Influence of UV radiation on the photosynthesis of arctic macroalgae in the field

Journal of Photochemistry and Photobiology B: Biology 38 ( 1997) 4W7

Influence of UV radiation on the photosynthesis of Arctic macroalgae in the field ’

Dieter Hanelt a**, Christian Wiencke ‘, Wilhelm Nultsch b a A&red Wegener Institute for Polar and Marine Research, D-27515 Bremerhaven, Germany

b Biologische Anstalt Hclgoland, Notkestr. 31. D-22067 Hamburg, Germany

Received 1 March 1996; accepted 21 June 1996

Abstract

The photoinhibition in brown and red macroalgae from Spitsbergen (79”N, 12”E) was investigated to study the effects of UV under balanced UV/photosynthetically active radiation (PAR) conditions. Algae were collected from different depths and exposed to natural solar radiation. Various parts of the UV radiation spectrum were successively cut off by filters absorbing wavelengths of less than 295 nm, less than 320 nm and less than 400 nm. The samples were covered with these filters and exposed to daylight 10 cm below the water surface in outdoor tanks near the shore supplied with running seawater. PAR and UV radiation were continuously measured during the experiments. The degree of photoinhibition was observed during the course of the day by measuring the in vivo fluorescence of photosystem 11 (FJF,,,) .

In addition, the transmittance of the water body of the Kongsfjord (Spitsbergen, Norway) related to the UV and PAR wavelength ranges was determined. Even on a sunny day in August, only relatively low fuence rates of UVA (approximately 13 W me2), UVB (approximately 0.14 W mm2) and PAR (approximately 1100 pmol rns2 s- ‘) were measured in the air at noon due to the low position of the sun at this high latitude. The UV transmittance of the water body in the fjord was also low. As a result, UV stress occurred only in seaweeds growing in the intertidal zone or in shallow water. The photoinhibition of photosynthesis was mainly induced by white light in shallow water. The inhibitory effects of UV radiation caused a delay in the recovery processes in the afternoon and evening, rather than an inhibitory effect on photosynthesis in the morning. Fucus distichus, growing in the upper intertidal zone, was most insensitive to UV radiation. Algae from the sublittoral zone had problems coping with the natural UV radiation in shallow water, whereas those from the intertidal zone were acclimatized to the unfavourable UV/PAR conditions. By cutting off sequentially the shorter wavelengths of the UV range, the investigated brown algae showed no significantly different effects. In contrast, the red alga Palmaria paintutu showed a clear response to the different UV ranges, i.e. the UVB wavelength range was very effective in causing photoinhibition. In addition, the recovery phase was delayed in spite of the low fluence rates impinging on the alga during the course of the day. 8 1997 Elsevier Science S.A. All rights reserved.

Keywords: Algal zonation; Fluorescence; Macroalgae; Photoinhibition; Photosynthesis; Solar radiation; UV radiation

1. Introduction

Sessile plants living in the intertidal zone have to cope with extreme changes in the incident solar radiation and variable weather conditions. Thus, in algae uncovered during low tide or floating near the water surface, strong photoinhibition is observed [ l-4 1. During rising tide, the increased absorption and scattering of light by the rising water column counteract the increasing fluence iates of daylight, so that the fluence rate under the water may even decrease, e.g. a water column of 1 m or more is sufficient to protect algae from the high

* Corresponding author. ’ Dedicated to Prof. Dr. Pill Soon Song on the occasion of his 60th

birthday.

101 l-1344/97/$17.00 8 1997 Elsevier Science S.A. All rights reserved PIISlOl l-1344(96)07415-5

fluence rates at midday [ 31. In contrast, the intertidal zone is a potentially vulnerable location for incurringphotoinhibition or damage by photosynthetically active radiation (PAR) or W radiation. Mature kelps can cope with a high fluence of solar radiation, but the growth and survival of the early spo- rophytic stages are strongly photoinhibited by PAR [S] or even damaged by UV radiation [ 61. However, a water column above the algal bed can protect these organisms from harmful W radiation both by a decrease in the fkuence rate as well as by spectral changes, especially if the water is turbid. Polne and Gibor [ 71 suggested that intertidal algae may pos- sess photoadaptive mechanisms to minimize damage by solar UV. They found that plants living in the subtidal zone are much more sensitive to UV radiation than specimens from the intertidal zone. Although UVB quanta (280-320 nm) are mure damaging than WA quanta ( 320400 nm), the greater

D. Hunelt et ul. / Jourttul of Pltotochernistry und Photobiology B: Biology 38 (1997) 40-47 41

fluxes of WA in the ocean cause stronger UV inhibition in phytoplankton [ 8 ] .

The effects of UV radiation on plants and especially on photosynthesis are manifold; a summary has been given by Bornman and Teramura [ 91 and Holm-Hansen et al. [ lo]. It is obvious that photosystem II (PS II) is strongly affected, so that the effects induced by UV can be easily observed in field experiments by changes in the variable fluorescence of PS II. Recently, Larkum and Wood [ 111 have shown that the O2 production and variable fluorescence of seaweeds decrease due to UVB radiation. However, the photodamage induced by UV radiation is often incorrectly described as photoinhibition [ lo]. According to new definitions, photoinhibition is a protective mechanism, which causes an active downregulation of photosynthesis, rather than passively induced damage [ 121. Measurements of the kinetics of recovery can reveal whether UV exposure causes a fast reversible downregulation of photosynthetic activity similar to PAR.

In winter 1994-1995, measurements of the stratospheric ozone layer above the Arctic in the European SESAME cam- paign (Second European Stratospheric Arctic and Midlati- dude Experiment) showed a clear depletion of 20%-300/c of the concentration compared with that observed in 1988 [ 131. The resulting increase in UVB radiation may aggravate the light stress of photosynthesis [9]. Therefore the sensitivity of photosynthesis of several macroalgae collected at different depths in the Kongsfjord of Spitsbergen and exposed to different spectral ranges of natural solar UV radiation was observed in simulated field experiments under balanced UVI PAR ratios. It is shown that UV radiation delays the recovery process from photoinhibition, which is mainly induced by PAR.

2. Materials and methods

The photoinhibition of photosynthesis in marine macroalgae was investigated in the Kongsfjord (79’N, 12”E; Ny Alesund, Spitsbergen, Norway) in August and September 1995. Algae were collected by hand in the intertidal zone or from a boat by a specially designed sampling device [ 141 from different water depths in the fjord. Underwater PAR was measured using a LI-COR 47runderwater sensor (LI 192 SB, LI-COR, Lincoln, USA) connected to a datalogger (LI- COR, LI- 1000). Underwater UV radiation was measured with a portable bandpass radiometer ( RM-2 1, Griibel, Karls- ruhe, Germany) equipped with broadband 27rUVA and UVB underwater sensors. WB radiation in air was measured using a special 32 channzl quanta counting radiometer installed on the roof of the NDSC building (Koldewey Station, Alfred Wegener Institute). The instrument was developed at the Alfred Wegener Institute for measuring continuously with high accuracy the UVB fluence rate to observe possible increases in UV radiation caused by stratospheric ozone depletion.

Whole thalli of FUCUS distichus L. and Palmaria palmta ( L. 10. KLJN’lZE and pieces (diameter, 10 cm) cut from the middle part of the large blades from L.umiruwia sacc/u.n-ina (L-1 LAMOUR., L. digitata (HUDS.) LAMOUR. and Maria esculema (L.) GREV. were exposed to natural sunlight. The thalli were kept in boxes uncovered or covered with different cut-off filters (WG 295, WG 305, WG 320, GG 400; Schott, Mainz, Germany) to study the effects of full solar radiation or solar radiation depleted of UV of different wavelengths. The boxes containing the algae were immersed in large seawater pools 10 cm below the water surface. A continuous exchange of seawater, pumped from the deep water of the Kongsfjord into the pools, ensured a nearly constant water temperature and salinity during the experiments and prevented a depletion of nutrients. W radiation from the sun was continuously determined underwater using an RM-2 1 sensor and PAR in air was evaluated with a LICOR LI- 190-SB 27r sensor.

Algae were kept overnight and, in some cases, for several days in the seawater pools in the different light fields. During the course of the next day, samples were cut from the blades. In vivo chlorophyll fluorescence was measured with a portable pulse-amplitude modulation fluorometer (PAM 2000, Walz, Effeltrich, Germany) connected to a portable computer (Poqet PC, Santa Clara, USA). This is an improved system based on the principle devised by Schreiber et al. [ 151. As a measure of the photoinhibition, the ratio of variable to maximal fluorescence F,/F,,, of the dark-adapted plant was used [ 161. F, = F,,, - P;;,, where F,, is the initial fluorescence, i.e. when all the reaction centres of PS II are active or “open”, and F, is the maximal fluorescence, i.e. when all the PS II centres are “closed”. Earlier experiments have shown [ 1,3,4,17,18] that the results of fluorescence measurements are consistent with the photosynthetic efficiency determined by oxygen measurements. Small pieces cut from the blades (diameter, 9 mm) were fastened to the fibreoptics and incu- bated in a home-built seawater cuvette cooled by a surround- ing water jacket. A temperature of about 0 OC was adjusted by a connected cryostat. After application of a 5 s far-red pulse (approximately 30 pm01 m - ’ s - i, 735 nm) , used to oxidize the electron transport chain, the red alga P. palmata was left in the dark. After 5 min, a short pulse of red actinic light (5 s, 8 pmol m-* s-‘, 655 an,! was given to ensure a stabilized fluorescence emission during the following F,,, measurement. In red algae, this pulse excites, in particular, photosystem I and the onset of F, dechne during a saturation pulse is delayed. Subsequently, a second 5 s far-red pulse was given to oxidize fully the electron transport chain. Then FO was measured with a pulsed red measuring light (approximately 0.3 pm01 m-* s- ‘, 650 nm) and F,.,, was determined with a 400 ms completely saturating white light pulse (approximately 9200 ymol m - ’ s - ’ ) . This sequence was repeated three times with an intermediate dark period of 5 min to control possible changes in the fluorescence parameter by incomplete recovery of the fluorescence quenching parameters (e.g. energy quenching qn or quenching by state tran-

42 D. Hanelt et ul. /Journal of Photochenristry and Photobiology B: Biology 38 (I 997) 447

sitions qT). The brown algae were measured using the same protocol, but without a preceding red pulse and with a longer saturating white light pulse of 600 ms to determine F,,,. In contrast with red algae, the actinic red pulse induces in brown algae photochemical or energy quenching (qp, qE) by additional excitation of PS II. Moreover, the application of a red pulse is not necessary because brown algae do not show such a fast F,,, decline during the saturation pulse as observed in red algae or cyastibs:teria (see also Ref. [ 191) .

For the detenklrnation of the photosynthetic efficiency of the control, the mean of four FJF,,, values from four different non-photoinhibited individuals was calculated. For non-photoinhibited brown algae, an F,/F,,, ratio of about 0.75 was determined and for P. pulma~u a ratio of about 0.57. The mean of the respective FJF, values was normalized to 100% photosynthetic efficiency and all the following values were calculated as a percentage of the control. Each thallus piece was measured three times as mentioned above and the stan- dard deviation was generally less than 1%.

3. Results

Due to the high latitude (79”N), the position of the sun ac noon is low, and even on a sunny day in August only low fluence rates of UVA (approximately 13 W m - *) , UVB (approximately 0.14 W m - *) and PAR ( approximately 1100 pm01 me2 s-l, about 220 W m-*) were measured in air. The transparency of the water body changes with the weather conditions and with the input of turbid meltwater from gla- ciers close to the bay. As an example, the results of underwater light measurements at 13:00 on a normal bright calm day are shown in Figs. 1 and 2. The transmittance of the water body close to Ny Alesund is not very high as is typical for coastal waters. However, even fluence rates lower than 5 pm01 me2 s-l were sufficient for the growth of L. saccharina, collected at a depth of 20 m. The maximum fluence rate of PAR above the water surface was about 800 pmol mm2 s-‘,ofWAabout9Wm”*andofWB60mWm-*.WB radiation decreased strongly with increasing water depth, and at a depth of0.5 m the fluence rate was at the detection limit

1

Depth Cm) fig- 1. Light transmittance and photosynthetically active radiation (PAR) bound at different water depths in the Kongstjord on 2.9% at 13:oo.

i i Depth (ml

Fig. 2. Fluence rates of UVA and UVB measured at different depths on 2.9.95 with a portable bandpass radiometer ( RM-2 1) . The UV transmittance declines sharply with increasing depth of the coastal water type.

0 300 305 310 315 320

Wavelength (mn) Fig. 3. Solar radiation in the UVB range and fluence rates of wavelengths passing the different cut-off filters used to cover the algae. Fluence rates were measured at 15:45 (2.9.95) on the roof of a building with a special UVB monitoring spectroradiometer.

of the measuring instrument. At 1 m depth, the UVA level was only about 22% of the level measured at the surface. Thus the water is relatively non-transparent to UV radiation and algae growing in the sublittoral zone are usually not severely stressed by UV. Therefore the influence of UV radiation impinging on algae exposed close to the water surface was investigated in the following simulated field experiments.

The transmittance of the cut-off filters was determined by covering the light entrance of the spectroradiometer with the filters. Fig. 3 shows that the fluence rate of solar UVB was already low at 1545 due to the low position of the sun. The transmittance of the WG 295 filter in the longer UVB wavelength range was already less than 100%. WG 320 cut off nearly all UVB and GG 400 most of the WA. The transmittance of the WG 295 and WG 320 filters in the PAR range was about 96% and of the GG 400 filter about 93%. Thus the fluence rate of PAR was diminished only slightly by scattering and absorption.

The daily course of the photosynthetic efficiency at a water depth of 10 cm was measured in L. saccharina collected from a depth of 6 m. The photon fluence rate on the measuring day

OJ.

Tie of day

I ?? . . - , . , 9 11 13 15 17 19

Time of day

Fig. 4. DaiIy course of daylight (24.8.95 ) measured in the PAR, UVA and UVR ranges. PAR was measured above the water surface and UVA and UVB at a water depth of IO cm near the samples. The fluence rates of PAR and UV were measured every second; PAR was averaged for time intervals of 5 min and UV For intervals of 30 min. At 15:OO. the seawater pools were shaded by a building. Note the different units of UVA and UVR.

is shown in Fig. 4. Heavy clouds lowered the radiation many times during the course of the day. From about 1500, the seawater pools containing the algae were shaded. The relatively high irradiation from 9:00 to 14:OO caused a strong decrease in the photosynthetic ~f~ciency measured by the fluorescence parameter F,,/F, (Fig. 5 ) . Concomitant with the decreasing fluence rates, the recovery of photosynthesis commenced at 13:30. Photosynthesis did not fully recover until IWO (see also Table 1) . The course of the photosynthetic efficiency is clearly opposite to the fluence rate of daylight measured during the day (Fig. 4). During the following 18 days, the algae were kept in specific light fields and on 10.9.95 the photosynthetic efficiency was measured again. On that day, the photosynthetic efficiency was about 90% at 9:00 and decreased at noon by about the same amount as observed on 24.8.95 (Fig. 5, right). In particular, accli- ~atization or photodamage of the thalli due to the higher irradiation at 10 cm compared with the 6 m collecting depth was not observed. A comparison of the algae irradiated by natural solar radiation and those covered by different cut-off filters showed that the various WC filters did not cause clear differences in reaction (Figs. 5 and 6). However, if the UV radiation was cut off completely, the decrease in the photosynthetic efficiency was less pronounced and recovery in the afternoon was much higher than in natural solar radiation.

The decrease in the photosynthetic efficiency in response to an increase in excessive solar radiation is shown in Fig. 6, with L. saccharina collected from a water depth of 1 m. The low efficiencies of the algae exposed under WG 295 and WG

8 10 12 14 16 18 Time of day

Fig. 5. Photosynthetic efficiency of Lmninaria saccharina measured during the course of the day (24.8.95). The photosynthetic efficiencies of the non- photoinhibited controls, collected the day before at a depth of 6 m. were measured by the fluorescence ratio F,/F, and st~d~dized to 100%. The full fitted line indicates the reaction caused by unfiltered solar radiation and the broken line indicates the reaction caused by radiation depleted of UV due to a GG 400 filter. After an acclimatization period of 18 days, tlx photosynthetic efficiency was measured again; the values are shown after the interruption of the abscissa.

320 filters at 11:30 and 13:00 were not caused by the specific wavelengths, but were due to the tempor~y high fktence rates of PAR. This shows the clear time relation between the low efficiency values and PAR peaks, whereas the fluence of UV radiation increased only slightly. After 30 min, the efficiency increased again because passing clouds led to a decrease in i~adiation. The v~~ab~lity of the fluorescence data was often caused by these fluctuating light conditions and not by indi- vidual reactions of the algae. UV radiation caused a delay in recovery. Without UV, fast recovery was observed, and in the light field depleted of UVB only (WG 320) the results indicated that the recovery was faster than in unfiltered solar radiation. A comparison between L. saccharina thalli collected from 1 and 20 m showed that the algae from deep water were more sensitive to radiation than those from shallow water (Table 1) . Although these investigations were made on different days, the algae were exposed to similar fluences. The algae from 20 m were much more inhibited and recovered at l&00 to a signi~~antly smaller extent than the specimens from shallow water.

The weather conditions on 1.9.95 were fine and high fluence rates were measured (Fig. 7). At about 13:45 the tanks were shaded and the fluence rates decreased rapidly. L. digitata collected from shallow water showed a strong decrease in photosynthetic efficiency in the morning (Fig. 8). In the shade, photosynthesis recovered, but without W radiation the recovery was much faster. Again, most of the photoinhibition of photosynthesis was induced by PAR and not by W radiation, The photosynthesis ofI,. ~~g~~~~u from deeper water was more inhibited and the recovery was less than in algae from shallow water (Table 1). Although the fluence was higher on 19.8.95, the level of recovery at 18:OO without W radiation was similar in specimens from both depths. Now- ever, in unaltered solar radiation, the recovery of the algae

44 D. Hanelt et al. /Journal (f Photochemistry and Photobiology B: Biology 38 (I 997) 40-47

Table I -ten describing the light environment and the reaclion of the algae in the experiments. Light conditions are described by the maximum fluence rates during the coutse of the day. Exposures to PAR, UVA and UVB are calculated for the time interval lO:OO-18:OO. Photoinhibition of the algae is described by the averaged minimum photosynthetic efficiency during the course of the day and the recovered efficiency at 18:OO in unfiltered solar radiation or solar radiation depleted of UV (GG 400)

Species Collected at Date of Water Maximum Fluence (time period 1 O:OO- Minimum Photosynthetic depth (m) of measurement temperature irradiation PAR 18:OO) photosynthetic efficiency at l&O0 sublittoral zone (“0 (pmolm-“s-l) efficiency (%) (%)

UVA UVB PAR Unfiltered GG 400 (kJ m-“) (J m-“) (mol m-‘)

Alaria esculenta 5 27.8.95 4.6 827 203.3 505.7 10.3 16 16 34 Fucus distichus Upper eulittoral 20.8.95 5.0 793 134.5 849.9 15.3 26 76 101

1 3.9.95 5.0 529 120.2 297.7 7.9 27 88 100 Laminaria digitata Upper sublittoral 1.9.95 4.0 669 138.3 413.5 9.7 22 71 86

5-6 19.8.95 6.0 824 141.3 792.6 15.3 17 58 92 taminaria saccharina 1 5.9.95 4.0 464 97.6 351.4 4.3 65 86 99

6 24.8.95 4.6 721 143.0 514.3 8.0 35 60 87 20 30.8.95 4.1 238 88.3 267.8 4.6 24 25 67

Palmaria palmata 1 9.9.95 3.9 193 50.8 - 4.1 52 65 103 3 8.9.95 3.9 548 117.9 395.7 6.8 10 14 81

Time of day

Fig, 6. As shown in Fig. 5, the photosynthetic efficiency of Laminaria sw- charina collected at I m depth. The thalli were exposed to solar radiation on 5.9.95 and were measured again next morning. In addition, the fluence rate of PAR is shown. The right ordinate is drawn inversely to show the relationship between the low fluorescence data and the high irradiation values of PAR.

collected from the deeper zone was clearly less, indicating a higher sensitivity to UV radiation.

Mucus distichus grows only in the intertidal and upper sublittoral zones of the Kongsfjord. The irradiation experiment was performed on a sunny day which caused a strong decrease in the photosynthetic efficiency during the morning (Fig. 9). From about 13:00, the tanks were shaded, resulting in the recovery of photosynthesis. The difference in recovery between filtered and unfiltered solar radiation was only small. On a day with an even higher fluencc rate (Table 1 ), the difference between filtered and unfiltered solar radiation was higher; however, compared with the results for other species collected from the upper littoral zone, the photosynthesis of Fucus distichus was rather insensitive to UV radiation.

Aluriu esculenta grows on an exposed site of the Kongsfjord and was collected from a depth of 5 m. Pieces of the thinner distal parts of the blades were used for the exper- imen-’ . The alga was very sensitive to strong light and pho-

800

0 9 11 13 15 17 19

Time of day

9 11 13 15 17 19 Time of day

Fig. 7. As shown in Fig. 4 for 1.9.95. At about 13:45, the seawater pools were shaded temporarily and after 14:30 continuously by a building.

tosynthesis recovered very slowly even in thalli protected from UV radiation (Table 1) . In the morning of the following day, the photosynthetic efficiency had recovered to no more than 80% of the control. The high sensitivity of the alga was not only caused by the higher irradiation, but was a genera1 effect related to the change in environment and was also observed in the large culture tanks indoors.

The thalli of the red alga Palmaria pulmatu, collected from a depth of 1 m, indicated by their green colour an acclimatization to high fluence rates. At a depth of 3 m the thalli were red, and thus the content of phycobiliproteins in relation to chlorophyll u was higher, i.e. it can be assumed that the antenna complex of PS II was larger. When the experiments

D. Hunelt et ul. /Juurrral of Plwtochemistry and Plwtobiolugy B: Biology 38 (I 997) 40-47 45

Tiie of day

Fig. 8. As shown in Fig. 5 for Luminariu digitutu ( 1.9.95 1, collected from the upper sublittoral zone. Photosynthesis was measured again the next morning.

1 Fucus diaid~uc 3.9.92

9 11 13 15 17 Time of day

Fig. 9. As shown in Fig. 5 for Mucus distichs ( 3.9.95 ), collected from I m depth. At about 13:00, the algae were shaded by a building and recovery commenced.

120

1 jb&w& prlmur 9.9.199s

Time of day

Fig. 10. Photosynthetic efficiency of the red alga Palmaria palmatu during the course of the day (9.9.95). It was a cloudy day and the fluence rate decreased continuously after 14: 10. The lines indicate the different reactions caused by the different spectral light fields. Next morning, the photosynthesis was measured again.

were performed, the photon flldence rate was relatively low (Table 1). In contrast with the results obtained with brown algae, Palmariapalmata showed a reaction which was clearly dependent on the different UV radiation fields (Fig. 18). By cutting off successively more of the shorter wavelengths, the degree of photoinhibition decreased and recovery commenced earlier during the course of the day. Next morning,

photosynthesis had only recovered to 85% in algae which

were not protected from UVB radiation. In relation to the fluence to which the algae had been exposed, UVB clearly showed a much stronger inhibitory effect than WA or PAR.

With the exception of Alaria esculenta, the photosynthesis of all the algae had fully recovered the next morning when

the thalli were protected from UV radiation. Mowever, with additional UV radiation, the photosynthesis of the algae from

the upper zone recovered very well from photoinhibition. Only L. saccharina from a depth of 20 m clearly showed severe photodamage when not protected from WA and UVB. The recovery was slight (40% efficiency), but better if the thalli were protected only from UVB (58%) r

4. Discussion

Apart from phytoplankton, macrophytes play an important role in the primary production of coastal waters, serving as food for herbivores and detritivores [20] and as shelter for juvenile animals. They may be even more vulnerable than higher plants [ lo], as eulittoral macrophytes become exposed to full sunlight at low tide and any screening by seawater is absent at low tide [ 31. Macrophytes are more affected by W radiation in clear waters than in turbid waters since the penetration of UV is higher. This may have dele- terious effects, especially in polar species, where seasonal growth activity coincides with high water transparencies and higher UV radiation underwater in spring [ lo,21 1. The knowledge of how UV influences the uptake of nutrients by macrophytes is very small. Diihler et al. [ 221 recently showed an inhibition of ammonia uptake by WB in all tested seaweeds, whereas inhibition by UVA was species dependent. The abiotic key factors clearly affect intraspecific competi- tion and eventually the community structure of the macro- phytic vegetation [ 231.

Herrmann et al. [ 241 investigated the effect of filtered and unfiltered solar radiation on the photosynthesis of Ulua lue- tevirens using the fluorescence method. Solar radiation seemed to have a smaller inhibitory effect on photosynthesis if W was filtered out; however, recovery observations were not performed. Thus it was not determined whether the photosynthetic efficiency decreased due to a regulatory process or due solely to photodamage. In contrast, our studies clearly show that, in intertidal algae, a delay in the regulatory process is involved and the effects are differentiated between the WA and WI3 wavelength ranges. However, fluorescence values may be misinterpreted, since differences have been found between photosynthetic oxygen production [251 or carbon fixation [ 261 and fluorescence parameters. The flue- rescence ratio F,/F, is not well suited for the observation of changes in the photosynthetic capacity as determined by oxY- gen measurements, i.e. changes in the saturation level of fluence rate-response curves are not well correlated with changes in the variable fluorescence [ 25,317 1. However, the photosynthetic efficiency (i.e. non-saturated photosynfietic

46 D. Hanelt et al. /Journal of Photochemistry and Photobiology B: Biology 38 (1997) 40-47

rate) is strongly correlated with &IF,,,, and therefore flue- rescence measurements are a powerful tool for the investi- gation of the light stress of the energy converting photosynthetic apparatus as performed in our studies.

The transmittance measurements performed in the summer in the KongsQord showed that light stress induced by W radiation was a problem for algae growing in the intertidal and upper subtidal zones. It was clearly shown that photoinhibition was mainly induced by white light, and that UV

tion caused a delay in the recovery process in the afternoon and evening, but did not strongly affect the inhibitory process of the morning at least in the brown algae studied. Thus the repair cycle of photosystem II may be affected. A sensitivity to W was observed in all the investigated species fvrn~t sttoqly !r? species from the sublittoral zone), but only to a very small extent in Fucus distichus growing in the upper intertidal zone. This indicates that algae from deep water have problems coping with the natural W radiation, whereasspec- imens from the intertidal zone are acclimatized to the unfavourable W/PAR conditions. Unexpectedly, only the red alga Pulmariupalmatu showed acleardifferentiatedresponse to the various W ranges. The low fluence rate of UVB induced a strong inhibitory effect, stronger than WA or PAR especially when related to the fluence. Moreover, the low fluence rates of the shortest wavelengths, which could not pass the WG 295 filter, induced a relatively strong effect. This is demonstrated by a comparison of the effect caused by natural solar radiation with the response caused by radiation transmitted through the WG 295 filter. The reflectance or scattering on the filter surface could not induce such a high inhibitory effect. Temperature effects below the glass filters were experimentally excluded.

In recent times, it has been recognized that photoinhibition is a protective process of photosynthesis, which can be differentiated into dynamic and chronic photoinhibition [ 121. Dynamic photoinhibition, as a photoprotective mechanism, amplifies non-photochemical energy dissipation so that excessive absorbed energy, which is not utilized in photochemistry, is converted harmlessly into thermal radiation [ 16,281. Chronic photoinhibition is related to the rate of damage of the DI protein, which exceeds its rate of repair, resulting in a breakdown (degradation) of the D, protein and a 10s~ of photosynthetic activity [ 291. Fast recovery during the afternoon is indicative of photoprotection, whereas photodamage of proteins and pigments would require several days for repair [ 171. The experiments clearly show that mod- erate U’V radiation does not induce strong photodamage, for- merly often wrongly defined as photoinhibition, With the exception of Alaria esculenta and Laminaria saccharina from deep water, the algae had fully recovered by the following morning, and thus the thalli were not photodamaged. The quantum yield of photosynthesis was again at a maximum and the low fuence rate of dawn could be used with high efficiency. However, the delay in recovery to the afternoon due to W radiation caused additional energy costs since the quantum yield would be higher at low fluence rates and,

possibly, more energy is necessary photoinhibition, i.e. the repair of centres.

to recover from chronic inactive PS II reaction

Acknowledgements

We are indebted to the Deutsche Forschungsgemeinschaft and the European Commission (Project PL950112) for financial support. Thanks are due to Thomas Hanken and Helmuth Tiig for their help and support and for the use of the W spectroradiometer. This paper is Contribution No. 1170 from the Alfred Wegener Institute for Polar and Marine Research.

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Influence of UV radiation on the photosynthesis of arctic macroalgae in the field

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