Marine Biology 62, 111-117 (1981) MARINE BIOLOGY �9 Springer-Verlag 1981

Do Correlations Exist Between Chromatophore Arrangement and Photosynthetic Activity in Seaweeds?

W. Nultsch, J. Pfau and U. Riiffer

Lehrstuhl fiir Botanik, FB Biologie der Universi6it Maxburg/Lahn; D-3550 Marburg/Lahn, Germany (FRG)

Abstract Introduction

In Dictyota dichotoma, as in many other plants, the chromatophores which at low intensities occupy the cell walls perpendicular to the light beam move to the side walls parallel to the light beam if exposed to high light intensities. The aim of this investigation was to find out whether or not the changes from low- to high-intensity arrangement and vice versa function as an active control mechanism to regulate photosynthetic activity in D. dichotorna under the respective light condition. Four different experimental approaches were made: (a) In white and blue light experiments the changes of the transmittance and of the rate of photosynthetic oxygen production in high- and low-intensity arrangement were compared. (b) The kinetics of the depression and recovery of the PS-rates, as well as of the transmittance changes, were determined during high- and low-intensity move- ment, respectively. (c) Transmittance and PS-rates of thalli under illumination with polarized and unpolarized light of the same intensity (1,000 lx) were compared. (d) PS-rates of thalli after darkening as well as after pre- irradiation with weak and strong red light, conditions under which the chromatophores occupy the same position in the cells, were measured. In all these experi- ments the photosynthetic activity was strongly influenced by pre-illumination, but was independent of the respec- tive chromatophore arrangement. This finding was confirmed by experiments with two other algae: (1) In the brown alga Alaria esculenta which does not display light-induced chromatophore displacements and con- comitant transmittance changes, pre-irradiation with high light intensities decreases the PS-rates. (2) In file green alga Ulva lactuca, which shows circadian chloro- plast movements, the PS-rates depend on the pre-irradia- tion only, irrespective of the chloroplast position. Thus we may conclude that in these organisms the function of chromatophore displacements is not the regulation of photosynthetic activity. Other ecological functions are discussed.

Light-induced displacements of chloroplasts are wide- spread among higher plants, ferns, mosses and fresh- water algae (see reviews by Senn, 1908; Haupt, 1959, 1963, 1965; Zurzycki, 1962; Haupt and Schgnbohm, 1970; Britz, 1979). As shown by Nultsch and Pfau (1979), light-induced chromatophore displacements also occur in seaweeds, especially in brown algae. These movements induced by light have to be clearly distin- guished from circadian chromatophore movements which are governed by the physiological clock, as repor- ted byBritz (1976, 1979) for the green alga Ulva lactuca.

The chromatophores of the brown alga Dictyota dichotoma, the phaeoplasts, display 3 characteristic arrangements: the lowqntensity arrangement, the high- intensity arrangement and the dark arrangement (Pfau et al., 1974; Rtiffer et al., 1981). In low-intensity arrangement almost all of the phaeoplasts occupy the cell walls perpendicular to the light direction (=face position). This is caused by white light of about 1,000 lx or by blue light (440 rim) of about 1 W m -2 . With increasing light intensity a growing number of phaeo- plasts move to the side walls parallel to the light beam. The complete high-intensity arrangement in which most of the phaeoplasts occupy the side walls (= profile position) is achieved above 12,000 lx white light and 25 W m -2 blue light, respectively. In darkness phaeo- plasts are found at the anticlinal and the inner periclinal cell walls, whereas the outer periclinal walls are nearly free from phaeoplasts.

As already observed by Biebl (1954), the movements from face to profile position and vice versa cause-due to the Beer's law - corresponding transmittance changes. The transmittance of the thalli in the high-intensity arrangement is higher than in the low-intensity arrange- ment. For absorbance the contrary is true. As shown by Pfau et al. (1974) and Nultsch and Benedetti (1978), these transmittance changes measured microphoto-

0025-3162/81/0062/0111/$01.40

112 W. Nultsch et al.: Chromatophore Arrangement and Photosynthesis in Seaweed

100- %

80-

60-

40-

20-

/~

/ e

/

/

' 1'o

Fig. 1. Dictyota dichotoma. Irradiance-response curve of photosynthetic O 2 production measured at 672 nm. Abscissa: irradiance in Win-2; ordinate: photosynthesis rate in relative units

100 %

80

60-

40-

20-

f j f~ //I Jj //I

fj //I f~ 11.-i

11 .i.~

"" / /

f /

f ~

~ J

/ J i

I II Ill

Fig 2. Dictyota dichotoma. Relative PS-rates of the same thal- lus, measured at 439 nm (1.2 W m -2 ), after irradiations with weak and strong white light. (I) 16 h, 1,0001x; (II) 4 h, 20,000 Ix; (III) 4 h, 1,000 Ix

metrically can be used as a measure of the phaeoplast displacement.

Zurzycki (1955) has shown with the seed plant Lernna trisulca L. and the moss Funaria hygrometrica that the rate of photosynthesis increased after the illumination had been changed from high to low intensities. He con- cluded that this increase was due to the absorbance increase caused by the movement of chloroplasts from the prof'fle to the face position. This, however, might not be true for the green alga Mougeotia sp. in which the rate of photosynthesis reaches its new level before the chloroplast has occupied the face position (Zurzycki, 1955). Lechowski (1974) has found that in the higher plant Ajuga reptans the rate of photosynthesis in the high-intensity arrangement was reduced to about 50% compared to that in the low-intensity arrangement, although the change in light absorption caused by this movement was only about 6%.

Since Dictyota dichotorna and several other brown algae which display light induced chromatophore dis- placements live in the intertidal belt, they are frequently

exposed to direct sunlight at low tide. Thus, correlations between chromatophore arrangement and photosynthesis may also be expected in these algae.

Material and Methods

The same strain of Dictyota dichotoma (Huds.) Lamour as in earlier investigations (Pfau et al., 1974) was used. The thaUi were grown in a modified Schreiber-solution under an illumination of 1,000 lx fluorescent light in a 14 h L:10 h D regime. Growth rate was increased by aerating the cultures. Details of the culture method are described elsewhere (Pfau, 1974). Ulva lactuca L. had been sampled from the rocky shore of the island of Helgoland immediately before starting the pre-illumina- tion. Alaria esculenta (L.) Grev. thaUi were obtained from Dr. K. L/ining, Helgoland.

In general the transmittance changes were measured by means of a single beam recording microphotometer (Pfau et al., 1974), in which the stimulus light was also used as measuring light. For comparing the effects of different wavelengths a dual-wavelength recording micro- photometer was developed (Pfau et al., 1981) in which different wavelengths could be used for stimulus and measuring light. Red and blue light were produced by inserting SFK filters 16 and 20, respectively (Schott and Gen., Main). The experiments were carried out in a con- stant temperature room (15 ~ + 0.2 C~

The relative PS-rates were measured by means of a platinum/silver electrode (Hydro-Bios, Kiel). Discs of 5 mm diameter were cut out of the Dictyota dicho- toma thalli with a cork borer and placed on the surface of the electrode. The electrode was mounted in a small flow-through cuvette with a window which allowed illumination of the thallus disc from the free side. Nutrient medium was passed along this free disc surface providing a constant temperature and a constant partial pressure of 02. On the electrode side of the thallus disc a constant 02 pressure also appears in darkness due to the diffusion. Photosynthetic oxygen production by the alga results in a proportional increase of the O2 pressure on the electrode side. Oxygen production was measured in weak light of equal photon fluence rates in the blue (1.2 W m -2 ,BG 28) and in the red (0.8 W m -2 , SFK 16). This photon fluence rate lies in the linear part of the irradiance-response curve measured in red light (Fig. 1.).

Results

White and Blue Light Experiments

The rates of oxygen production of the same Dictyota dichotoma thallus disc were measured in weak blue light (1.2 W m -2) after subsequent irradiations with white light of 1,000 lx for 16 h (phaeoplasts in a low-inten- sity arrangement), 20,000 lx for 4 h (phaeoplasts in a high-intensity arrangement) and again 1,000 lx for 4 h. As shown in Fig. 2, the O2 production of thaUi with

W. Nultsch et al.: Chromatophore Arrangement and Photosynthesis in Seaweed 113

100- %

80-

50-

+~ t 20

\ \.

\ I

%0. ?~_,___.~__.~ 9 ~ , ~ ._ ._ + ? 1 2 3 4. h

Fig. 3. Dictyota dichotoma. Comparison of the kinetics of highqntensity movement and PS-rate depression in strong blue fight (48 W m -a) after a pre-irradiation with weak blue fight (1.2 W m -a ). Measuring light for PS-rate: 439 nm, 1.2 W m -a . Transmittance as a measure of high-intensity movement (inver- ted): closed circles, solid line; PS-rate changes: open circles, dashed line. Abscissa: time in hours; ordinate: transmittance (T/To) and PS-rate, both in relative units. For comparison of the kinetics the curves were normalized at two ordinate points: 0 and 100%

t00- %-

80-

% -

4.0-

20-

+/"

0000"0- - - - 0 . . . . . . . . . . . . . 0

o / o / o / o / o / o ~ . O ~176 ~ 1 7 6 I - - ~ ~ ~ ~ ~ ~ ~ ~ ~ P 9 r

/ / . /

/ /

i 2 3 4 5 5 7 ~ h

of high-intensity irradiation. Similar differences are found when the kinetics of low-intensity movement are compared with the kinetics of PS-rate increase after decreasing the light intensity from 48 to 1.2 W m -2 (Fig. 4). The depression of oxygen production caused by high-intensity irradiation does not correspond quanti- tatively with the total transmittance change of the Dictyota dichotoma thallus caused by high4ntensity movement. Whereas the depression of the PS-rate amounts to about 75%, the real difference between the transmittance in the high4ntensity arrangement (6%) and the low-intensity arrangement (3%) is only 3% refer- red to the transmittance of the nutrient medium = 100%.

Experiments with Polarized Light

In order to find out whether the pre-illumination per se or the phaeoplast arrangement induced by the pre- illumination or both are responsible for the changes of the PS-rates, we have to compare the PS-rates of 2 thalli with either different phaeoplast arrangements in spite of the same pre-irradiation or with the same phaeoplast arrangements in spite of different pre-irradiation. To achieve the first situation, experiments with weak polarized and unpolarized light seemed promising, since preliminary investigation had shown that the chromato- phore arrangement in weak poiarized light resembles the high-intensity arrangement as in many other plants (Zurzycki, 1967, 1969). But unfortunately a more detailed analysis (Pfau et al., 1979) has revealed that in weak polarized light chromatophores do not move quan- titatively to the side walls, thus causing only transmit- tance changes of 5 to 20% referred to those caused by high-intensity movement.

Fig. 4. Dictyota dichotoma. Comparison of the kinetics of low- intensity movement and PS-rate recovery in weak blue light (1.2 W m -a ) after a pre-irradiation with strong blue light (48 W m-2). Measuring light for PS-rate: 1.2 W m -2, 439 nm. Trans- mittance as a measure of low-intensity movement: closed circles, solid line; PS-rate changes: open circles, dashed line. Abscissa: time in hours; ordinate: transmittance (T/To) and PS-rate, both in relative units. Curves normalized as in Fig. 3

phaeoplasts in a tow-intensity arrangement is up to 3 to 4 fold higher than that of thalli with phaeoplasts in a high-intensity arrangement. Similar results were obtained with blue light (439 nm) at irradiances of 1.2 and 48 W m -z , respectively.

These results seem to be consistent with those of Zurzycki's (1955, 1975) and Lechowski's (1974) experi- ments with higher plants. However, if the kinetics of high-intensity movement under continuous blue light irradiation (48 W m -2) following a pre-irradiation with 1.2 W m -2 are compared with the kinetics of the PS-rate depression occurring under the same light conditions, striking differences are found (Fig. 3). While the complete profile position is achieved after 3 to 4 h, the final rate of oxygen production is reached within 1 h after onset

Red Light Experiments

Therefore, another experimental way was devised in which the intensity of the pre-illumination was different, while the phaeoplast arrangement was the same. Obser- vations by microscope had revealed that after irradiation with red light the phaeoplast arrangement of Dictyota dichotoma resembles the dark arrangement very closely, independent of the irradiance. Chromatophore arrange- ments in darkness as well as after weak and strong red light irradiation are shown in Fig. 5 A-C.

Transmittance measurements confirm these findings. If thalli with phaeoplasts in low-intensity arrangement, induced by weak blue light irradiation (1.2 W m-2), are irradiated with either weak (0.8 W m -2) or strong red light (32 W m-2), the transmittance changes caused are of about the same size as those caused by darkness (Fig. 6).

Thus, we compared the PS-rates of thallus discs after exposure to different light conditions: darkness, strong and weak red light (672 nm). The photon fluence rates were the same as in the previous blue light experiments, i.e., 0.8 and 32 W m -2 , respectively. As shown in Fig. 7

114 W. Nultseh et al.: Chromatophore Arrangement and Photosynthesis in Seaweed

"D" b b R b "O" b

Fig. 6. Dietyota diehotorna. Transmittance changes of a thallus caused by successive exposure to relative darkness ("D" = 4 .10 -4 W m -2 , BG 28), weak blue light (b = 1.2 W m-2), weak red light (r = 0.8 W m -2) and strong red light (R = 32 W m-2). Abscissa: time in hours; ordinate: transmittance (T/To) in rela- tive units

100-~ % 00-

00-

40-

20-

[ 7 " 7

l / / / / / / / / / / / " / /

/ / / /

l / / / / / / / / / / / / / / / / ' /

l /

/ / / / / / / / / /

/ / / /

/ / ~ / / / / / / / / / / / / - / /

I II III

Fig. 7. Dictyota diehotoma. Relative PS-rates of one thallus after exposure to darkness as well as strong and weak red light. (I) Darkness, 20 h; (II) 32 W m -2, 4 h; (III) 0.8 W m -n, 1 h. Measu- ring light: 0.8 W m-=, 672 nm

Fig. 5. Dietyota dichotoma. Photomicrographs of phaeoplast arrangements in the cortical cells (ca 480x). (A) after 24-h dark- ness. (B) after 24-h irradiation with weak red light (0.8 W m-= ). (C) after 24-h irradiation with strong red light (32 W m-2). Focus was given on the inner periclinal walls above the lumina of the underlying large medullary cells. In the same plane the anti- clinal walls of the cells above the walls of the medullary cells are to be seen. Objects were fixed and stained as described by Riiffer et al. (1978)

the PS-rate after irradiation with weak red light (0.8 W m -2) was about the same as after darkening, whereas the irradiation with strong red light (32 W m -2) reduces the PS-rate to less than 20% of the dark value, similar to the white and blue light experiments.

As demonstrated by the transmittance measurements the number of the photons absorbed by the phaeoplasts in the high-intensity arrangement is significantly smaller than in the dark arrangement, which is also occupied by the phaeoplasts in red light (see above). Therefore, one should expect that the PS-rate depression caused by high4ntensity irradiation would be stronger in the blue than in the red. However, as shown in Fig. 8, the oppo- site is true. If a thallus disc is exposed to successive 4 h periods of strong blue and red light of equal photon fluence rates, the depression caused by red light is even stronger than the one caused by blue light.

The kinetics of the PS-rate depression in strong red light are relatively fast and similar to those in the blue light experiment. Fig. 9 shows the kinetics of PS-rate depression of one thallus disc caused by high4ntensity irradiation with strong blue and red light, respectively. The stronger effect of strong red light compared with blue light of equal photon fluence rate is obvious again (see Fig. 8). The kinetics of PS-rate recovery in weak red light after 4 h of pre4rradiation with strong red light (Fig. 10) is similar to the kinetics of the PS-rate depres- sion.

W. Nultsch et al.: Chromatophore Arrangement and Photosynthesis in Seaweed 115

100- % BO-

60-

40-

20-

D R B R B R B D

"D" b B r "O" b

I i 1 1 1 1

10

5 / C Z 4 ~i 8 1'0 II2

Fig. 8. Dictyota dichotoma. Relative PS-rates of one thallus disc after successive 4-h exposures to strong red light (R = 32 W m -z ) and strong blue light (B = 48 W m-2). Measuring light: 0.8 W m -z , 672 nm. Dark controls at the beginning and end of the experiment

100- %

B0-

60-

40-

20-

~ i ~ - o . . . . . . . . . o . . . . . . . . o . . . . . . . . . o

Fig. 9. Dictyota dichotoma. Kinetics of the PS-rate depression caused by strong red light (32 W m -z , closed circles, solid line) and strong blue light (48 W m -z , open circles, dashed line) in a thallus disc which had been exposed to weak red light (0.8 W m -2 ) before the onset of high-intensity irradiation. Measuring light: 0.8 W. m -z , 672 rim. Abscissa: time in hours; ordinate: PS-rate in relative units

Fig. 11. Alaria esculenta. Transmittance changes of a thallus caused by successive exposures to relative darkness ("D" = 4 �9 10 -4 W m -z , BG 28), weak blue light (b = 1.0 W m-2), strong blue light (B = 17 W m -z) and weak red light (r = 0.65 W m-~). Abscissa: time in hours; ordinate: transmittance (T/To) in relative units

100- %

80-

50-

z,0-

20-

/ / !

J . < J / i J / i

F

i f f J ~

I II Ix/

I / j / /

/ j

/ /

III

7 - 7 / / , / / / / / / / / / / / / / / / / / /

/ /

/ /

[ / / / /

V

Fig. 12. Alaria esculenta. Relative PS-rates of a thallus disc after: (I) Darkness, 12 h. (II) Strong blue light (48 W m -2, 12 h). ( l id Weak blue light (1.2 W m -z, 12 h). (IV) Strong red light (32 W m -z , 12 h). (V) Weak red light (0.8 W m -2 , 12 h). Measu- ring light: 0.8 W m -z, 672 nm

100- % 80-

50-

40-

20-

e/e,~ e ~ e ~ l /

/ /.

/. /

I I

1 Z 3 h

Fig. 10. Dictyota dichotoma. Kinetics of the PS-rate increase in weak red light (0.8 W m -z) of a thallus disc which had been pre- irradiated with strong red light (32 W m -2) for 4 h. Abscissa: time in hours; ordinate: PS-rate changes in relative units

Invest igat ions with Other Algae

In order to suppor t the results ob ta ined with Dictyota dichotoma some addit ional exper iments were carried out wi th other algae, main ly Alaria esculenta and UTva

lactuca. A. esculenta, a b rown alga wi th a broad, flat thallus, was of special interest in this connec t ion . In this alga no phaeoplast displacements and, hence, no corresponding t ransmi t tance changes could be caused by changing the blue light i r radiat ion from low (1 W m -2) to high- intensi ty (17 W m -2) and vice versa (Fig. 11). Only by darkening or by i r radiat ion with weak or s trong red light is t ransmi t tance slightly bu t significantly increased, obviously as a result o f a special dark ar rangement of the phaeoplasts. Al though no t ransmi t tance changes are caused by increasing the blue irradiance, a significant depression of the PS-rate is observed (Fig. 12). The same is t rue for s trong red light (Fig. 12), though the t ransmi t tance of thaUi irradiated with weak or s t rong red light is the same as in darkness.

In Ulva lactuca only circadian chloroplast movements occur, as shown by Britz (1976) . I f some plants are grown in a normal and some others in an inverse light: dark regime (12 h L :12 h D) and then darkened for 12 or 24 h, it is possible to ob ta in at the same t ime plants with chloroplasts in face and in profile posi t ion, bo th adapted to darkness. I f n o w the pho tosyn the t i c oxygen

116 W. Nultsch et al.: Chromatophore Arrangement and Photosynthesis in Seaweed

100- %

80-

60-

4,0-

20-

FP

# / /

PP

/ / / / / /

z Z Z / /

z z ,

z z z

I

PP FP

/ / / / / /

r162

/ /

# II

FP FP

//

/i

f/ Ii

Z

III I7

Fig. 13. Ulva lactuca. Relative PS-rates of two thaUi (I and II) with chloroplasts in face (FP) and profile (PP) position after a darkening period of 12 and 24 h respectively. For comparison another U. lactuca thallus in face position after irradiations with white light of 20,000 lx (III) and 1,000 lx (IV). Measuring light: 0.8 W m -2, 672 nm

production of these plants with different chloroplast arrangement is compared, the PS-rates are of the same order of magnitude (Fig. 13). On the other hand, by high-intensity irradiation the PS-rates were decreased to about 50% of the weak light value (Fig. 13), independent of the chloroplast position.

Discuss ion

In all 3 seaweeds investigated -Dictyota dichotoma, Alaria esculenta and Ulva lactuca - the rate of the photo- synthetic oxygen production is strongly decreased by pre-irradiation with white as well as monochromatic blue and red light of high-intensity. This decrease of the PS- rate is independent of the respective arrangement of the chromatophores within the cells. Consequently in these organisms the function of chromatophore displacements is obviously not the regulation of the photosynthetic activity, as suggested by Zurzycki (1955, 1976) and Lechowski (1974) for higher plants and mosses.

These Findings are in good agreement with the obser- vation by Titlyanov et al. (1978) that in Ulvafenestrata changes in photosynthetic capacity were correlated with changes in the chlorophyll content but not with the chloroplast position. In addition, they obtained similar results with Enteromorpha linza in which no chloroplast movements can be detected. Recently, Witztum et al. (1979) have reported that in a mutant strain of Lemna paucicostata light-induced chloroplast displacements occur although the photosynthetic electron transport chain is blocked between plastoquinone and cytochrome f. Furthermore, DCMU did not prevent chloroplast dis- placement in bright light, neither in the normal strain nor in the mutant. These findings suggest that also in the genus Lemna chloroplast movement might not be coupled with photosynthesis.

Two questions arise: (1) What is the biological func- tion of the chromatophore movement if not the regula- tion of photosynthetic activity? (2) How is the photo-

synthetic activity regulate d if not by chloroplast arrange- ment?

The first question cannot yet be answered satisfac- torily. As it has been demonstrated by Nultsch and Pfau (1979), with several different Fucus species investigated, the intensity dependence of light-induced transmittance changes brought about by phaeoplast displacements (Riiffer et al., 1978)corresponds well with their zonation in the intertidal belt. Since the regulation of photo- synthesis is apparently not the function of these phaeo- plast displacements, one could imagine that the high- intensity movement and the concomitant decrease of absorbance (= increase of transmittance) protects the algae from photodamage.

The decrease of the photosynthetic activity after high-intensity irradiation could have different reasons. The effects of high light intensities on various algae have already been studied by Noddak and Eichoff (1939) and Steeman Nielsen (1962). Moreover, individual aspects of the influence of light intensities on the ratio of chloro- phyll a/b (Reger and Krauss:. 1970), photosynthetic rates (Godvindjee et al., 1967; Oquist, 1974) and photosyn- thetic units (Myers and Graham, 1971) have been investigated. Recently, the adaptation of the photosyn- thetic apparatus of the green alga Scenedesmus obliquus to strong light conditions has been studied in detail by Senger and Fleischhacker (1978) and Fleischhacker and Senger (1978). However, since in most of these papers the photosynthetic capacity was determined, their results cannot satisfactorily explain the effect of high intensities on the rate of photosynthesis reported in this paper. Therefore, more detailed investigations in this field are necessary.

Acknowledgements . We are indebted to the Deutsche Forschungsgemeinschaft for financial support and to Professor Dr. O. Kinne for giving us the facilities to carry out some of these studies in the marine station of the Biologische Anstalt Helgoland. We thank Dr. K. Liining for culture material ofAlaria esculenta, and Mrs. G. Puhe and Mrs. M. Tidow for technical assistance.

Literature Cited

Biebl, R.: Lichttransmission und Chloroplastenbewegung. Flora 141,163-177 (1954)

Britz, St. J.: Studies on a circadian rhythm of chloroplast move- ment in Ulva, 228 pp. Thesis, Cambridge Mass. (1976)

Britz, St. J.: Chloroplast and nuclear migration. In: W. Haupt and M. E. Feinleib (Eds.) Physiology of movements, Encyclo- pedia of plant physiology, New Series, Vol. 7, pp 170-205, Berlin, Heidelberg, New York: Springer-Verlag 1979

Fleischhacker, Ph. and H. Senger: Adaptation of the photosyn- thetic apparatus of Scenedesmus obliquus to strong and weak light conditions. II. Differences in photo-chemical reactions, the photosynthetic electron transport and photosynthetic units. Physiol. Plant. 43, 43-51 (1978)

Govindjee, G. Papageorgiou and E. Rabinowitch: Chlorophyll fluorescence and photosynthesis. In: G. G. Guibault (Ed.) Fluorescence theory, instrumentation and practice, New York: M. Dekker Inc. 1967

W. Nultsch et al.: Chromatophore Arrangement and Photosynthesis in Seaweed 117

Haupt, W.: Chloroplastenbewegung. ln: W. Ruhland (Ed.) Handbuch der Pflanzenphysiologie, 17/1, pp 278-317. Berlin, G6ttingen, Heidelberg: Springer 1959

Haupt, W.: Photoreeeptorprobleme der Chloroplastenbewegung. Ber. Dtsch. Bot. Ges. 76, 313-322 (1963)

Haupt, W.: Perception of environmental stimuli orienting growth and movement in lower plants. Ann. Rev. Plant Physiol. 16, 267-290 (1965)

Haupt, W. and E. SchSnbohm: Light-oriented chloroplasts move- ments. In: P. Halldal (Ed.) Photobiology of microorganisms. pp 283-307. London, New York, Sidney, Toronto: Wiley- Interscience 1970

Lechowski, Z.: Chloroplast arrangement as a factor of photo- synthesis in multilayered leaves. Acta Soc. Bot. Pol. 43, 531-540 (1974)

Myers, J. andJ. -R. Graham: The photosynthetic unit in Chlorella measured by repetitive short flashes. Plant Physiol. 48, 282- 286 (1971)

Noddack, W. and H. I. Eichoff: Untersuchungen fiber die Assimi- lation der Kohlens'~iure durch die griinen Pflanzen. II. Assimi- lation und Lichtintensit~it. Z. phys. Chem. 185, Abt. A, 222- 237 (1939)

Nultsch, W. and J. Pfau: Occurrence and biological role of light- induced chromatophore displacements in seaweeds. Mar. Biol. 51, 77-82 (1979)

Nultsch, W. and P. A. Benedetti: Microspectrophotometric measurements of the light induced chromatophore move- ments in a single cell of the brown alga Dictyota dichotoma. Z. Pflanzenphysiol. 87, 173-180 (1978)

Oquist, G.: Distribution of chlorophyll between the two photo- reactions in photosynthesis of the blue-green alga Anacystis nidulans grown at two different light intensities. Physiol. Plant. 30, 38-44 (1974)

Pfau, J.: Studien zur Chromatophorenbewegung der Braunalge Dictyota dichotoma. 146 pp. Thesis, Marburg (1974)

Pfau, J., G. Throm and W. Nultsch: Recording microphotometer for determination of light-induced chromatophore movements in brown algae. Z. Pflanzenphysiol. 71,242-260 (1974)

Pfau, J., U. Riiffer and W. Nultsch: Der Einflu$ polarisierfen Lichtes auf die Chromatophorenanordnung yon Dictyota dichotoma. Ber. Dtsch. Bot. Ges. 92,695-715 (1979)

Pfau, J., W. Nultsch and U. Riiffer: Action spectra of phaeoplast displacement in Dictyota dichotoma measured with a dual wavelength recording microphotometer. (In preparation) (1981)

Reger, B. J. and R. W. Krauss: The photosynthetic response to a

shift in the chlorophyll b ratio of Chlorella. Plant Physiol. 46, 568-575 (1970)

Rfiffer, U., W. Nultsch and J. Pfau: Untersuchungen zur lichtinduzierten Chromatophorenverlagerung bei Fucus vesiculosus. Helgol~nder wiss. Meeresunters. 31, 333-346 (1978)

Rfiffer, U., J. Pfau and W. Nultsch: Movements and arrangements of Dictyota phaeoplasts in response to light and darkness. Z. Pfianzenphysiol. 101,283-293 (1981)

Senger, H. and Ph. Fleischhacker: Adaptation of the photosyn- thetic apparatus of Scenedesmus obliquus to strong and weak light conditions. I. Differences in pigments, photo- synthetic capacity, quantum yield and dark reactions. Physiol. Plant. 43, 35-42 (1978)

Senn, G.: Die Gestalts- und Lagever'~nderungen der Pflanzen- Chromatophoren. 397 pp. Leipzig: Engelmann 1908

Steeman Nielsen, E.: Inactivation of the photochemical me- chanism in photosynthesis as a means to protect the ceils against too high light intensities. Physiol. Plant. 15, 161-171 (1962)

Titlyanov, E. A., P. V. Kolmakov, B. D. Lee and I. Horv~th: Functional states of the photosynthetic apparatus of the marine green alga Ulva fenestrata during the day. Acta Bot. Acad. Sci. Hungaricae 24, 167-177 (1978)

Witztum, A., H. B. Posner and R. A. Gower: Phototactic chloro- plast displacement in the photosynthetic mutant Lernna paucicogtata Strain 1073. Ann. Bot. 44, 1-4 (1979)

Zurzycki, J.: Chloroplasts arrangement as a factor in photo- synthesis. Acta Soc. Bot. Pol. 24, 27-63 (1955)

Zurzycki, J.: The mechanism of the movements of plastids, ln: W. Ruhland (Ed.) Handbuch der Pfianzenphysiologie 17/2, pp 940-978, Berlin, GSttingen, Heidelberg: Springer 1962

Zurzyeki, J.: Properties and localization of the photoreceptor active in displacements of chloroplasts in Funaria hygro- metrica. II. Studies with polarized light. Acta Soc. Bot. Pol. 36, 143-152 (1967)

Zurzyeki, J.: Experimental modification of the reaction pattern of Lemna leaf cells to polarized light. Protoplasma 68, 193- 207 (1969)

Zurzycki, J.: Adjustment processes of the photosynthetic apparatus to light conditions, their mechanism and biological significance. Pol. ecol. Stud. 1, 41-49 (1975)

Date of final manuscript acceptance: January 30, 1981. Communicated by O. Kinne, Hamburg