturated photosynthesis was found to be the same whether cells were grown at 5, 10, 15 or 25°C (Ll and MORRIS, 1982). For freshwater phytoplankton assemblages in Lake Ontario, QI. (a measure similar to E~) was also found to be the same at different seasons (HARRISand PICCININ, 1977). However, for the marine phytoplankton studied here, 13 and E,, were correlated with in situ temperature (Table 2). Although the values of E,, for arctic phytoplankton (Table 2) were similar to those of many other plants (RABINOWITCIt, 1956; BJORKMANand PEARCY, 1971), the values of E,, for the lower latitude phytoplankton (Table 2) appeared quite large. In arctic phytoplankton, the E,, for P and ribulose-1, 5bisphosphate carboxylase (RUBPC) activity have been found to be similar, indicating that RUBPC may be important in controlling the rate of photosynthesis at suboptimal temperatures (Lt et al., 1984). In contrast, SMmt and PLAT1"(1985) found that the E,, for RUBPC activity was significantly lower in phytoplankton in the tropics than in the arctic. Thus, in tropical phytoplankton, the greatly dissimilar values of E,, for P (reported here) and for RUBPC activity (reported by Smith and Piatt) suggest that RUBPC may not be directly important in the photosynthetic response to temperature changes in the suboptimal range. Another feature sometimes observed in thermally adapted phytoplankton is that the light-saturated rate of photosynthesis remains constant over a range of growth tempera-
Photosynthctic rcsponsc to tclnpcraturc of nlarille phytoplankton
1389
tures. In other words, the P vs in situ temperature plot is a horizontal line (so-called perfect compensation). This was found to be the case in Phaeodactylum tricornutum at 10, 15 and 25°C (LI and MORRm, 1982). For natural asscmblagcs of phytophmkton, plots P vs in situ temperature seldom yield a horizontal line. This was also the case in the present set of experiments. This was most likely because P at any one temperature depends on the diel rhythm (MACCAULLand PLATr, 1977; HARDINGet al., 1982), light history (YENTSCItand LEe, 1966; BEARDALLand MORRIS, 1976), cell size and species composition (MALONE, 1971; DURBINet al., 1975; GLOVER, 1980; CO'rEand PLA'Fr, 1983) and nutrient conditions (T)toMAS, 1970; GLOVER, 1980). The ecological implications of this study appear straightforward. In terms of photosynthesis, phytoplankton at high latitudes are not sensitive to slight increases in their habitat temperature. They have relatively low 13values and live at temperatures far from Toot and Tm~,~. On the other hand, low latitude phytoplankton are relatively much more sensitive to any change in habitat temperature. As they are at or near Topt, a slight temperature increase will rapidly bring them near Tmax,while a temperature decrease will reduce P by a relatively large extcnt because of high 13values. Acknowledgements--I thank B. D. Irwin for unpublished information, P. M. Dickie for assistance in the experiments, Dr. E. P. W. Home for assistance in the mathematics, and D. Rudderham for assistance in computing. Drs T. Platt, J. C. Smith and W. G. Harrison read the manuscript. REFERENCES AMELUNXENand A. L. MURDOCK(1978) Microbial life at high temperatures: mechanisms and molecular aspects. In: Microbial life in extreme environments, D. J. KUSHNER,editor, Academic Press, New York, pp. 217-278. ARAGNOM. (1981) Responses of microorganisms to temperature. In: Physiologicalplant ecology, Vol. 1, O. L. LANGE, P. S. NOBEL, C. B. OSMONDand H. ZIEGLER, editors, Springer-Verlag, Berlin, pp. 339-369. ARUGA Y. (1965) Ecological studies of photosynthesis and matter production of phytoplankton 1. Scasonal changes in photosynthesis of natural phytoplankton. Botanical Magazine, Tokyo, 78,280--288. BARD Y. (1974) Nonlinear parameter estimation. Academic Press, New York, 332 pp. BEARDALLJ. and I. MORRIS(1976) The concept of light intensity adaptation in marine phytoplankton: somc experiments with Phaeodactylum tricornutum. Marine Biology, 37, 377-387. BERRY J. and O. B.IORKMAN(1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology, 31,491-543. BERRY J. and J. J. RAISON(1981) Responses of macrophytes to temperature. In: Physiologicalplant ecology, Vol. 1, O. L. LANGE,P. S. NOBEL, C. B. OSMONDand H. ZIEGLER, editors, Springer-Verlag, Berlin, pp. 277-338. BJORKMAN O. and R. W. PEARCY (1971) Effect of growth temperature on temperature dependence of photosynthesis in vivo and on CO2 fixation by carboxydismutase in vitro in C 3 and C4 species. Carnegie Institution of Washington Yearbook, 70, 511-520. BRAARUDT. (1961) Cultivation of marine organisms as a means of understanding environment influences on population. In: Oceanography, M. SEARS,editor, American Association for the Advancement of Scicnce, Washington, pp. 271-298. BRANDL. E., L. S. MURPHY,R. R. L. GUILLARDand H.-t. LEE ( 1981 ) Genetic variability and differentiation in the temperature niche component of the diatom Thalassiosira pseudonana. Marine Biology, 62, 103-110. C|IRISTOPHERSENJ. (1973) Basic aspects of temperature action on microorganisms, In: Temperature and life, H. PRECHT, J. CHRISTOPHERSEN,H. HENSELand W. LARCHER,editors, Springer-Verlag, Berlin, pp. 3--59. COT~ B. and T. PLATr (1983) Day-to-day variations in the spring-summer photosynthetic parameters of coastal marine phytoplankton. Limnology and Oceanography, 28, 320--344. DEANA. C. R. and C. HINSHELWOOD(1966) Growth, function and regulation in bacterial cells, Clarendon Press, Oxford. 439 pp. DURBIN E. G., R. W. KRAWIECand T. J. SMAYDA(1975) Seasonal studies on the relative importance of different size fractions on phytoplankton in Narragansett Bay (USA). Marine Biology, 32, 271-287. GLOVERH. E. (1980) Assimilation numbers in cultures of marine phytoplankton. Journal of Plankton Research, 2, 69-79.
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Photosynthetic response to temperature of marine phytoplankton
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