Aquatic Botany, 26 (1986) 285---306 285 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

P R O D U C T I V I T Y - I R R A D I A N C E R E L A T I O N S H I P OF POSIDONIA OCEANICA A N D ITS E P I P H Y T E S

MAURICE LIBES

Centre d'Oc~anologie de MarseiUe-Luminy, Station marine d'Endoume, rue de la Batterie des Lions, F 13007 Marseille (France)

(Accepted for publication 14 August 1986)

ABSTRACT

Libes, M., 1986. Productivity-irradiance relationship of Posidonia oceanica and its epiphytes. Aquat. Bot., 26: 285--306.

The photosynthetic response to light of the marine phanerogam Posidonia oceanica (L.) Delile and its epiphytes from the Bay of Port-Cros (France) was determined monthly from March 1981 to July 1982. A ~4C technique was developed in situ for entire plants of P. oceanica. Their epiphytes were then removed in the laboratory after incubation. The productivity increased with light to an asymptotic value at which the system was light saturated. During summer photoinhibition was observed. In spite of a high variability, epiphytic productivity was twice that of P. oceanica. The productivity-irradiance relationship showed both circadian and seasonal variations. During the year, productivity-irradiance curves of P. oceanica and its epiphytes followed the sun-shade model for photosynthetic adaptation. The photosynthetic efficiency was highest in winter and decreased towards summer. During the day photosynthetic efficiency was highest in the morning and decreased towards sunset. Factors which may regulate these variations in efficiency are discussed.

INTRODUCTION

Posidonia oceanica (L.) Delile is an endemic phanerogam of the Mediter- ranean Sea. Its long ribbon-shaped leaves are grouped in clusters (or leaf shoots) which cover huge areas down to 30-40 m.

Previous research has shown that P. oceanica beds play a major role in the whole marine environment: their primary production is important for water oxygenation (Bay, 1978; Ott, 1980) and their density for bottom stabilization ( Boudouresque and Jeudy de Grissac, 1983) and they provide favourable con- ditions for the development and reproduction offish (Kikuchi and Pdr~s, 1977; Bell and Harmelin-Vivien, 1982, 1983) and marine invertebrates (Harmelin, 1964; Ledoyer, 1966, 1968).

In spite of the extensive works on ecology and dynamics of P. oceanica beds (Boudouresque et al., 1977), there are only a few basic studies on plant pri-

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286

mary production and physiology and on physical and chemical factors which regulate primary productivity.

So far, few studies have measured primary production of P. oceanica (Bay, 1978, 1984; Cristiani, 1980; Ott, 1980; Romero-Martinengo, 1983, 1985). A critical review of the methods used for measuring primary productivity of marine phanerogams is given by Plante-Cuny and Libes (1984). Most of these methods involve estimates of leaf growth using leaf tagging (Zieman, 1974) or biomass changes (Cristiani, 1980), which advance "blind" estimates of the leaf net production. Conversely, metabolic measurement methods, such as the 02 (Bay, 1978, 1984; Drew, 1978) or ltC technique (Drew and Jupp, 1976; Libes, 1984a) provide qualitative information about the photosynthetic response to some environmental variables such as light, temperature, nutrients and to the internal plant status such as chlorophyll and enzyme content. Apart from the 14C method, none of these methods can separate the production of the epiphytic algae from that of the host-macrophyte.

New leaves of P. oceanica are rapidly colonized by numerous microscopic algae and bacteria. Epiphytic colonization is a result of complex interactions (Nowak, 1984). Apart from diatoms, the first algae which settle are multicel- lular Phaeophytes such as Myrionema orbiculare J. Ag. and Rhodophytes such as Dermatholiton littorale Suneson, FoslieUa farinosa ( Lamouroux ) Howe and Fosliella lejolisii (Rosanoff) Howe, which constitute an incrusting stratum on the leaf surface. During the year, different algal communities follow each other and finally an erect stratum overlies the crustaceous one, with larger species such as the Phaeophytes Giraudia sphacelarioides Derbes et Solier and Castag- nea cylindrica Sauvageau (Van der Ben, 1971; Panayotidis, 1980; Nowak, 1984). In late spring, the epiphytic community on the leaves may constitute 20-30% of the total above-ground biomass (Thelin and Bedhomme, 1983; Libes 1984a) and may therefore play a major role for primary production of the host-macro- phyte system by affecting nutrient and light availability ( McRoy et al., 1972, 1973; Goering and Parker, 1972; Penhale and Smith, 1977).

To evaluate the primary production of a P. oceanica bed using the ltC tech- nique, we first attempted to estimate the carbon assimilation of both P. ocean- ica and its epiphytes in relation to some chemical and physical variables and to develop a multifactorial predictive model describing the productivity as a function of some independant prevailing factors. Particular emphasis was given to the productivity-irradiance relationship (P-I curves).

MATERIAL AND METHODS

Field experiments

The experimental site is located in shallow waters ( 3 m) in the Bay of Port- Cros island offthe Mediterranean coast of France (Fig. 1 ). Mean shoot density ofP. oceanica here is 475 m -2 (Libes, 1984a).

287

TOULON ~ ~ ~

N

- 43ON

Ikm I I 6 ~ 5 ~

l

Fig. 1. Location of Port-Cros Island off the Mediterranean coast of France.

All the 14C labelling experiments were carried out in situ by SCUBA diving. In each experiment, a whole plant of P. oceanica was enclosed in a watertight transparent plexiglas incubator (4.1 1) equipped with a stirring device (Fig. 2) in order to homogenize the radioactive solution and to avoid water strati- fication inside this incubator. The morphology of P. oceanica allows fitting of a rubber ring tightened at the bottom of the incubator and to the orthotropic rhizome of the shoot. This incubation system, with an entire plant enclosed without clipping it from the rhizome, preserves as well as possible the natural life condition of the plant. The tightness of the incubator was tested several times by means of various dyes.

The experiment was started by injecting 2 ml of a NaH14CO3 solution (20 #Ci ml-~). After incubation for 2--3 h, the labelled shoots were collected,

288

ry compartment

ing dev ice

ing

r membrane i n j e c t i o n )

i g l a s c y l i n d e r e r n a l Q ) . I0 cm)

tubing2

i m e n t

Fig. 2. Plexiglas incubator enclosing a P. oceanica shoot.

quickly dried on absorbant paper and immediately deep frozen in dry ice ( - 70 °C) for later t reatment in the laboratory. During incubation we mea- sured the underwater quantum flux reaching the tip of the leaves (Lambda instrument quantameter LICOR 550 equipped with a light sensor LI 192 SB), and selected variables in the water:temperature, salinity (always 37--38%o) and pH-alkalinity according to Strickland and Parsons (1972) ( Table I ). Mean shoot chlorophyll a + b concentration was measured on adjacent shoots by spectrophotometry after extraction in acetone ( 90% ) at 4 ° C (Libes, 1984b).

Sample treatment

The leaves were separated according to their position on the shoot ( Giraud, 1979). We distinguished "juvenile" leaves with a length of less than 5 cm appearing at the center of the shoot; "intermediate" leaves, in a state of rapid

289

TABLE I

Environmental variables and biotic parameters of P. oceanica on which principal component analysis was applied

h : mean incubation hour

di : incubation time lag lu : light energy irradiance during the incubation (Em - 2 h- ~ )

t ° : water temperature (°C)

pH : pHinwater

co : total inorganic carbon concentration in water (nag C l- i )

Im : mean leaf length (cm) sf : leaf shoot area index (era 2 ) pf : shoot dry matter weight (rag DW) nf : leaf number per shoot %f : percent of intermediate leaves in rapid growth ep : dry weight of epipbytes (rag DW) d : mean shoot density (mgcm -~) pr : P. oceanicaproductivity (rag C g D W -1 h -~) pe : epiphyte productivity (rag C g D W - ~ h - ~ )

growth, and "adult" ones that had stopped growing and had a distinct leaf sheath (Ott, 1980).

Epiphytes were carefully scraped off with a razor blade, and all epiphytes from the same shoot were combined. The thick cuticle on the leaf surface made it possible to remove almost all epiphytes without damaging the leaf. Although the term epiphytes is used to refer to epiphytic algae, the collected material also consists of other microscopic organisms and inorganic material such as silt or calcium carbonate of the Corallinaceae thalli. The ash proportion (after a combustion time of 24 h at 480 ° C ) of the epiphytic material can be as high as 40-50% of the total dry weight.

After lyophilization, each sample (leaves, epiphytes ) was weighed and com- busted in a Packard TriCarb B 306 oxidizer. Carbon dioxide was trapped in 9 ml Carbosorb (Packard product) which was then mixed with 12 ml of Per- mafluor scintillation cocktail before liquid scintillation counting. All counts were corrected for background, recovery efficiency after combustion and counting efficiency. Disintegrations per minute were then converted into mil- ligrams of carbon given the isotopic dilution ratio at the start of the experi- ment: ~4C/12C. Each leaf was combusted separately, and the data were combined for calculation of mean shoot production.

From March 1981 to July 1982, 175 labelling experiments were carried out. Each experiment consisted of 2-4 replicates and was carried out from 10:00 to 12:00 h (legal local t ime) and from 15:00 to 18:00 h. Once per season we carried out daily productivity cycles in order to study circadian productivity varia- tions. These cycles included a succession of experiments from sunrise to sunset.

290

Statistical methods

In order to quantify the correlation between both the primary productivity and the different measured environmental parameters and between the factors themselves, we applied a simple correlation and a multifactorial analysis (Principal Components Analysis: P.C.A. ) to our data. The 15 different para- meters measured during each incubation-experiment are identified in Table I.

The Principal Component Analysis (P.C.A.) enables us to point out, according to their contributions in the axis plan and their mutual position, the relationships between the variables and the ecological significance of the axis. Data were log10 transformed in order to normalize their distribution, to linear- ize the productivity-irradiance relationship, and to minimize the productivity measurement variance. We obtained several regression lines of the form log P=a log I+b (where P is the productivity and I the irradiance), from which we could estimate and compare the slope (a=ziP/AE, i.e. the photosynthetic efficiency) and the original ordinate (coefficient b). Instead of a t-test which allows the comparison of only 2 regression lines, the Reeve's test (Reeve, 1940) using an " F " test allows the comparison of several regression lines between themselves.

RESULTS

Relationship between productivity and biotic and abiotic factors

The correlation coefficients matrix (Table II) shows that P. oceanica pro- ductivity is significantly correlated with that of the epiphytes (r--0.896). Among the other parameters, only irradiance is significantly correlated with both phanerogam (r = 0.715) and epiphyte productivity (r = 0.593). If we leave out productivity measurements under high inhibiting irradiances (described below), the correlation coefficient increases (r-= 0.81 for P. oceanica and r = 0.66 for the epiphytes; n = 140).

The variance explained by the first 3 axes of the P.C.A. comprises 62% of the total inertia of the data distribution (Fig. 3 ). Axis I extracts 37.8% of the variance. It is represented by parameters which behave in a similar way throughout the year. They are the main biotic factors of P. oceanica (see Table I) "pF', "sf", "lm", water temperature "t °'' and epiphytic biomass "ep". Axis II extracts 15.2% of the total inertia. It is represented by primary productivity of P. oceanica ("pr") and its epiphytes ("pe") , and by "lu", the underwater available irradiance. No particular parameter could be correlated with Axis III which extracts only 9% of the total inertia.

The distribution of descriptors on the plan axes I-II, and II-III (Fig. 3) shows that most o f the other measured parameters such as "pH", "co", "di", "d", "% f", "nF' and "h" have a poor contribution in the axis and do not exhibit

291

TABLE II

Matrix of correlation coefficients between photosynthet ic and environmental parameters. For key to symbols see Table I

di 1 h 0.083 1 pr 0.009 - 0.328 1 pf 0.064 0.283 0.006 1 sf 0.091 0.329 0.135 0.944 1 nf -0 .161 0.024 0.212 0.076 0.055 1 lm 0.162 0.273 0.094 0.788 0.852 -0 .465 %f -0 .055 0.005 0.034 -0 .148 -0 .009 0.354 d -0 .027 0.009 0.004 0.579 0.289 0.100 pe 0.044 -0 .335 0.896 -0 .131 -0 .147 -0 .129 ep 0.155 0.260 0.025 0.749 0.741 -0 .102 lu 0.112 -0 .075 0.715 0.157 0.154 -0 .326 t ° 0.039 0.291 0.180 0.501 0.486 -0 .364 pH 0.011 0.176 0.031 0.066 0.106 -0 .039 co -0 .084 -0 .028 0.114 0.191 0.180 -0 .067

di h pr pf sf nf

lu 1 t ° 0.480 1 pH 0.217 -0 .061 1 co 0.039 0.246 - 0.264 1

lu t ° pH co

1 -0 .276 1

0.192 -0 .190 1 - 0.063 0.025 - 0.024 1

0.706 -0 .117 0.346 -0 .122 1 0.307 -0 .160 0.085 0.593 0.239 0.6,!6 -0 .361 0.244 0.022 0.445 0.112 0.068 -0 .048 -0 .021 0.042 0.192 -0 .050 0.113 0.064 0.214

lm %f d pe ep

any correlation with the primary productivity of P. oceanica and its epiphytes. They can be largely ignored in the predictive model of the seagrass bed pro- duction, at least with regard to this study and area.

Productivity-irradiance relationship of P. oceanica and its epiphytes

Light-photosynthesis curves of P. oceanica and its epiphytes follow a com- mon pattern (Rabinowitch and Govindjee, 1969; Fogg, 1972; Steemann-Niel- sen, 1975 ). An initial phase where productivity increases proportionally with irradiance is followed by a phase where the productivity reaches a maximum value (Pro,x) due to light saturation (at ca. 600 #E m -2 s -1. In P. oceanica Pn~,x is ca. 700-800 ttg C g D W - 1 h - 1. In late-spring and summer a third pho- toinhibition phase was observed for irradiances exceeding 750-800 #E m 2 s - 1. In P. oceanica the assimilation rate decreased down to ca. 250/~g C g D W - 1 h -1 (Fig. 4) .

Depending on season and weather conditions during the experiments, the 3 successive phases were not always observed (Figs. 4 and 5) . In winter, for instance, irradiance is too low to induce photosaturation. Likewise, bad weather may induce a winter-like response during other seasons (Fig. 4, Curve 7 ).

292

"LI

nf

I I

p# pr

eli

t "

CO

ep

Im /

p~ sf

n¢

ZI d

M

sf wp

III

CO

fm ph

p#

pr

I!

Fig. 3. Axis plan I-II and II-III of the principal component analysis of the measured parameters (see Table I for the meaning of symbols).

The carbon assimilation kinetic is similar for P. oceanica and its epiphytes (Fig. 5 ). For instance the same saturating and inhibiting irradiance levels were regularly observed for both components. On the other hand, in spite of large

293

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March-April 1981

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March 1982 May-June-July 1982

Fig. 4. Productivity-irradiance relationship for P. oceanica as observed during different seasons• Full circled points were obtained from the standard station (2.5 m) and open circles from a shal-

lower station (1 m).

294

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1200.

.

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i

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March 1982

I I i i

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200- 00 I May-June-July 1982

Fig. 5. Productivity-irradiance relationship for epiphytes of P. oceanica as observed during dif- ferent seasons. (For meaning of symbols, see Fig. 4.)

295

#g Cass gDW -1 h-1

1800

1600

1400

1200

I000

800

600

400

200

#gCas s gDW -1 h-1

t Hay 28 t h , 1 9 8 1

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1600

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1 2 3 4 Em-2h -1

t h ,June I 1

p" ! i ! !

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E m-2h -1

• EPIPHYTES

POSIDONIA OCEANICA

Fig. 6. Comparative produc~v~y-irradiance relationships for P. oceanica and its epiphytes. Daily productivity cycles for 28 May 1981 and 11 June 1982 at 2.5 m depth at Port-Cros Bay.

variations in the relationship of productivity to irradiance (discussed below), epiphytic productivity appears to be twofold higher than productivity of P. oceanica. It reaches a maximum value of ca. 1200-1400/xg C g DW -1 h -1 in the light saturated phase, then decreases (under higher irradiance values) down to ca. 600-800 pg C g D W - 1 h - 1 ( Fig. 6 ).

Circadian variations of primary productivity

Several kinds of circadian rhythms of pr imary productivity were observed depending on season. During winter, when irradiances are low, productivity follows irradiance, i.e. a maximum at noon and symmetrical min imum values at sunrise and sunset (Fig. 7a). In contrast, during summer, productivity is highest as early as 09:00 h. Then irradiance increases up to 1600/xE m -2 s -1 and induces a considerable decrease of the photosynthet ic rate down to 250/xg C g D W - 1 h - 1. Close to sunset, at irradiances similar to morning values, pro- ductivity remains at a low level. The photoinhibition effect continues until the end of daylight (Fig. 7b ).

When the photosynthetic efficiency is plotted (productivity per unit of light ) against irradiance, it is observed as expected tha t the photosynthet ic efficiency decreases with increasing irradiances (Fig. 8). This method also enables the separation of data which correspond to morning and afternoon experiments. At low irradiances, the photosynthet ic efficiency is usually lower in the after-

296

~e m-2S -1 ug C g D W -~ h -1

Harch 1981 1600

1200. I I I

IV

800 I I

I ] i I / 7 8 9 10 11 12 13 14 15 16 17 18 19

I

2o 2'1

600

450

300

150

Hours

~ m-2s -1 ~g C g D W - l h -1

1600. 600

1200. 450

800 300

400 150

,

7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 Hours Fig. 7. Diurnal patterns of productivity (histograms, right axis) and irradiance (continuous line, left axis) ofP. oceanica during winter (above, 5 March 1981 ) and during summer (below, 29 July 1981).

noon than in the morning. This depression effect depends on actual light con- ditions during the day, i.e. the depression being highest when mid-day irradiances and thus photoinhibition is highest. Such photosynthetic varia- tions could also be observed as a function of depth. For instance, we found P. oceanica photosynthetic efficiency, measured at a site 25 m deep, to be twice as high as in shallow water, the photosynthetic efficiency of the epiphytes being 7- to 10-fold higher ( Table III).

pg C g D W -1 E m -2

297

900"

7 0 0 -

5 0 0 -

3 O 0

1 0 0

!% I ! I ! ! ! 1 2 3 4 5 6

E m-2h-1

o Afternoon

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Fig. 8. Photosynthetic efficiency with increasing light irradiance. Measurements (open circles) which do not fit the model were obtained from afternoon experiments,

Seasonal variations in productivity

The productivity-irradiance regression lines for each month are shown in Table IV. A Reeve's test performed on the monthly productivity-irradiance

TABLE III

Photosynthetic efficiency in relation to depth for P. oceanica and its epiphytes

Depth 1.5 m 2.5 m 25 m Irradiance 1.30 1.20 0,15 (E m-2 h -1 )

25 m 0.15

P. oceanica Productivity ~ 560 600 200 130 Efficiency 2 430 500 1330 870

Epiphytes Productivity ~ 1320 1360 1680 1130 Efficiency 2 1015 1130 11200 7533

~Productivity is expressed as ~g C g D W - 1 h ~. 2 1 2 Efficiency is expressed as P4~ C g D W - / E m - ' .

298

TABLE IV

Productivity-irradiance regression lines after log10 transformation of the data, with the exception of those situated in the photoinhibition phase of the P-I curves 1

Posidonia oceanica (1) March-April 81 Log P=0.614 log I+ 2.48 r2--0.66 n = l l (2) May-June 81 Log P=0.659 log I+2.45 r2=0.92 n=15 (3) Sept.-Oct. 81 Log P--0.965 log I+2.34 r2=0.91 n=22 (4) November 81 Log P-- 1.043 log I+2.70 r2-0.94 n = l l (5) January 82 LogP=0.769 logi+2.71 r2=0.98 n= 7 (6) March 82 Log P--0.767 log I+2.62 r2-~0.61 n=21 (7) May-June 82 Log P - 1.022 log I+ 2.42 r2-~ 0.80 n=25

Epiphytes (1) March-April 81 Log P-- 0.537 log I+2.83 r2--0.32 n=lO (2) May-June 81 Log P--0.673 log I+ 2 .73 r2-:0.82 n=17 (3) Sept.-Oct. 81 Log P-- 1.051 log I+2.56 r2--0.87 n=26 (4) Nov.81-Jan. 82 Log P-0.868 log I+ 3 .02 r2-0.80 n=16 (5) March 82 Log P - 0.796 log I+ 2 .96 r2-0.71 n=21 (6) May-June 82 Log P--0.971 log I+2.70 r2-0.80 n=22

1p = productivity; I= irradiance, r 2 = determination coefficient; n = data number.

regression lines demonstra tes significant differences between both the slopes and the mutual posit ion of the curves (Table V). When pooling these different curves on the same axis, we can show a progressive evolution of the carbon metabolism of both P. oceanica and its epiphytes throughout the year (Fig. 9a, b) . Photosynthet ic efficiency (deduced from the P - I slopes) seems to follow the usual pa t te rn of sun-shade adaptat ion during the season. In both P. ocean- ica and its epiphytes photosynthet ic efficiency is at its maximum during winter (November - Janua ry ) and decreases to a minimum level in summer.

DISCUSSION

Principal componen t analysis

The P.C.A. shows in a quanti tat ive manner the pre-eminence of the irradi- ance (" lu") over the other factors for regulating the in situ productivity of P. oceanica and its epiphytes. The distribution of the other parameters which develop in a seasonal t rend along Axis I, such as water alkalinity, temperature, pH, epiphyte biomass or leaf surface area, shows that they have no influence on the pr imary productivity. Thus primary productivity of both P. oceanica and its epiphytes seems essentially to be a function of irradiance. In this study, owing to the absence of other explanatory factors, irradiance is sufficient to build a satisfactory predictive model for pr imary production of the seagrass. The working hypothesis is that the water and sediment concentrations of NH4 +,

299

TABLE V

Reeve's analysis applied on different groups of productivity-irradiance regression lines ~

(a) P. oceanica

Curves Slope test Position test Fo.o5 Foo, fd 2

Totality 7 curves F = 2.55* F = 12.55"** 2.19 2.99 6,98

March-April 81 May-June 81 Sept.-Oct. 81

F-- 5.86*** F= 3.46* 3.21 5.12 2,44

Nov.81-Jan. 82 March 82 May-June 82

F= 1.15 NS F--10.10"** 2.76 - 3,59

Nov.81-Jan. 82 March 82 F= 1.73 NS F-- 1.62 NS 3.28 - 2,35

Nov.81-Jan. 82 March 82 May-June 82

F= 1,18 NS F-- 14.98"** 3.15 - 2,60

Nov.81-Jan. 82 May-June 82 F= 12.17"** F= 29.63*** 4.08 - 1,40

(b) Epiphytes

Curves Slope test Position test Fo.os Fo.ol fd

Totality 6 curves F= 2.44* F-- 18.47"** 2.31 3.21 5,98

March-April 81 May-June 81 Sept.-Oct. 81

F= 4.65* F= 5.48*** 3.20 5.11 2,45

March-April May-June 81 Sept.-Oct. 81

Nov.81-Jan. 82 March 82 May-June 82

March-Oct. 81 Nov.-Jan. May-June 82

F= 9.79*** F= 8.96*** 4.05 7.20 1,47

F= 1.73 NS F=19.09"** 3.15 5.01 2,55

F= 5.68* F-- 28.76"** 3.94 6.90 1,106

1"Fobs < Foos; "'Fob8 < Foo,; ""Fobs < Fo oo,. 2fd = freedom degrees.

300

#g C gDW-lh -1 N o v . 8 1 - J a n . 8 2

® , 1~ March-april 81

~ g e g D W - l h -1 Nov.81 (~) May-June 81 @ ~ Jan.82 1300 -

I / March 82 / J i ~) /~ May-June 82 " ! / / / I , , • 1 1 0 0 -

' ,, , " // i I d S 700 March april t l

May- une '-

5 0 0 f / t ~ 700 -

500 - y81

3 0 0 ] 3 0 0 -

P. o c e a n i c a W//J E p i p h y t e s lOO lOO - p "

:2 3 4 Em-2h-1 ; 2 3 4 E m - 2 h -I

Fig. 9. Seasonal variation in productivity-irradiance curves of (left) P. oceanica and (right) its epiphytes.

NO3- and PO43- are not limiting factors, which has not yet been verified, except where PO43- is concerned (Delgado-Torrbs, 1985).

Comparison o/productivity o/P. oceanica and its epiphytes

Although epiphytic biomass and chlorophyll content are lower than those of P. oceanica (Libes, 1984b), productivity is twice as high for epiphytes as for P. oceanica (Fig. 6). The ash fraction of epiphytes on seagrasses is consider- able: it can reach 40-50% in P. oceanica (as compared to 46-76% in Zostera marina L. (Penhale, 1977) and 23-33% in Thalassia testudinum Banks ex KSnig ( Capone et al., 1979) ). Thus the actual productivity of the living algae fraction (expressed as ash-free dry weight) should be around twice as much as the one we measured. Similarly the high variability of the measurements mainly originates from the large and fluctuating fraction of inorganic and animal material in the epiphyte samples. The high productivity of the epiphytes orig- inates from their high turnover rate (Panayotidis, 1980; Panayotidis and Giraud, 1981 ).

As previously noted by Penhale (1977) and Capone et al. (1979) there was a similarity between the P - I curves of P. oceanica and its epiphytes (Fig. 6). In spite of considerable taxonomic differences of these components, the same

301

saturating and inhibiting irradiance were regularly observed. These results suggest that the primary productivity patterns of the host-macrophyte and its epiphytes are closely interrelated. This kinetic similarity in assimilation may reflect a rapid pooling of newly formed photosynthates in both components which may distort the real productivity of each of them.

Relation between productivity and productivity factors

The initial linear phase and the saturation phase of the P- I curves show a typical hyperbolic relation which is common when considering most of the relations between the production of an organism and the regulating environ- mental variables (e.g., light, nitrogen, phosphorus, chlorophyll, CO2 concen- tration; Margalef, 1977). Beer and Eshel (1983) observed this relationship when studying the dependancy of photosynthesis on CO2 and HCO3- concen- tration for Ulva sp. Thursby and Harlin (1982) and Iizumi and Hattori (1982) observed the same when the growth rate of Zostera marina was described as a function of NH4 + concentration in the sediment. By contrast, the photoinhi- bition phase is not always observed for all plants. In some cases, depending on the ecological characteristics of a given biotope (latitude, depth, temperature, plant density, shading, etc.) inhibiting light intensities are not reached. Drew (1978) and Bay (1978, 1984) observed no photoinhibition for P. oceanica, at a water depth of 10 m.

Saturating and inhibiting irradiances

The irradiances inducing photosynthesis saturation and photoinhibition are highly variable according to the species and biotopes studied, giving evidence of physiological adaptations to different environmental conditions. Light adaptations have mainly been demonstrated in phytoplankton (Steemann- Nielsen, 1975 ) but are also found among vascular plants, where the usual pat- tern corresponds to the "sun-shade" adaptation model. Usually, the sun- adapted plants exhibit a low photosynthetic efficiency ( slope of the P-I curve), a high saturation level and photoinhibition is rarely observed. In shade-adapted plants, high photosynthetic efficiency is found while light saturation and pho- toinhibition occur at lower irradiances. Jones and Adams (1982) demon- strated this general trend for epiphytes on MyriophyUum spicatum L. Adaptation to different light regimes may be a function of several parameters such as temperature (Bulthuis, 1983), season, depth, latitude, shading, etc. Salvucci and Bowes (1982) showed major differences in light dependency between aerial and submerged leaves of MyriophyUum brasiliense Cambess. Aerial leaves continuously exposed to high irradiances were not saturated until ca. 2000 p~E m -2 s -1 whereas submerged shade-adapted leaves were already saturated at 250-300 ~tE m -2 s- 1. In benthic algae, Vooren (1981) showed that

302

the saturating irradiance decreased with increasing depth. Williams and McRoy (1982) showed that higher irradiances are needed to saturate photosynthesis of marine phanerogams in the tropics than in temparate climates. Finally, Pen- hale (1977) in a Zostera marina bed located in North Carolina (U.S.A.) observed photosaturat ion at 600 HE m -2 s - 1 whereas McRoy (1974) in Alaska for the same species found this value at 360 HE m -2 s-1.

It should be noted that for P. oceanica saturation and inhibition levels vary noticeably from one year to another. In May-June 1981 the saturation phase occurred at about 3 E m-2 h - 1 ( 830 H E m -2 s - 1 ) and photoinhibition was not observed. In May-June 1982 the photosaturation was observed at about 2 E m -2 h -1 (560 HE m -2 s -1) and inhibition at about 3 E m -2 h -1. At present these differences cannot be explained by any variability in production factors. The differences are most probably due to different light conditions in the days before or on the day of incubation.

Circadian variations in productivity and photosynthetic efficiency

Photosynthetic efficiency of P. oceanica exhibits circadian variations. The efficiency is usually higher in the morning, decreases at noon with increasing irradiances and then increases again in the evening. During summer, this t rend changes somewhat since the higher irradiances induce photoinhibition and this effect persists until the end of the day. The same general t rend has also been observed by Gattuso and Jaubert (1985) for Caulerpa racemosa (Forsk.) J. Ag. and by Sournia (1974) on the coral reefs. The origin of such variations may depend on multiple factors among which light conditions is the main one. Under constant irradiance, Levavasseur and Giraud (1982) showed significant variations of oxygen release in Ulva gigantea (Kiitzing) Bliding, which suggest the existence of a photosynthetic activity rhythm. The same authors pointed out the influence of light pre-exposure on photosynthesis, i.e. "net photosyn- thesis decreases with increasing pre-exposure duration". This decrease in pho- tosynthetic capacity may also be induced by a physiological regulation linked with the accumulated amylaceous storage in the tissues. Photosynthetic aci- tivity may decrease with glucide retention and be stimulated under opposite conditions. Levavasseur and Giraud (1982) measured an increase in thallic starch content in relation to light duration which may explai n the photosyn- thetic variations they observed.

Concerning P. oceanica, little is known about the real factors which regulate circadian variations. We think, as does Ott (1979), that there is an endogenous rhythm of photosynthetic capacities, as well as a polysaccharide accumulation in the leaves and rhizomes (Pirc, 1985), which can inhibit further carbon assimilation.

303

Seasonal variations in photosynthetic efficiency and productivity

The photosynthet ic efficiency of P. oceanica is highest in winter when low irradiances are sufficient to induce maximum photosynthesis without inducing photosaturat ion or photoinhibit ion. During spring, efficiency decreases with increasing mean irradiances and daylight duration. It reaches a minimum value in summer as was suggested by Drew (1978).

These seasonal variations in the metabolism of both P. oceanica and its epi- phytes correspond most probably to physiological adaptat ions allowing them to have maximum benefit of available light. Such adaptat ions have also been observed as a function of depth (Vooren, 1981 ). The results of Bay (1978) also show slope differences in the P - I relation, but these do not follow a seasonal logic. They appear to depend more on water temperature.

ACKNOWLEDGEMENT

I wish to thank Dr. Marie-Reine Plante-Cuny (Centre d'Ocdanologie de Marseille, Stat ion marine d 'Endoume) and Prof. Ch-F. Boudouresque (Laboratoire d'Ecologie du Benthos et de Biologie vdgdtale marine, Facultd des Sciences Luminy, 13288 Marseille, France) for their constructive criticism of the manuscript, and Prof. Henri Jupin and Dr. Alain Sournia for their help in the interpretat ion of results. I am particularly grateful to Dr. Jean-Claude Fardeau and the D B / S R A (C.E.N. Cadarache, St Paul lez Durance, France) for their cooperation and assistance in treating the labelled samples, and to Dr. R. Plante for his help in translat ing the manuscript. This s tudy was sup- ported by a contract with the National Park of Port-Cros (Var, France) , and the "Agence Franqaise pour la Maitrise de l 'Energie" ( A.F.M.E. ).

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