DIURNAL PHOTOSYNTHETIC RESPONSES TO LIGHT BY MACROALGAE

336 MARET VESK AND S. W. JEFFREY

and cell division in the chrysophycean alga Ochrnmnnas danica. J . Phjcnl. 8:243-56.

Stauber, J. L. 1984. Photosynthetic pigments in diatoms. M.Sc. Thesis, University of Sydney, N.S.W., Australia, 174 pp.

Suzuki, R. & Fujita, Y. 1986. Chlorophyll decomposition in Ske- letonma costatum: a problem in chlorophyll determination of water samples. Mar. Ernl. Prngr. Ser. 28:81-5.

Throndsen, J. & Kristiansen, S. 1985. Pelagococcus subz'iridis Nor- ris as a major component of the nanoplankton at Halten- banken, Norwegian Sea in July 1982. Abst. International Phy- cnlogiral Congress, p. 160.

Vesk, M., Hoffman, L. R. & Pickett-Heaps, J . D. 1984. Mitosis

and cell division in Hjdrurusfnetidus (Chrysophyceae). J . Phi- cnl. 20:461-70.

Vesk, M., Jeffrey, S. W. & Stauber, J. L. 1987. Pplagnccussubviridzs from the East Australian Current. 1st Int. Chrjsophjte Syn- posium 1983, Grand Forks, North Dakota. Abstract 39.

Withers, N. W., Fiskdahl, A., Tuttle, R. C. & Liaaen-Jensen, S. 198 1. Carotenoids of the Chrysophyceae. Cotnp. Binchem. Phjsinl. 68B:345-9.

Wright, S. W. &Jeffrey, S. W. 1987. Fucoxanthin pigment mark- ers of marine phytoplankton analyzed by HPLC and HPTLC. Mar. Ecnl. Prngr. Ser. In press.

J . Phycol. 23, 336-343 (1987)

DIURNAL PHOTOSYNTHETIC RESPONSES TO LIGHT BY MACROALGAE's2

Ricardo Coutinho and Richard Zingmark3 Belle W. Baruch Institute for Marine Biology and Coastal Research and

Biology Department, University of South Carolina, Columbia, South Carolina 29208

ABSTRACT

T h e dzurnal variabilit) of photosjnthesis zis. irradiance (P-I) cunies was evaluated f o r the six most dominant speczes of macroalgae that occur annuall) i n ,Vorth Inlet Estuar) , South Carolina. Three existing models best simulated the obsenled data: (1) the Hjperbolic Tangent Model of Jassb) and Plat t (1976), which was applied to data that shoued n o photoinhibitzon, (2) the Exponentzal Inhibition Model of Parker (1974), and (3) the Photoinhibition Model of Plat t et a1 (1980), which were emploqed when photo- inlzibition was measured Photoinhtbitzon uas obsenled in about 75% of the experiments, and in some cases a t irradiance lezlels as low as 500 p E . w 2 . s - ' . Most of the resulting P-I curties did not differ signzficantl) when measured at narious times of the da). As a consequence of these results, uie question conclusions expressed bj others that it is not possible to accuratel) deterinme diurnal photosjnthesis of macroalgae f r o m lzght saturation cunles that are measured oiler short time periods.

Keq index words: diurnal; estuary, P-I curzles, photoinhibition, photosjntheszs; productit f i t)

Measurements of photosynthesis are commonly used to estimate primary productivity in ecosystems. The usual approach for estimating diurnal production of macroalgae is to measure their photosynthesis over an interval of several hours around midday and to extrapolate the resulting data to the whole day (Littler and Murray 1974, Littler and Arnold 1985). This method however does not account for possible diurnal changes in the photosynthetic rate due to photoinhibition, photorespiration or circadian periodicity (Britz and Briggs 1976, Ramus and

Accepted: 18 January 1987. 2 Contribution No. 663 of the Belle W. Baruch Institute for

Marine Biology and Coastal Research. Address for reprint requests.

Rosenberg 1980), nor does it consider periods during the day when photosynthesis is not light saturated, such as those occurring near dawn and dusk and those associated with clouds, water turbidity, and tides which affect plants living especially in the sublittoral zone. The development of mathematical models having as a basis the relationship of photosynthesis vs. irradiance (P-I curve) and the daily irradiance provide a more realistic approach to estimate diurnal production in macroalgae (Brinkhuis 1977, Pregnall and Rudy 1985) and in phytoplankton (Vollenweider 1965, Fee 1969, Harris 1978). When using such a model to estimate diurnal production, an assumption is made that the initial slope of the curve [alpha (a)] and the maximum photosynthetic rate (Pm,,) are fixed properties for individuals of a given species (Ramus 1981). However, several factors such as nutrient, temperature and irradiance histories have been shown to affect these photosynthetic parameters (Curl and Small 1965, Thomas 1970, Platt and Jassby 1976, McCaull and Platt 1977, Jones 1978, Ramus 1981, Malone and Neale 198 1, Harding et al. 1982). When estimating diurnal productivity of a species of macroalgae it is important to know how variable is its P-I curve and its parameters during the day.

Although instantaneous P-I curves and diurnal photosynthetic measurements have been determined separately for various species of macroalgae (Britz and Briggs 1976, King and Schramm 1976, Arnold and Murray 1980, Ramus and Rosenberg 1980), no study has compared the parameters of P- I curves measured at different times of the day. Therefore, the purpose of this study was to evaluate the diurnal variability of P-I curves in several species of macroscopic algae, in order to test the hypothesis that the P-I curve for a particular species does not vary significantly during a day.

PHOTOSYNTHETIC RESPONSES BY MACROALGAE

MATERIAL AND M E T H O D S

P-I c u n v mmsurements. Four species of Chlorophyta [C'/z'a cur- ra tn L., Enteromorpha l i m n (L) J. Agardh, Enteroinorphn prol f rra (Miiller) J . Agardh and Brjopsisp(urnosa (Hudson) J. Agardh], one Phaeophyta [Ectocarpussiliculosus (Dillwyn) Lyngby] and one Rho- dophyta (Porphjra rosrngurtii Coll et Cox), were collected from an intertidal reef formed and dominated by the edible oyster Crnssostrrn ilirginica in North Inlet Estuary, South Carolina. These species are the dominant primary producers of macroalgae in this estuary (Coutinho and Zingmark 1985). North Inlet Estuary is a 32 km2, high salinity, subtropical, tidally influenced, pocket salt marsh common to the southeastern United States (Kjerfve 1978).

Several individuals from the same population of each species were collected in the field the evening before each experiment and kept overnight in an indoor aquarium with running seawater at ambient temperature. T h e following morning the specimens were sorted, rinsed of accumulated sediments and several individuals of the same species transferred to dual-chambered, 720 mL Plexiglas photosynthetic incubators with continuous stirring at 60 rpm (Fig. 1). The upper chamber of each incubator was filled with estuarine water. About 0.1-0.5 g dry weight of algal material per liter was added to the upper chambers and the chambers sealed to prevent exchange of gases with the air, for a period ranging from 0.5-1.5 h. Preliminary experiments showed no significant reduction in photosynthetic rates using this amount of algae for as long as 3 h. Incubators were kept in a thermo- statically controlled water bath at field temperatures i 1' C. Net photosynthesis and respiration were determined by measuring changes in dissolved oxygen with an Orbisphere 2714 oxygen system using a sensor placed into the side of each incubator. T h e results were converted to mg C.gdw-'.h-', while assuming a photosynthetic quotient (PQ) of 1.2 (Strickland and Parsons 1972). Two unfiltered controls (without macroalgae) were established to account for phytoplankton and microbial metabolism.

Samples were incubated outdoors under natural light. Three sets of incubations were run sequentially during the day for each species, in February and March 1984. The periods of experiments ranged from 0830-1030 (morning), 1100-1300 (noon) and 1330- 1530 (afternoon). The same plants were used throughout each daily experiment but fresh seawater from the original source was used for each experiment in each incubator to reduce bottle effects. For each experiment five different relative photon fluence rates (0.75 I, 0.38 I, 0.23 I, 0.05 I, 0.00 I = dark respiration) were obtained using appropriate layers of fiberglass window screening to serve as neutral density filters.

The algae were acclimated for 15 min at each light regime before beginning each series of measurements. Incident light was continually recorded in the field during the incubations with a Licor Model 185A Quantum meter connected to a LI-193SB spherical quantum sensor. T h e absolute photon fluence rate [WE. m-2. s-I of Photosynthetic Active Radiation (PAR), 400-700 nm] was calculated as the average of values taken at 5 min intervals throughout the incubation. Our approach was not significantly different from that used in laboratory experiments under con- stant conditions (Rosenberg and Ramus 1982). Appropriate cor- rections were made for attenuation due to light absorption by the Plexiglas, water and to self-shading by the incubation chambers.

All curve-fitting was performed statistically using nonlinear least-squares regression techniques, by computer using the SAS version 79.5 statistical package (SAS Institute, Inc., Cary, North Carolina). P-I parameters were estimated simultaneously using a derivative-free algorithm (The Dudley algorithm) of Ralston and Jennrich (1978). Three models were used to evaluate their capacity to simulate the observed data, i.e. closeness of fit between the observed data and the prediction derived from the following parameterized models:

Model (1); the Hyperbolic Tangent Model of Jassby and Platt (1976) was used when experiments showed no photoinhibition

337

FIG. 1. Schematic diagram of our submersible Plexiglas productivity incubator. The upper incubation part of the chamber (a) is flooded with seawater. T h e lower portion (b) is the battery/ motor chamber which has remained dry at depths up to 50 m. A 60 RPM, DC motor (d) with a magnet attached to the end of its shaft, is powered by 2 "D" cell batteries ( f ) , which turns the stirring bar below a the slotted spacer disk (c). An 0, electrode is introduced into the chamber through a hole in the side (g). (Drawing by Frech 1977.)

(defined here as a reduction in photosynthesis at high-irradiance):

P = P,,;tan h(a.I/P,,,) + R

where P (mg C.gdw-l.h-') is the photosynthetic rate, P,,, (mg C.gdw-l,h-') is the maximum rate of photosynthesis at saturating irradiance, a [mg C.gdw-L.h-1.(~E.m~2.s-L)- l ] is the initial slope of the curve at pre-saturation irradiance, I (pE.m-P.s-I) is the irradiance, and R (mg C.gdw-l.h-') is the rate of respiration.

When photoinhibition was observed models 2 and 3 were used. Model (2); the photoinhibition model of Platt et al. (1980):

(1)

P = P,[1 -exp(-a.I/P,)exp(-/3.I/P,)] + R, (2) where P, (mg C.gdw-l.h-') is similar to P,,,, and numerically equal when /3 is zero, P[mg C.gdw~L.h- ' .(pE.m-2.s-l )-I], and a, I and R are as described above.

Model (3): the exponential inhibition model of Parker (1974):

(3)

where I, (pE.m-2.s-') is the saturating irradiance, m [mg C.gdw-" h-'.(pE.m-2.s-1)-l] is the shape parameter for the curve, and P,,,, I and R are the same as described above.

Ten experimental data points were used for each P-I curve for statistical fitting. A Chi-square goodness of fit test (P < 0.05) was performed on each curve for each model tested. Criteria used for selecting the models are explained below in the Discussion.

Pairwise comparisons were performed on the values of the parameters obtained at different times of the day. Two alpha values (for example) were compared using the estimates A1, A2 and their standard errors SE,, SE, and the fact that, if the-esti- pates were computed from independent experiments, T = (A1 - A2)/\/SE12 + SEZ2 has approximately a standard normal distri- bution under the null hypothesis that A1 = A2. Tests were performed at the 0.05 significance level, so the H: A1 = A2 was rejected if IT1 > 2.

338 RICARDO COUTINHO AND RICHARD ZINGMARK

FEBRUARY MARCH

Ulva curvata

-2t

Bryopsis plumosa I

Enteromorpha prol i fera

10

-4 L

4

2tY 0 500 1000 1500 2000 0 500 1000 1500 2000

IRRADIANCE (uE.m-*.S-’ 1

FIG. 2. Daily variations in photosynthetic-light (P-I) curves in February and March. (1) Hyperbolic tangent model, (2) photoinhibition model, (3) exponential inhibition model. (M) Morning, (N) noon, (A) afternoon. * means significantly different from the others (P > 0.05).

The light saturation parameter, Ik(PmaX/a) was estimated by curve fitting.

Diurnal photosynthesis. Four diurnal photosynthetic measurements were performed with Ulzu curuata to compare the predicted with the measured values, two simulated in situ and two in situ in the estuary. Predicted photosynthesis was calculated from P-I curves measured around noon of the same day of the experiment under simulated in situ incubations and diurnal irradiance.

Diurnal photosynthesis was estimated by measuring changes in dissolved oxygen every hour during the daytime. The same plants

were used throughout the daytime, but the incubation water was replaced each hour of the experiment with fresh seawater from the original source to avoid depletion of nutrients and gases.

RESULTS

Photoinhibition was observed frequently during the experiments, especially in March (Fig. 2). During this month only Brypsis plumosa and Enteromorpha linza, incubated in the afternoon, did not demon-

PHOTOSYNTHETIC RESPONSES BY MACROALGAE 339

TABLF. 1. duj. Units are pE.m-2.s-'for I , and I, , mg C.gdw-'.h-'for P, and P,,,,, and mg C.gdw-'.h-' (pE.m-2.s-1)-1 for m, p and a.

A comparison of means and standard errors of measured, calculated and estimated parameters for equations ( I ) , (2) and (3) during the

February

Ulva cumata Morning (2) 0.095 i 0.027 Noon (2) 0.050 i 0.041 Afternoon (1) 0.024 i 0.009

Morning (2) 0.257 f 0.080 Noon (2) 0.217 f 0.091 Afternoon (2) 0.297 i 0.097

Morning (1) 0.042 i 0.040 Noon (1) 0.041 i 0.013 Afternoon (1) 0.012 f 0.005

Morning (1) 0.062 f 0.016 Noon (1) 0.045 i 0.023 Afternoon (1) 0.1 15 i 0.028

Enteromorpha linza Morning (2) 0.206 i 0.054 Noon (2) 0.137 i 0.063 Afternoon (2) 0.335 i 0.201

Morning (1) 0.026 f 0.015 Noon (1) 0.036 f 0.030 Afternoon (1) 0.019 f 0.004

Ectocarpus szliculosus

Bryopszs plumosa

Enteromorpha proltfera

Porphjra rosengurtii

8.38 i 1.5

5.93 f 2.1 5.97 i 0.8 5.58 i 1.0

6.7 k 0.67 5.0 f 0.93 5.8 i 0.56

6.0 f 1.38 6.7 f 2.02 3.7 i 0.42

7.84 f 1.2 0.002 f 0.001 8.23 f 3.0 0.0004 f 0.002

20.1 f 3.5 0.0089 i 0.005 25.1 f 5.3 0.0056 i 0.005 17.7 t 2.7 0.0041 f 0.004

16.5 i 2.8 0.011 f 0.006 12.8 f 3.2 0.003 f 0.004 12.7 f 3.5 0.010 f 0.008

March

66.6 f 25 129 f 126 348 i 348

66 f 26 101 f 51 51 f 19

140 i 116 143 i 41 316 i 165

108 f 24 109 f 48 51 2 10

64 f 22 84 i 32 57 i 20

231 f 145 182 f 165 185 f 45

C'lita cunlata Morning (3) Noon (3) Afternoon (3)

Morning (3) Noon (3) Afternoon (3)

Bryopszs plumosa Morning (2) 0.19 f 0.07 Noon (2) 0.11 f 0.05 Afternoon (2) 0.13 i 0.02

Morning (2) 0.23 f 0.14 Noon (2) 0.09 i 0.03 Afternoon (2) 0.10 i 0.02

Morning (2) 0.29 * 0.18 Noon (2) 0.13 f 0.09 Afternoon (1) 0.04 f 0.008

Porphyra rosengurtzz Morning (3) Noon (3) Afternoon (3)

Ectocarpus siliculosus

Enteromorpha proltfera

Enteromorpha lznza

10.3 i 1.2 10.5 f 3.03 10.5 f 2.3

21.7 f 3.0 17.1 k 2.8 14.7 i 2.9

15.0 f 3.1

14.9 f 1.9 19.4 f 2.3 12.1 f 2.3

25.5 f 6.8 31.5 f 24 27.4 i 4

12.3 f 4.1 28.7 f 19 33.4 f 8.6

15.9 f 2.9 19.4 f 7.4

1.02 t 0.28 0.62 i 0.49 0.81 f 0.43

0.71 f 0.26 0.81 f 0.30 0.52 f 0.28

117 f 60 233 f 209 178 2 43

0.014 i 0.01 0.019 i 0.03 0.015 f 0.006

0.007 f 0.009

0.015 f 0.003

49 i 36

246 f 92 0.02 f 0.006 266 i 193

0.007 f 0.003 0.004 i 0.007

50 f 38 137 f 115 379 i 81

0.82 f 0.24 0.63 i 0.18 0.64 f 0.32

574 ? 62 866 f 318 701 i 152

396 i 53 576 f 89 487 f 134

668 i 80 635 f 80 710 f 165

~~

a Parameter not in equation.

strate decreases in photosynthesis at high irradiances. Photoinhibition occurred with irradiance as low as 500 ~l.E.rn-'.s-l (Enteromorpha linza and Ec- tocarpus siliculosus in February), but, Enteromorpha proli&era and Brjopsisplumosa showed no sign of pho-

toinhibition during February even at irradiance levels as high as 1800 pE.m-'.s-' (Fig. 2).

Of the 36 experiments, 6 paired comparisons were significantly different in their photosynthetic responses at different times of day based on non-linear


h r

I F

3 F

I

Tl [J)

0, E W I-

Y

a a 0 r I- W

I- z P v)

0 I n

z

SIMULATED IN SlTU o----Q Predicted

Jan 11 .1986 - Measured

:,\.:::. I r r a d ia nc e

I April 28 .1988

14 1 1 2 . 1 0 . 8 . 6 . 4 - 2 - 0 -

2400 3A

2000

1600 - 1200

800

400

0

-.

TIME OF DAY (h )

FIG. 3. Diurnal irradiance, predicted and measured diurnal photosynthetic rates of C'lzra cunlata incubated under simulated in situ conditions.

regression analysis--P > 0.05 (Fig. 2). These vari- abilities were related to the presence or absence of photoinhibition.

Alpha values ranged from 0.335 to 0.012 mg C. gdw-'(pE.m-'.s-l)-' (2 = 0.1 13, n = 27), and about 85% of the values showed no significant differences throughout the day (Table 1).

N o significant differences in P,,, and P, were observed among daily comparisons. Values of P,,,, with the exception of those measured in Ectocarpus siliculosus, were higher in March than in February and ranged from 3.7-8.3 mg C.gdw-I.h-' (2 = 6.0, n = 10) to 10.3-23.2 mg C.gdw-I.h-l (2 = 15.4, n = 10) respectively in February and March.

The parameter p, which characterizes photoinhibition, did not vary significantly among comparisons made using only Model 2. However, it varied by about 22% when Model 1 (p = 0) was included. On the other hand, the parameter m that characterizes the shape of the curve in Model 3, did not vary significantly during the day. Values of m ranged from 0.52 to 1.02 mg C.gdw-'.h-l.(pE.m-z.s-')-' (x = 0.72, n = 16) and in general decreased as the magnitude of photoinhibition increased. Saturating irradiances (Is) ranged from 396 to 866 pE*rn-'.s-', with an average of 623 ~ E . m - ~ . s - ' (n = 9) during March.

I, represents the minimum light intensity neces- sary to produce saturated photosynthesis and is ap- proximated on a P-I curve by dropping a vertical

IN SlTU *---* Predicted

April 27.1986 - Measured ,h.':,'* ,.:.: ., l r radianc e ,

1 Ok . - 1000

800

600

400

200

e F

' 8 f 7

I3

; 2 D

a a O $ m

-0

P 4 0

Y

P o D

1 1 1

41200 F , April 3 0 , 1 9 8 6

iJJ I I- z > v)

0 I- 0 I n

12 rn

10 1000 hJ

8 800 m ,

6 Y

4

2

-. 600

400

0 200

-2 0 0 4 8 12 16 2 0 24

TIME OF DAY (h)

FIG. 4. Diurnal irradiance, predicted and measured diurnal photosynthetic rates of U h a cun'ata incubated in situ.

line to the x axis from the point where the initial slope (a) intersects P,,, (Talling 1957). I, was gen- erally higher in March than in February. The minimum value (average of the day) observed was 83 pE.m-z*s-l in Enteromorpha prolqera and the maximum of about 200 ~ E . m - ~ . s - l was seen in Brq'opsis plumosa and Porphjra rosengurtii (both in February). The average value of Ik for all species was 133 pE. m-z.s-l in February and 183 pE.m-z.s-l, in March. N o significant differences were observed in this parameter through the course of any day.

Comparisons between the predicted and the measured diurnal photosynthesis of Ulva cuwata compared closely in both simulated in situ and in situ conditions (Figs. 3, 4).

Although large differences could be observed on an hourly basis and especially at high irradiance, diurnal net photosynthesis varied only about 10% from the predicted value of photosynthesis. Pho- toinhibition in these experiments was observed only under simulated in situ conditions and was more accentuated in January.

DISCUSSION

Previous work on macroscopic algae in North In- let Estuary has been restricted to floristics (Wiseman 1979) and to community ecology (Zingmark et al. 1977). This current work addresses basic questions concerning functional relationships between light and photosynthesis. Several models have been pro- posed to describe these relationships. These models, which when graphed produce curves can be classi-


pigment composition, or stage in the growth cycle of the species.

The parameter It (Pmax/a, described above) ranged from about 89 to 200 pE*m-*.s-l and increased from February to March, coinciding with the general overall seasonal increase of the total light. These values are higher than those reported by Arnold and Murray (1980) from data obtained on the Cal- ifornia coast, where they found a range of 50-90 pE.m-2.s-1 for several intertidal species. Usually eu- littoral species are light saturated at about 500 PE. m-2.s-1, middle sublittoral are saturated at about 200 pE.m-2.s-', while deep sublittoral require only about 100 pE.m-2.s-' for saturation (Luning 1981). Using these criteria our experimental plants could be characterized as being between middle sublittoral and deep algae. This is not surprising considering that during the growing season of the macroalgae the water column is reasonably turbid. Sechi disk readings for the months Dec-Mar ranged between 0.8-1.6 m over the past five years (R. Zingmark, unpubl. data). Nevertheless, comparisons between I, values reported in the literature has to be made with caution because of the various methodologies used to calculate this parameter (Arnold and Murray 1980).

Although there have been many investigations into photosynthesis of macroalgae, only two studies, Brinkhuis (1977), and Pregnall and Rudy (1985), have used short-term P-I curves to predict diurnal photosynthesis in the field, based on daily irradiance. However, no assessment was done in these studies to test the validity of their extrapolations. To improve our accuracy in predicting diurnal production in macroalgae it is important to know ex- actly how variable the P-I curve is during the day. Since 83% of our P-I curves did not vary diurnally and since we found no evidence of endogenous photosynthetic rhythms that were independent of irradiance, we do not support the conclusions of Jass- by (1 978), Ramus and Rosenberg (1 980) and Ramus (1 98 1) that, it is impossible to derive net die1 photosynthesis from an instantaneous light saturation curve. Using the approach above we predicted total diurnal photosynthesis with -t 10% of error under both simulated in situ and in situ conditions.

It is obvious from the P-I curve experiments that the reduction of photosynthesis at high irradiance (i.e. photoinhibition) was the main source of variability. However, the influence of this factor on the total production of the macroalgae in North Inlet Estuary is probably minimal because most macroalgal species in this estuary live in the sublittoral; only under a combination of low turbidity, low tide, and clear sky does the irradiance exceed 1000 pE. m-2.s-*, which is, according to our results the irradiance where photoinhibition is more pronounced. This aspect can be observed in Figure 4, where irradiances above 1000 pE e m-" s-I only occurred during a short period of time.

Nevertheless, if more work is done to elucidate the mechanisms that result in photoinhibition or other phenomena that could cause a reduction of photosynthesis at high irradiance such as photorespiration or circadian periodicity (Ramus and Rosen- berg 1980), we would most probably increase our capacity to predict diurnal production using data from short-term photosynthetic experiments, since most of the variance in primary production is ac- counted for by the fluctuations in light (Platt et al. 1977).

Clearly, the use of instantaneous light saturation curves is an advance over the classical procedure of measuring photosynthesis at an interval of several hours around midday and extrapolating this result to the whole day (Littler and Murray 1974, Littler and Arnold 1985), especially in turbid estuaries where non-saturating light conditions in the field are commonplace.

This work was supported by a NSF Ecosystems grant for Long- Term Ecological Research (DEB801 21 65); RC was supported by a Post-graduate Scholarship of the MinistPrio da Educa$o do B r a d (CAPES-MEC, Process. 3303/81-82). We thank D. Lin- coln, T . Platt, J. Ramus, J. Spurrier and J. Vernberg for critical review of an earlier draft, and D. Edwards for his statistical ex- pertise. Appreciation i s also conveyed to two anonymous review- ers whose constructive comments improved the quality and style of the manuscript.

Arnold, K. E. & Murray, S. N. 1980. Relationships between irradiance and photosynthesis for marine benthic green algae (Chlorophyta) of differing morphologies. J . Exp. Mar. Biol. Ecol. 43:183-92.

Arntzen, C. J., Kyle, D. J., Wettern, M. & Ohad, I . 1984. Pho- toinhibition: A consequence of the accelerated breakdown of the apoprotein of the secondary electron acceptor of pho- tosystem 11. In Thornber, J. P., Staehelin, L. A. & Hallick, R. B. [Eds.] Biosynthesis of the Photosynthetic Apparatus Molecular Biologj, Dalelopment and Regulation. Alan R. Liss, Inc., New York, pp. 313-34.

Bannister, T. T . 1974. Production equations in terms of chlorophyll concentration, quantum yield, and upper limit to production. Limnol. Oceanogr. 19:l-12.

Brinkhuis, B. H. 1977. Comparison of salt-marsh fucoid production estimated from three different indices.J. Phyol. 13:

Britz, S. J. & Briggs, W. R. 1976. Circadian rhythms of chlo- roplast orientation and photosynthesis capacity in Ulna. Plant. Phjsiol. 58:22-7.

Burris, J. E. 1977. Photosynthesis, photorespiration, and dark respiration in eight species of algae. Mar. Bid. (Berl.) 39:

Chalker, B. E. 1980. Modelling light saturation curves for photosynthesis: An exponential function. J . Theor. B id . 84:205- 15.

Coutinho, R. & Zingmark, R. 1985. Macroalgal productivity in a salt marsh estuarine system. Second International Phjcolopal CongrPss, Copenhagen, Abs., p. 30.

Curl, H., Jr. & Small, L. F. 1965. Variance in photosynthetic assimilations ratios in natural, marine phytoplankton communities. Limnol. Oceanogr. 10(suppl.):R67-R73.

Drew, E. A. 1974. Light inhibition of photosynthesis in macroalgae. Br. Phjcol. J . 9:217-8.

Dunstan, W. M. 1973. A comparison of the P-I relation in phy- logenetically different macroa1gae.J. Exp. Mar. Biol. Ecol. 13: 181-7.

Fee, E. J. 1969. A numerical model for the estimation of pho-

328-35.

371-9.

PHOTOSYNTHETIC RESPONSES BY MACROALGAE 343

tosynthetic production over time and depth, in natural waters. Limnol. Oceanogr. 14:906-11.

Frech, W. 1977. Productivity and seasonality of macroalgae in North Inlet Estuary. M.Sc. thesis, University of South Car- olina, Columbia, 69 pp.

Gallegos, C. & Platt, T. 1981. Photosynthesis measurements on natural populations of phytoplankton: Numerical analysis. I n Platt, T. [Ed.] Phjsiological Basis of Phjtoplankton Ecologj. Can. Bull. Fish. Aquat. Sci. 210, pp. 103-12.

Harding, L. W., Prkzelin, B. L. & Cox, J . L. 1982. Die1 oscilla- tions of the photosynthesis irradiance (P-I) relationship in natural assemblages of phytoplankton. ’Mar. B id . (Berl.) 67: 167-78.

Harris, G. P. 1978. Photosynthesis, productivity and growth: The physiological ecology of phytoplankton. Arch. Hjdrobiol. Brih, Ergebn. Limnol. 1O:l-171.

Jassby, A. D. 1978. Polarographic measurements of photosynthesis and respiration. In Hellebust, J. A. & Craigie, J. S. [Eds.] Handbook of Phjcological LMethodJ, Phjsiological and Bio- chrmical Methods. Cambridge University Press, London, pp. 285-96.

Jassby, A. D. & Platt, T. 1976. Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol. Oceanogr. 2 1 :540-7.

Jones, R. I. 1978. Adaptations to fluctuating irradiance by natural phytoplankton communities. LZmld Ocranogr. 23:920-6.

Kerby, N. W. & Raven, J. A. 1985. Transport and fixation of inorganic carbon by marine algae. I n Callow, J. A. & Wool- house, H. W. [Eds.] Adz~ances in Botanical Rrsearch, Vol. 11, Academic Press, Orlando, pp. 71-1 18.

King, R. J. & Schramm, W. 1976. Photosynthesis rates of benthic marine algae in relation to light intensity and seasonal vari- ation. Mar. Bid. (Berl.) 37:215-22.

Kjerfve, B. 1978. Bathymetry as an indicator of net circulation in well-mixed estuaries. Limnol. Ocranogr. 23:s 16-2 1.

Kremer, B. P. 1980. Photorespiration and @-carboxylation in brown macroalgae. Planta 150: 189-90.

Lederman, T. C. & Tett , P. 1981. Problems in modelling the photosynthesis-light relationship for phytoplankton.Bot. Mar. 24:125-34.

Littler, M. M. & Arnold, K. E. 1985. Electrodes and chemicals. In Littler, M. M. & Littler, D. S. [Eds.]HandbookofPhjcological Methods, Ecological Firld Methods: Macroalgae. Cambridge Uni- versity Press, New York, pp. 377-98.

Littler, M. M. & Murray, S. N. 1974. T h e primary productivity of marine macrophytes from a rock intertidal community. Mar . Bid. (Bed.) 27: 13 1-4.

Lloyd, N. D. H., Canvin, D. T. & Culver, D. A. 1977. Photo- synthesis and photorespiration in algae. Plant. Phjsiol. 59: 936-40.

Luning, K. 1981. Light. In Lobban, C. S. & Wynne, M. J. [Eds.] The Biologj of Seaweeds. Blackwell Scientific Publications, Ox- ford, pp. 326-55.

MacCaull, W. A. & Platt, T. 1977. Die1 variations in the photosynthetic parameters of coastal marine phytoplankton. Limnol. Oceanogr. 22:723-3 1.

Malone, T . C. & Neale, P. J. 198 1. Parametersof light-dependent photosynthesis for phytoplankton size fractions in temperate estuarine and coastal environments. ‘Mar. Bid. (Berl . j46: 191- 202.

Mathieson, A. C. & Norall, T. L. 1975. Physiological studies of subtidal red algae.]. Exp. Mar. Bid. Ecol. 20:237-47.

Parker, R. A. 1974. Empirical functions relating metabolic pro- cesses in aquatic systems to environmental variables.]. Fish. Rrs. Board Can. 3 1 : 1550-2.

Peterson, R. D. 1972. Effects of light intensity on the morphol- ogy and productivity of Caulerpa racemosa (Forskal) J. Agardh. ,Micronesica 8:63-86.

Platt, T. , Denman, K. L. & Jassby, A. D. 1977. Modelling the productivity of phytoplankton. I n Goldberg, E. D. [Ed.] The Sea, Vol. 6. John Wiley and Sons, New York, pp. 807-56.

Platt, T., Gallegos, C. L. & Harrison, W. G. 1980. Photoinhi- bition of photosynthesis in natural assemblages of marine phytop1ankton.j. Mar. Rex. 38:687-701.

Platt, T . & Jassby, A. D. 1976. T h e relationship between photosynthesis and light for natural assemblages of coastal marine phytoplankton. j . Phjcol. 12:42 1-30.

Pregnall, A. M. & Rudy, P. P. 1985. Contribution of green macroalgal mats (Enteromorpha sp.) to seasonal production in an estuary. Mar. Ecol. Prog. Ser. 24:167-76.

Ralston, M. L. & Jennrich, R. I. 1978. Dud, a derivative-free algorithm for non-linear least-squares. Technornetrics 20:7- 14.

Ramus, J. 1981. T h e capture and transduction of light energy. In Lobban, C. S. & Wynne, M. J. [Eds.] TheBiologjofSeaweeds. Blackwell Scientific Publications, Oxford, pp. 458-92.

Ramus, J . & Rosenberg, G. 1980. Diurnal photosynthetic per- formance of seaweeds measured under natural conditions. ,Mar. B id . (Berl.) 56:21-8.

Rosenberg, G. & Ramus, J. 1982. Ecological growth strategies in the seaweeds Gracilaria foliijrra (Rhodophyceae) and Ulva sp. (Chlorophyceae): Photosynthesis and antenna composition. Mar. Ecol. Prog. S w . 8:233-41.

Smith, E. L. 1936. Photosynthesis in relation to light and carbon dioxide. Proc. ,\‘at/. Acad. Sci. Il’ash. 22:504-11.

Steele, J. H. 1962. Environmental control of photosynthesis in the sea. Limnol. Oceanogr. 7: 137-50.

Steeman-Nielsen, E. 1952. On detrimental effects of high light intensities on the photosynthetic mechanism. Phjsiol. Plant. 5:334-44.

Strickland, J. D. H. &Parsons, T. R. 1972. A practical handbook of seawat.er analysis. Bull. Fish. Res. Board Can. 167:l-130.

Talling, J . F. 1957. T h e phytoplankton as a compound photosynthetic system. hPut Phjtologist 56: 133-49.

Thomas, W. H. 1970. On nitrogen deficiency in tropical Pacific Ocean phytoplankton: Photosynthesis parameters in poor and rich water. Limnol. Oceanogr. 15:380-5.

Vollenweider, R. A. 1965. Calculation models of photosynthesis- depth curves and some implications regarding day rate estimates in primary production measurements. In Goldman, C. R. [Ed.] Primarj Productizlitj in Aquatic Enzjironments. Uni- versity of California Press, Berkeley, pp. 425-57.

Wiseman, D. R. 1979. Benthic marine algae. In Zingmark, R. [Ed.] An Annotated Checklist of the Biota of the Coastal Zone of South Carolina. University of South Carolina Press, Columbia,

Zingmark, R. G., Wohlgemuth, S., Wagner, G., Vennowitz, M., Reis, R., Hall, M. O., Ebeling, D. &Brown, D. 1977. Ecology of macroalgae in a temperate salt marsh at a site in North Inlet, SC. I. Biomass and productivity of intertidal species. ]. Phjcol. 13(suppl.):77.

pp. 23-36.

DIURNAL PHOTOSYNTHETIC RESPONSES TO LIGHT BY MACROALGAE

Documents

Transcript of DIURNAL PHOTOSYNTHETIC RESPONSES TO LIGHT BY MACROALGAE