K. Bischof Æ D. Hanelt Æ J. Aguilera Æ U. Karsten

B. Vogele Æ T. Sawall Æ C. Wiencke

Seasonal variation in ecophysiological patterns in macroalgaefrom an Arctic fjord. I. Sensitivity of photosynthesisto ultraviolet radiation

Received: 17 August 2001 /Accepted: 7 January 2002 / Published online: 29 March 2002� Springer-Verlag 2002

Abstract Marine macroalgae inhabiting Arctic coastalecosystems are exposed to pronounced seasonal varia-tions in the radiation regime, including harmful UVBradiation. This study presents the first data on theseasonal changes in the sensitivity of macroalgal photo-synthesis towards UV exposure by comparing under-ice,clear-water and turbid-water conditions characteristic forlate winter, spring and summer. Various brown (Lami-naria saccharina, L. digitata, L. solidungula, Saccorhizadermatodea, Desmarestia aculeata), red (Palmaria pal-mata, Devaleraea ramentacea) and one green macroalgalspecies (Monostroma aff. arcticum) were collected atthe same water depth throughout the seasons in theKongsfjord (Spitsbergen, Svalbard, Norway). Maximumquantum yield (Fv/Fm) and maximum photosyntheticelectron transport rates (ETRmax) were determinedimmediately after collection, after 2 h exposure to artifi-cial UV radiation and after 18 h recovery in dim whitelight. Photosynthesis of the studied species showeddifferent responses dependingon their morpho-functional

and physiological characteristics, their life strategies,phenology and depth distribution. Within the genusLaminaria, maximum quantum yield of adult specimensof the deep-water speciesL. solidungulawas most stronglyUV sensitive. Adult L. saccharina exhibited a lower UVsensitivity than a 6-month-old specimen. Inhibition ofphotosynthesis after UV exposure remained at thesame level throughout the study period, both in adultL. saccharina and S. dermatodea. However, adult speci-mens of L. saccharina collected in May showed partialrecovery only, whereas photosynthesis of specimens fromboth species collected later recovered fully. D. aculeataexhibited a remarkable decrease of UV sensitivity duringthe study period. Photosynthesis of specimens collectedunder the ice was strongly inhibited by UV, but the degreeof inhibition decreased during spring and summer.Concomitantly ETRmax values were low after UV expo-sure in specimens collected in June, but increased later inthe season. P. palmata exhibited a relatively flexibleresponse. Photosynthesis in specimens collected under theice in June or in turbid water in July/August was relativelystrongly inhibited; specimens collected during sunnyperiods and in clear water in spring showed a much lowerdegree of photoinhibition after UV exposure. Theseasonal pattern of low/high ETRmax values in spring/summer is probably a characteristic of the life strategy ofthis species. TheUVsensitivity ofD. ramentacea exhibiteda similar seasonal pattern. In M. aff. arcticum, UV sensi-tivity increased and ETRmax values decreased during thestudy period, reflecting the life strategy of this annual latewinter/spring species. The physiological basis for theseasonal changes in UV sensitivity of photosynthesis ispresented in a companion paper (this issue).

Introduction

Polar regions are characterised by strong seasonal vari-ations in environmental conditions. During periods ofice cover, little or no light reaches benthic communities

Marine Biology (2002) 140: 1097–1106DOI 10.1007/s00227-002-0795-8

Communicated by O. Kinne, Oldenburg/Luhe

K. Bischof Æ T. Sawall Æ C. Wiencke (&)Alfred Wegener Institute for Polar and Marine Research,Am Handelshafen 12, 27570 Bremerhaven, Germany

E-mail: cwiencke@awi-bremerhaven.deFax: +49-471-48311425

D. HaneltFoundation Alfred Wegener Institute,Biologische Anstalt Helgoland, Kurpromenade,27483 Helgoland, Germany

J. AguileraUniversidad de Malaga, Facultad de Ciencias,Departamento de Ecologıa,Campus de Teatinos s/n, 29071 Malaga, Spain

U. KarstenUniversity of Rostock, Institute of Aquatic Ecology,Freiligrathstrasse 7/8, 18051 Rostock, Germany

B. VogeleAkvaplan-Niva AS,Polar Environmental Centre, 9296 Tromsø, Norway

(Gerland et al. 1999; Hanelt et al. 2001). At our studysite, the Kongsfjord (Spitsbergen, Svalbard, Norway),sea ice regularly breaks up between April and early June,often within a few days (Mehlum 1991; Gerland et al.1999). Consequently, there is a rapid increase in under-water irradiance, especially due to the high watertransparency at that time (Hanelt et al. 2001). In 1998,the fjord was covered by ice until the end of June(Bischof et al. 1999). After the break-up of sea ice, thewater body was characterised as a Jerlov coastal watertype I, and UVB radiation penetrated down toapproximately 10 m depth (Aguilera et al. 1999a; Haneltet al. 2001). The benthic communities, which had toprevail in darkness throughout the winter period, weresuddenly exposed to high photosynthetically active ra-diation (PAR) as well as to high UV radiation. However,the period of high underwater irradiance, in general, isrelatively short, due to the input of turbid meltwatercausing a high influx of sediments into the water, and, inturn, a marked decline in water transparency (Haneltet al. 2001; Svendsen et al., unpublished data).

Benthic marine macroalgae are an important groupof marine organisms, which are exposed to the drasticchanges in radiation climate along the shores of theKongsfjord (Hop et al., unpublished data). Earlierstudies have shown that the ability to resist high radia-tion stress may be one of the factors controlling verticalmacroalgal zonation patterns (Hanelt 1992, 1998;Maegawa et al. 1993; Bischof et al. 1998a). Numerousstudies have revealed the multitude of direct and indirecteffects UVB exerts on marine algae, including moleculartargets such as nucleic acids and proteins, resulting inimpairment of photosynthesis and growth (e.g. Wood1987; Karentz et al. 1991; Larkum and Wood 1993;Buma et al. 1995; Clendennen et al. 1996; Aguilera et al.1999a,b; Bischof et al. 2000; for review see Franklin andForster 1997; Hader and Figueroa 1997).

However, polar macroalgae also exhibit a high po-tential to acclimate to the relatively rapid changes inirradiance as well as spectral composition (Henley andDunton 1995; Hoyer et al. 2001; Karsten et al. 2001;Luder et al. 2001; van de Poll et al. 2001). Bischof et al.(1999) have shown the rapid acclimation of maximumquantum yield of photosynthesis in the brown algaAlaria esculenta to moderate artificial UV exposure.Seasonal changes in solar and underwater light condi-tions control growth rates of the macroalgae inhabitingthe fjord (Aguilera et al. 1999a). Transplantationexperiments on algae from deep to shallow waters and insitu experiments showed a positive correlation of growthrate and variations in natural solar radiation during thesummer, with a significant inhibitory effect of both UVAand UVB on growth of species from deeper waters. Theability to acclimate and adjust photosynthesis andgrowth to rapid changes in light climate is thereforeregarded as one prerequisite for macroalgal life underthe strong seasonal changes in the Arctic.

This study presents the first data on the photosyn-thetic response of marine macroalgae from the field to

UV exposure during late winter, spring and summer,both under ice cover and after the sea-ice break-up. Theresults presented are subdivided into two companionpapers within this issue. The first part focuses on theseasonal changes in UV tolerance of photosynthesis indifferent species of macroalgae from the Kongsfjord,with respect to changing radiation and ice conditions,and changing water transmittance resulting from turbidfreshwater runoff during the summer season. The secondpart provides data on the physiological basis of theacclimation processes, as triggered by the changes ofabiotic factors in the field including changing irradiance,as well as nutrient availability (Aguilera et al. 2002).

Materials and methods

Algal material and study site

Specimens of eight different macroalgal species (Table 1) werecollected from the sublittoral zone of the study sites located in theKongsfjord (Ny-Alesund, Spitsbergen, Norway, 78�55.5¢N;11�56.0¢E; Fig. 1) during the spring/summer season 1998 (see Fig. 2for dates of sampling). Algal samples were collected by SCUBAdiving and put in black bags to avoid exposure to high irradianceduring transportation. After collection, samples for photosyntheticperformance experiments were maintained in the laboratory underdim light conditions and in running seawater pumped directly fromthe fjord.

Abiotic parameters

UVB radiation in the atmosphere was continuously measured by a32-channel spectroradiometer installed on top of the NDSC(Network for Detection of Stratospheric Changes) building in NyAlesund. Recorded irradiances were integrated over the wave-length range (290–320 nm), and the daily fluence was calculated(see Groß et al. 2001 for details). Continuous measurements ofglobal radiation using a CM 11 pyranometer (Kipp and Zonen,Delft, The Netherlands) were performed approximately 15 mabove sea level at the Ny Alesund station of the Baseline SurfaceRadiation Network (BSRN). These data were used to calculatedaily averages of PAR as described by Hanelt et al. (2001).Underwater radiation conditions at 1 and 5 m water depth weredetermined using the surface irradiance data and the respectivevertical attenuation coefficients (Kd) previously published byHanelt et al. (2001).

Photosynthetic performance

In vivo chlorophyll fluorescence was measured using a portablepulse amplitude modulated fluorometer (PAM 2000, Walz, Effel-trich, Germany). The maximum quantum yield (Fv/Fm) of photo-chemistry was determined in samples of five individuals, placed in acooled seawater cuvette during the measurement. Determination ofFv/Fm in the different macroalgal species was conducted asdescribed by Hanelt (1998). Additionally, photosynthesis versusirradiance curves (P/I-curves) were monitored by means of thePAM 2000 according to Bischof et al. (2000), to calculate maxi-mum photosynthetic electron transport rates (ETRmax). Respectiverelative electron transport rates were determined by multiplying theeffective quantum yield DF/Fm¢ (Genty et al. 1989) with therespective actinic photon fluence rate emitted by the fluorometer(Schreiber et al. 1994).

Seasonal changes in UV sensitivity of photosynthetic parame-ters were tested by exposing field samples to a 2 h artificial radia-tion treatment in the laboratory (PAR=30 lmol m–2 s–1,

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UVA=10 W m–2, UVB=1.0 W m–2), produced by two UVA-340fluorescence tubes (Q-Panel, Cleveland, USA) and one white lighttube (Osram L58/W19). The extent of UV-induced inhibition ofphotosynthesis and the subsequent capacity for recovery were re-garded as indicators of acclimation of UV. The same test systemhas been applied successfully in previous studies (Bischof et al.1998b, 1999). Fluorescence parameters (Fv/Fm, ETRmax) weredetermined before and after UV exposure and after 18 h ofrecovery under UV exclusion and dim white light (�10 lmol m–2 s–1).

Statistics

Mean values of photosynthetic parameters and standard deviationswere calculated from five independent replicates per treatment.Statistical significance of means was tested with a model 1, one-wayANOVA followed by a Fisher’s protected least significant differ-ence test (LSD; Sokal and Rohlf 1995).

Results

Seasonal variation of abiotic factors

In the course of the summer season 1998, atmosphericradiation conditions were highly variable, which is also

reflected by the scattering of daily fluence of UVB ra-diation (Fig. 2a) as well as daily averaged irradiance ofPAR (Fig. 2b). Highest values of about 53 kJ m–2 ofUVB and 163 W m–2 of averaged PAR were recorded on21 June (for a detailed overview on abiotic conditions atthe Kongsfjord see Hanelt et al. 2001).

The optical properties of the water column at Kon-gsfjord undergo marked seasonal variations (Haneltet al. 2001); consequently underwater irradiances arealso extremely variable as they depend additionally onwater turbidity. In 1998, 1 m thick sea ice and a snowlayer of about 30 cm covered the Kongsfjord until 25June. Under these conditions, surface PAR was dimin-ished down to 2.4% when passing the snow and ice layer(Fig. 2c) and UV irradiation under the ice was too lowto be detected (Hanelt et al. 2001). Consequently mac-roalgae were exposed to darkness or dim light conditionsuntil the break-up of sea ice. This rapid event in com-bination with high water transparency, which only per-sisted for about 3 weeks, until the onset of snow melting,resulted in a short, but sudden, exposure of subtidalorganisms to high solar radiation (Fig. 2c).

Table 1. Species studied, depthdistribution in the Kongsfjord,collecting depth and site

Species Depth distribution (m) Collecting depth (m) Collectingsite

Chlorophyta, UlvalesMonostroma aff.arcticum Wittrock

1–9 3–4 Nansen Bay

Phaeophyta, LaminarialesLaminaria digitata(Huds.) Lamouroux

0.5–5 3 Blomstrand

Laminaria saccharina(L.) Lamouroux

2–15 3–4 Nansen Bay

Laminaria solidungulaAgardh

8–15 8 Blomstrand

Saccorhiza dermatodea(de la Pylaie) Agardh

2–15 3–4 Nansen Bay

Phaeophyta, DesmarestialesDesmarestia aculeata(L.) Lamouroux

1–15 3–4 Nansen Bay

Rhodophyta, PalmarialesPalmaria palmata (L.)

Greville1–10 3–4 Nansen Bay

Devalearaearamentacea (L.) Guiry

0.2–8 3–4 Nansen Bay

Fig. 1. Map of Svalbard archi-pelago, indicating the collectingsites (1 Nansen Bay; 2Blomstrand Island) in theKongsfjord on Spitsbergen, thelargest island of the archipelago

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Seasonal changes of UV tolerance of photosynthesis

In young, approximately 1-year-old, thalli of Laminariadigitata, UV exposure resulted in an 81% reduction in Fv/Fm, which was only partly restored (to 66% of initialvalues) after 18 h recovery (Fig. 3). Older thalli of thesame species exhibited almost the same response as theyounger individuals. Thin, young, approximately6-month-old individuals of L. saccharina showed an 83%inhibition of Fv/Fm and hardly recovered within 18 hunder UV exclusion (up to 28% of initial values). Incontrast, older and thicker individuals of L. saccharinawere shown to be less sensitive towards the UV treatment,showing a 73% reduction in Fv/Fm, followed by a signifi-cantly (P<0.001) higher recovery to 63% of the initial Fv/Fm value. In terms of inhibition of maximum quantum

yield under UV exposure, the deep-water species L. soli-dungula was the most sensitive species, showing a 90%reduction of Fv/Fm. However, samples recovered to 80%of the initialFv/Fm value by the end of the recovery period.

No clear seasonal pattern in the sensitivity of pho-tosynthesis towards artificial UV exposure was found inL. saccharina (Fig. 4a). Throughout the study period,Fv/Fm values immediately after the end of UV exposurewere between 0.1 and 0.23, almost at the same level as inthe initial samples collected in May (Fig. 3). However, incontrast to the thalli sampled earlier, recovery from UV-induced inhibition was almost completed within 18 hunder UV exclusion in all specimens sampled later than20 May. Maximum relative photosynthetic rates(ETRmax) before UV exposure ranged between 6 and 11relative units, with exception of the values measured inplants collected in early July, during the time of highwater transparency (Fig. 2). Although ETRmax was sig-nificantly (P<0.001) higher in these specimens, they stillexhibited a strong sensitivity towards UV exposure.

In Saccorhiza dermatodea almost the same responsewas observed (Fig. 4b). Fv/Fm values after exposure werereduced to 0.08–0.19, and all samples exhibited a com-plete recovery. ETRmax values also showed a similarpattern to that found for L. saccharina, with valuesgenerally ranging from 6 to 8 relative units. Againspecimens collected in early July revealed a strongstimulation of photosynthetic electron transport, coin-ciding with a high sensitivity towards UV radiation.

In Desmarestia aculeata, UV sensitivity continuouslydecreased during the study period (Fig. 4c). Whilesamples collected and exposed to UV radiation on 13June showed a 75% reduction in Fv/Fm, the degree ofinhibition became smaller in the course of the season,

Fig. 2a–c. Atmospheric and underwater radiation, and ice condi-tions in the course of the investigated season. a Daily fluence ofatmospheric UVB (integrated over the range 290–320 nm); b dailyaveraged irradiance of PAR at ground level; c corresponding dailyaveraged irradiance of PAR at 1 m (filled squares) and 5 m (opensquares) water depth, calculated from values in b and previouslypublished Kd-values (Hanelt et al. 2001). Arrows indicate samplingdates of macroalgae and subsequent conduction of UV exposureexperiments

Fig. 3. Laminaria spp. Maximum quantum yield of photosynthesis(Fv/Fm) in three Laminaria species, as measured immediately aftercollection on 20 May 1998 (black bars), after 2 h of UV exposure(hatched bars) and after 18 h of recovery under UV exclusion(shaded bars), respectively. The young individuals of the summer-fertile L. digitata had an age of approximately 1 year, whereas theyoung specimens of the winter-fertile L. saccharina were onlyapproximately 6 months old

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showing a minimal response of 33% reduction on 22July. The sensitivity towards UV radiation in samplescollected on 13, 18 and 30 June was significantly(P<0.001) higher than in samples collected on 22 Julyand 13 August. ETRmax values and UV sensitivity werehighest in samples collected under the ice. ETRmax val-ues were lowest around sea-ice break-up, then increasedagain. UV sensitivity remained low throughout theopen-water period.

In Palmaria palmata, Fv/Fm values measured aftercollection from the field and before the start of UVexposure were in a range characteristic for red algae andonly decreased during the relatively sunny period

combined with clear water conditions in July (Fig. 5a).While mean values of Fv/Fm measured in samplescollected in the middle and end of June were at 0.47 and0.54, respectively, maximum quantum yield from sam-ples collected on 10 July was only 0.33; Fv/Fm valuesfrom samples collected later, under turbid water condi-tions, were again higher. In contrast, Fv/Fm valuesmeasured immediately after the end of the 2 h artificialUV exposure show the reverse trend. Photosynthesis wasmaximally inhibited on 17 June and 3 August (mean Fv/Fm=0.15 and 0.17, respectively), and minimally insamples collected on 30 June and 10 July. In terms ofseasonal changes in ETRmax values, P. palmata showed

Fig. 4. Laminaria saccharina(a), Saccorhiza dermatodea (b),Desmarestia aculeata (c). Sea-sonal response to UV radiationof the brown algal species. Leftpanels: maximum quantumyield of photosynthesis (Fv/Fm)as measured immediately aftercollection (black bars), after 2 hof UV exposure (hatched bars)and after 18 h of recovery un-der UV exclusion (shaded bars);right panels: the respectivemaximum photosynthetic rate(ETRmax) before (filled circles)and after (open squares) UVexposure

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a pronounced optimum in the samples collected on 10July, significantly (P<0.001) above ETRmax on theother sampling dates. The UV sensitivity was consis-tently high throughout the study period.

In Devaleraea ramentacea, the UV-induced reductionin Fv/Fm was comparatively small (Fig. 5b). Samplescollected under the ice exhibited a 50% reduction ofFv/Fm after UV exposure. On all subsequent days ofmeasurement the reduction was smaller. In all samples,recovery was completed within 18 h. ETRmax and UVsensitivity were high in samples collected under the ice.After sea-ice break-up, initial ETRmax and UV sensi-tivity were lower.

Specimens of Monostroma aff. arcticum collectedbelow the ice (12 June) exhibited a high sensitivitytowards UV exposure (Fig. 6). Initial Fv/Fm values werearound 0.78, decreased to only 0.12 after UV exposure,but completely recovered within 18 h. Curiously, sam-ples collected on 17 June showed a significantly(P<0.001) lower UV sensitivity, which, however,became higher again in the further course of the season.As in the other species, the maximum quantum yield ofphotosynthesis decreased during the period of clearwater. A peculiar feature of this species was the markedreduction of ETRmax values throughout the open-waterperiod.

Discussion

This is the first study showing the responses of photo-synthesis of various macroalgal species to UV radiationduring the times of strongly changing radiation condi-tions from before sea-ice break-up in late winter throughperiods of clear and later turbid water characteristic ofArctic fjords (Svendsen et al., unpublished data).

Plants grown under dim light conditions generallyexhibit a high sensitivity towards UV radiation(Teramura 1986). However, distinct differences in UVtolerance among different plant species, which wereraised under identical culture conditions, indicate thatgenetic adaptation to environmental stress as well asacclimation strategies contribute to the response in UV-exposure experiments (Bischof et al. 1998a,b, 1999).Two main strategies to prevent UV-induced photo-damage have been described for algae: (1) the accumu-lation of detoxifying enzymes and specific scavengersagainst reactive oxygen species (Lesser et al. 1990; Ma-langa and Puntarulo 1995; Lesser 1996), and (2) thebiosynthesis of UV-absorbing compounds (Karentz etal. 1991; Dunlap and Shick 1998; Karsten et al. 1998,1999; Cockell and Knowland 1999). The contribution ofthese two mechanisms to the seasonal changes in the UV

Fig. 5. Palmaria palmata (a),Devaleraea ramentacea (b).Seasonal response to UV radi-ation of red algal species. Leftpanels: maximum quantumyield of photosynthesis (Fv/Fm)as measured immediately aftercollection (black bars), after 2 hof UV exposure (hatched bars)and after 18 h of recovery un-der UV exclusion (shaded bars);right panels: the respectivemaximum photosynthetic rate(ETRmax) before (filled circles)and after (open squares) UVexposure

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sensitivity of photosynthesis is discussed in detail byAguilera et al. (2002).

The Laminaria species sampled in May were exposedto negligible UV radiation for more than half a year.Therefore, the response to artificial UV exposure reflectsthe genetically fixed ability to cope with UV radiation(Fig. 3). The fact that the degree of inhibition after UVexposure was highest in L. solidungula reflects the strongshade adaptation of this endemic Arctic deep-waterspecies (Dunton and Jodwalis 1988; Table 1). Further-more, it confirms that the upper distribution limit ofmacroalgae is determined in part by their ability to resisthigh radiation stress including UV radiation (Hanelt1992, 1998; Bischof et al. 1998a). The persistent UV-induced inhibition of photosynthesis after 18 h ofrecovery in all three species is typical of thalli notacclimated to UV radiation. The potential for recoveryfrom either UV stress or radiation stress in general is oneimportant prerequisite for algae living in the uppersublittoral zone, allowing these species to cope with thedrastic changes in irradiance in the Arctic (Hanelt et al.1997a; Bischof et al. 1998b). Additionally, the differencein UV sensitivity between 6-month-old and adult thalliof L. saccharina (Fig. 3) shows the contribution of age-dependent morpho-functional features to UV tolerance(Dring et al. 1996; Hanelt et al. 1997b) and to generalphotosynthetic performance (Gomez et al. 1996). Itremains to be determined if only optical effects, e.g. thepathlength for UV absorption and shading of inner cellsby outer cell layers, are the bases for the changing UVtolerance with increasing thallus age. Cellular defencemechanisms may also become more active in older thalli(Franklin and Forster 1997). It is expected that thedifferences in UV sensitivity between different age classesare present in all studied species of Laminaria. Theminimal difference in the young and old specimens ofL. digitata is probably because the young thalli alreadyhad the same morphology as the older individuals.

The morphologically similar L. saccharina and Sac-corhiza dermatodea show a high degree of photoinhibi-tion after UV exposure throughout the study period(Fig. 4a, b). In contrast to the sample of L. saccharina

taken in May, all subsequent samples including the un-der-ice samples of 13 and 18 June show an almostcomplete recovery. As daily UVB doses (Fig. 2) andwater transparencies (Fig. 5 in Hanelt et al. 2001) werehigh during this time, the degree of recovery may indi-cate an acclimation to UV radiation penetrating throughmore transparent areas and cracks in the sea ice. Al-ternatively, these species may anticipate radiation stresscued by an external factor, e.g. daylength (cf. Kain1989). A higher degree of acclimation to UV radiationduring the rest of the study period is – although poten-tially possible (Bischof et al. 1998b) – obviously notnecessary for adult specimens of these species at thiswater depth and under the prevailing radiation regime.Deep-water individuals of these species are protectedfrom UV exposure by the water column above, as themaximum penetration depth of UVB is about 10 m inthe waters of Kongsfjord (Bischof et al. 1998b; Haneltet al. 2001). The strongly elevated ETRmax values duringthe time after sea-ice break-up are probably attributableto the underwater light and are regarded as a feature oftheir life strategies, as shown already for various Arcticand Antarctic macroalgae (Dunton 1990; Gomez et al.1995; Gomez and Wiencke 1997). For example, thebrown algae Himantothallus grandifolius and Ascoseiramirabilis exhibit their optimum photosynthetic ratesright after the break-up of the ice cover (Drew andHastings 1992; Gomez et al. 1995) and are therefore ableto use the incident light efficiently for photosynthesisand growth.

Desmarestia aculeata exhibits a remarkable trend interms of seasonally increasing UV tolerance of photo-synthesis (Fig. 4c). The results indicate a stepwise acc-limation of photosynthesis to UV radiation, as recentlydescribed for the brown alga Alaria esculenta (Bischofet al. 1999). In these species, the degree of inhibition isincreasingly reduced during the open-water period. Thebasis of this ‘‘hardening’’ against UV exposure in thesebrown algal species remains unknown. UV-screeningMAAs (mycosporine-like amino acids) usuallyoccur only in trace amounts, if at all, in the Phaeophy-ceae (Karsten et al. 1998). The accumulation of

Fig. 6. Monostroma aff. arcti-cum. Seasonal response to UVradiation of the green algalspecies. Left panel: maximumquantum yield of photosynthe-sis (Fv/Fm) as measured imme-diately after collection (blackbars), after 2 h of UV exposure(hatched bars) and after 18 h ofrecovery under UV exclusion(shaded bars); right panel: therespective maximum photosyn-thetic rate (ETRmax) before(filled circles) and after (opensquares) UV exposure

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phlorotannins has been shown to play a role in theprotection of brown algae against UV radiation (Paviaet al. 1997). Especially in the case of D. aculeata, sea-sonally related changes in morphology might contributeto increasing UV tolerance. While young D. aculeataexhibit tufts of delicate assimilatory filaments in springto early summer, later in the season the upper parts ofthese filaments are aborted and corticated spine-likebranchlets are formed (Fletcher 1987). A relationshipbetween photosynthetic performance and morphologyhas recently been demonstrated for D. menziesii fromAntarctica (Gomez and Wiencke 1996). The seasonalpattern of ETRmax values in D. aculeata, with thehighest value on 13 June, resembles the seasonal patternof Pmax (determined as oxygen evolution) in D. menziesiiby Gomez and Wiencke (1997). D. menziesii culturedunder seasonally fluctuating Antarctic daylengths ex-hibited optimum photosynthesis under October condi-tions and about 50% lower rates between January andJuly.

Palmaria palmata also exhibits pronounced photo-synthetic responses to the seasonal variations in envi-ronmental conditions. The seasonal pattern of the Fv/Fm

values directly after collection in the field and the ad-justment of ETRmax values to the changes in underwaterlight climate (Fig. 5a) are comparable to the seasonalvariation of photosynthetic activity in the AntarcticP. decipiens (Weykam and Wiencke 1996; Weykam et al.1997; Luder et al. 2001). The relatively low inhibition ofphotosynthesis after UV exposure in specimens sampledunder conditions of clear water in June and July mayreflect the ability of P. palmata to increase its intracel-lular MAA concentration in response to increased solarradiation (Karsten and Wiencke 1999). As we will showin the second part of this study (Aguilera et al. 2002), thechanges in seasonal photosynthetic performance are infact linked to the accumulation of MAAs in the tissue aswell as to the seasonal patterns in glutathion reductase(GR) and superoxide dismutase (SOD) activity. Thecomparatively flexible response enables P. palmata totolerate the extremely variable environmental conditionsin the Arctic.

Devaleraea ramentacea always shows a relatively highFv/Fm value after UV exposure and exhibits little sea-sonal change in UV sensitivity. A considerable UV tol-erance in this species even persists under prolongedexposure to darkness and dim light under ice coverduring the polar night (Fig. 5b). As sea-ice break-up isusually a rapid process, species such as D. ramentacea,which occur predominantly in the uppermost sublittoral,get exposed to high solar radiation within hours or days(Gerland et al. 1999). Therefore, an early establishmentof an efficient UV defence is necessary before the icebreak-up is likely to occur. D. ramentacea always con-tains UV-absorbing MAAs (Aguilera et al. 2002) and isable to synthesise MAAs in response to the prevailingnatural radiation conditions (Karsten et al. 1999;Aguilera et al. 2002), a pattern characteristic for type IIspecies, as described by Hoyer et al. (2001). However,

the energy costs to maintain this precautionaryprotection system are not known. The high capacity ofD. ramentacea to cope with UV stress was shown to berelated to its ability to synthesise UV-absorbing MAAs,thus preventing UV-induced inhibition of photosyn-thetic electron transport (Karsten et al. 1999). The hightolerance of D. ramentacea towards radiation stressmight also be based on efficient scavenging of reactiveoxygen species, as indicated by permanently high activ-ities of SOD (Aguilera et al. 2002). However, the hightolerance to UV radiation might also be one feature ofthe generally high tolerance to various stresses of speciesfrom the uppermost sublittoral zone (Davison andPearson 1996).

In Monostroma aff. arcticum ETRmax decreases con-siderably from spring to summer while the degree ofphotoinhibition increases (Fig. 6), reflecting the phe-nology of this species as a seasonal annual (Kornmannand Sahling 1977). As documented also for M. grevilleifrom the Barents Sea (Schoschina et al. 1996), macro-thalli of the species studied here grow in late winter/spring and degenerate in summer. The photosyntheticapparatus of degenerating stages is generally very sen-sitive to various stresses, including UV stress as shown inthe present study.

In some species (L. saccharina, S. dermatodea,D. aculeata, P. palmata) the increase of ETRmax valueswas linked to increasing light availability after the break-up of sea ice. This acclimation was reversible as soon assolar irradiance decreased (Fig. 2) and water turbidityincreased. This reflects the high ability to adjust photo-synthesis to the respective radiation conditions, whichmay be due to a multitude of specific regulatory eventsincluding, e.g., the de- and acceleration of dark reactions(Scheibe 1990; Schmid and Dring 1996), the adjustmentof the absorption cross section (Hanelt and Nultsch1991), antenna size and number of active reaction cen-tres (Dau 1994) as well as pigment composition (Gomezand Wiencke 1997). Moreover, we also detected seasonalchanges in pigment composition in L. saccharina,S. dermatodea, D. aculeata, P. palmata and M. aff.arcticum, as described in detail by Aguilera et al. (2002).

At the Kongsfjord, the period of high solar irradianceand UVB exposure within the water column is relativelyshort. Nevertheless, the macroalgal communities mightseriously be affected by UVB, as maximum irradiancescoincide with maximum water transparency (Fig. 2;Hanelt et al. 2001). This is particularly crucial for speciesthat exhibit their main growth and reproductive activityat this time. In this context it should be mentioned thatspores, e.g. brown algal zoospores, are highly susceptibleto UV damage (Wiencke et al. 2000). The time courseand potential of acclimation to changing irradiances isecologically relevant given the probable increase ofharmful UVB radiation resulting from the thinning ofthe stratospheric ozone layer. Up to 60% loss ofstratospheric ozone over the Kongsfjord area has beenrecorded in recent years (Muller et al. 1997; Rex et al.1997). In our opinion macroalgal communities will

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probably be even more strongly affected in a scenario ofrising water temperatures due to the greenhouse effect.Under such conditions, the period of winter sea-icecover will be shorter and macroalgae will be exposed toenhanced UVB radiation for longer time periods. Theinteractive effects of UV radiation and temperaturehave, however, rarely been investigated, and, clearly,more ecophysiological and ecological studies are neededin this area.

Acknowledgements This work was performed at the Ny AlesundInternational Research and Monitoring Facility. Authors aregrateful to H. Lippert and E. Philipp for providing samples bySCUBA diving, as well as to the staff at Koldewey Station, Spits-bergen. Funding by the European Union within the Environmentand Climate Programme (project ENV4-CT96-0188, DG12-UV/Marine Macrophytes) and by the German Ministry for Educationand Research (BMBF-project: MONA, 03FO229A) is gratefullyacknowledged. J. Aguilera is especially thankful to the Alexandervon Humboldt Foundation for a postdoctoral fellowship. Finallywe would like to express our sincere thanks to the three anonymousreferees for their constructive criticism. The experiments complywith the current laws of Germany and Norway.

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