Rev Environ Sci Biotechnol DOI 10.1007/s11157-006-9106-z
REVIEW
Life strategy, ecophysiology and ecology of seaweeds in polar waters
C. Wiencke Æ M. N. Clayton Æ I. Go´ mez Æ K. Iken Æ U. H. Lu¨ der Æ C. D. Amsler Æ U. Karsten Æ D. Hanelt Æ K. Bischof Æ K. Dunton
Received: 7 March 2006 / Accepted: 8 May 2006 Springer Science+Business Media B.V. 2006
Abstract Polar seaweeds are strongly adapted to present knowledge of seaweeds from both polar the low temperatures of their environment, Ant- regions with regard to the following topics: the arctic species more strongly than Arctic species history of seaweed research in polar regions; the due to the longer cold water history of the Ant- environment of seaweeds in polar waters; biodi- arctic region. By reason of the strong isolation of versity, biogeographical relationships and vertical the Southern Ocean the Antarctic marine flora is distribution of Arctic and Antarctic seaweeds; life characterized by a high degree of endemism, histories and physiological thallus anatomy; tem- whereas in the Arctic only few endemic species perature demands and geographical distribution; have been found so far. All polar species are light demands and depth zonation; the effect of strongly shade adapted and their phenology is salinity, temperature and desiccation on supra- finely tuned to the strong seasonal changes of and eulittoral seaweeds; seasonality of reproduc- the light conditions. The paper summarises the tion and the physiological characteristics of
C. Wiencke (&) Æ U. H. Lu¨ der U. Karsten Alfred Wegener Institute for Polar and Marine Institute of Biological Sciences, Research, Am Handelshafen 12, D-27570 Applied Ecology, University of Rostock, Bremerhaven, Germany Albert-Einstein-Strasse 3, D-18051 Rostock, e-mail: [email protected] Germany
M. N. Clayton D. Hanelt School of Biological Sciences, Monash University, Biocenter Klein Flottbek, University P.O Box 18, Melbourne, Victoria 3800, Australia of Hamburg, Ohnhorst-Str. 18, D-22609 Hamburg, Germany I. Go´ mez Instituto de Biologı´a Marina, Universidad Austral de K. Bischof Chile, Casilla 567, Valdivia, Chile Institute for Polar Ecology, University of Kiel, Wischhofstr. 1–3, D-24148 Kiel, K. Iken Germany Institute of Marine Science, University of Alaska Fairbanks, O’Neill Bldg., Fairbanks, AK 99775, USA K. Dunton Marine Science Institute, University of Texas at C. D. Amsler Austin, 750 Channel View Drive, Port Aransas, Department of Biology, University of Alabama at TX 78373, USA Birmingham, Birmingham, AL 35294-1170, USA
123 Rev Environ Sci Biotechnol microscopic developmental stages; seasonal of the Arctic Sea’’ (Kjellman 1883) is a taxonomic growth and photosynthesis; elemental and nutri- and biogeographic baseline study. Detailed stud- tional contents and chemical and physical ies on seaweeds from Greenland were made by defences against herbivory. We present evidence Rosenvinge (1898), and in the 20th century by to show that specific characteristics and adapta- Lund (1951, 1959a, b) and Pedersen (1976). tions in polar seaweeds help to explain their Taxonomic information concerning seaweeds ecological success under environmentally extreme from Spitsbergen and the Russian Arctic is also conditions. In conclusion, as a perspective and available in publications by Svendsen (1959), Zi- guide for future research we draw attention to nova (1953; 1955), Vinogradova (1995) and many many remaining gaps in knowledge. others. A very valuable contribution on seaweeds from the north-eastern coast of North America is Keywords Chemical ecology Æ Freezing Æ the book by Taylor (1966; first published 1937). Growth Æ Light Æ Phenology Æ Photosynthesis Æ The first extensive diving studies were performed Polar algae Æ Salinity Æ Seaweeds Æ Temperature by Wilce (1963), Chapman and Lindley (1980) and by Dunton et al. (1982) in the Canadian and Alaskan Arctic. As in Antarctica, diving is an History of seaweed research in the polar regions essential prerequisite for detailed studies on all aspects of seaweed biology and this technique has The first phycological studies in the Arctic and since been widely applied in several regions of the the Antarctic regions took place in the first half Arctic. Since 1991 there has been intensive re- of the 19th century. Studies on Antarctic sea- search on the ecology and ecophysiology of weeds started in 1817 with the work of Gaudi- Arctic seaweeds on Spitsbergen (Hop et al. 2002; chaud, Bory, Montagne, Hooker and Harvey Wiencke 2004). (Godley 1965). Later, between 1882 and 1909, intensive studies were carried out by Skottsberg, Reinsch, Gain, Hariot, Kylin, Hylmo¨ , Foslie and The environment of seaweeds in polar waters others (Papenfuss 1964). After this period of mostly taxonomic and biogeographical investiga- The polar regions are characterized by pro- tions, which culminated in the publication of the nounced seasonal variations of the light regime, catalogue by Papenfuss (1964), numerous diving low temperatures, and long periods of snow and investigations were conducted in West Antarctica ice cover. Littoral seaweed communities are often by, among others, Neushul (1965), De´le´pine et al. strongly impacted by icebergs and sea ice espe- (1966), Lamb and Zimmermann (1977), Moe and cially in areas with high wave action (Klo¨ ser et al. DeLaca (1976), Richardson (1979), Klo¨ ser et al. 1994). Icebergs can run aground in the Antarctic (1996) and in East Antarctica by Zaneveld (1968) down to 600 m depth (Gutt 2001). First-year sea and Cormaci et al. (1997). These studies gave ice has a thickness of up to 2 m, and in the Arctic greater insight into the depth distribution of multi-year ice can reach depths of about 40 m Antarctic seaweeds and allowed more detailed (Gutt 2001). Anchor ice forms on the seabed in studies on the life histories, ecophysiology and shallow waters and can enclose seaweeds espe- ecology of seaweeds from Antarctica. The highly cially in East Antarctica (Miller and Pearse 1991). fragmented information on the seaweeds of The seasons in the sublittoral are characterized Antarctica was summarized recently in a synopsis in polar regions by short periods of favourable by Wiencke and Clayton (2002). light conditions and extended periods of darkness Early algal research in the Arctic started in due to the polar night and sea ice cover in winter 1849 in the Canadian Arctic with Harvey and (Kirst and Wiencke 1995). At the poleward Dickie (Lee 1980). The Russian phycologist distribution limits of seaweeds, at 77 S and Kjellman worked in many places in the Arctic, 80 N, respectively, the annual solar radiation is especially in the Russian Arctic, the northern 30–50% less than in temperate to tropical regions, Bering Sea and Spitsbergen. His book ‘‘The algae and the polar night lasts for about 4 months
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(Lu¨ ning 1990). At lower latitudes, e.g. close to the thesis as well as the photomorphogenetic devel- northern limit of the Antarctic region, in the opment of the understorey (Salles et al. 1996). South Shetland Islands, daylength varies between The possible impact of enhanced UVB 5 h in winter and 20 h in summer (Wiencke radiation due to stratospheric ozone depletion on 1990a). This extreme light regime has strong primary production of seaweeds is higher during implications for primary productivity in general the spring season, as organisms in the eulittoral and for the seasonal development of seaweeds. In and upper sublittoral zone are already affected by addition the long periods of darkness are further UVB radiation throughout the polar day and tur- extended due to the formation of sea ice. If the bid melt water input occurs only during the sum- ice is also covered by snow, irradiance can be mer season. The strong increase of turbidity due to diminished to less than 2% of the surface value. a discharge of sediments by melt water and gla- Consequently, seaweeds may be exposed up to ciers applies especially to Arctic shorelines in half- about 10 months of darkness or very low light open fjord systems where the water exchange with conditions (Chapman and Lindley 1980; Dunton the clearer oceanic water is retarded (Svendsen 1990; Miller and Pearse 1991; Drew and Hastings et al. 2002). On open coastlines the melt water is 1992; Klo¨ ser et al. 1993). exchanged much faster with clear oceanic water so After sea ice break-up in spring, light pene- that seaweeds are exposed to biologically effective trates deeply into the clear water. On King UVR for longer time periods. George Island (South Shetland Islands) at this The inflow of melt water in summer has con- time average photon fluence rates are 70 lmol siderable effects on the salinity and temperature m–2 s–1 at midday in 30 m depth (Go´ mez et al. regime in inshore waters. During times of calm 1997). On Signy Island (South Orkney Islands) the weather, there is a strong stratification in the euphotic zone, i.e. the 1% depth for photosyn- water body with a layer of fresh water above a thetically active radiation (PAR), was determined layer of denser sea water. However, due to ver- at 29 m (Brouwer 1996). UV-radiation (UVR) tical water mixing by wave action and wind the and blue light are, however, more strongly atten- deeper water zones also become affected and a uated. The 1% depth for UVB radiation, repre- salinity decrease may occur down to about 20 m senting more or less the threshold irradiance of depth (Hanelt et al. 2001). UV-B with the potential to affect primary plant In contrast to the strong seasonal variation in the productivity negatively, is located between 4 and radiation conditions, water temperatures in the 8 m on Spitsbergen (Hanelt et al. 2001; van de sublittoral mostly change only little between – Poll et al. 2002). Later, in summer, coastal waters 1.8 C in winter and +2.0 C in summer, e.g. in the in polar regions become more turbid due to the Antarctic Peninsula region (Drew and Hastings development of phytoplankton blooms and the 1992; Klo¨ ser et al. 1993). At the boundary with the inflow of melt water carrying fine sediments and temperate region, maximum summer tempera- detritus that strongly affect light transmission. tures can go up to about 5 C in the Antarctic and up With increasing turbidity the wavelengths shift to about 8–10 C in the Arctic (Wiencke and tom from the blue to the green waveband in deep Dieck 1989; Lu¨ ning 1990; Svendsen et al. 2002). waters (Jerlov 1976). Consequently, sublittoral Macronutrient concentrations are high and not seaweeds are exposed only to low irradiances even limiting for seaweeds at any time of the year in though the sun altitude is relatively high (e.g. the Antarctic (Deacon 1937; Drew and Hastings about 34 elevation in July compared to only 14 1992). However, iron concentrations are low in in April at 79 North at noon). the Antarctic and inhibit phytoplankton growth In a canopy of kelps or other overstory brown (de Baar 1994; de Baar et al. 1995). Whether iron algae, PAR is strongly attenuated, and understorey deficiency also affects seaweeds is unclear. High species are exposed to even lower irradiances macronutrient concentrations are also present in (Hanelt et al. 2003). The light quality also changes. the area of Spitsbergen, which obtains nutrient- Below the canopy the spectrum is enriched in green rich water from the south during parts of the year and in far red light, probably affecting photosyn- (the so-called Spitsbergen current). This is one
123 Rev Environ Sci Biotechnol reason why the seas of the European Arctic temperatures, on the thickness of the ice cover in belong to the most productive seas in the world winter. (Orheim et al. 1995). In general, there is a con- Despite the remoteness of the polar regions siderable seasonal fluctuation of macronutrients. pollution is an issue both in the Arctic and the Nitrogen and phosphorus levels are relatively Antarctic. For example, radionuclide contami- high during the winter months but both ma- nants such as Technetium-99 (99Tc) are present cronutrients are almost fully depleted in summer around the Arctic archipelago of Svalbard (Chapman and Lindley 1980). This applies also to through the long-range oceanic transport of dis- the area close to Spitsbergen (Aguilera et al. charges of radioactive effluents from nuclear 2002). reprocessing plants in Europe and global fallout The tidal amplitudes on King George Island (Gerland et al. 2003; Gwynn et al. 2004). Another and on Spitsbergen vary between 120 and 150 cm problem are oil spills. When the Argentinean ship (Scho¨ ne et al. 1998; Svendsen et al. 2002). Like Bahia Paraiso ran aground near Anvers Island at terrestrial vegetation, supra-and eulittoral sea- the Antarctic Peninsula more than 150,000 gal- weeds are exposed to strongly changing light lons of petroleum were released to the sur- conditions and temperatures, but also frequently rounding bays (Kennicutt II et al. 1990). Such oil to desiccation and low or high salinities due to the spills can potentially cause servere harm tidal regime and the weather. Photon fluence depending on the amount and type of material rates close to terrestrial cryptogams in the mari- released. time Antarctic vary between 0.1 mol m–2 d–1 in winter and more than 30 mol m–2 d–1 with max- ima around 1600 lmol m–2 s–1 in summer Biodiversity, biogeographical relationships (Schroeter et al. 1995; Winkler et al. 2000). The and vertical distribution of Arctic and annual variation of thallus temperatures of a Antarctic seaweeds lichen growing on a coastal rock on King George Island (Antarctica) was between +27.4 Cin The Arctic and the Antarctic Oceans differ summer and –27.3 C in winter (Schroeter et al. considerably with respect to their genesis and 1995). However, smaller annual amplitudes of their cold water history. The Southern Ocean has only 10 C also occur depending on the degree of had no land bridge to temperate regions since the exposure and snow cover (Winkler et al. 2000). late Mesozoic and has been further separated With increasing temperature in spring the from the neighbouring southern continents by the supralittoral is flushed by meltwater, followed by Antarctic Circumpolar Current since 26 Ma a period of desiccation in summer, which can be (Hempel 1987; Lu¨ ning 1990; Kirst and Wiencke interrupted by rehydration during rain-or snow- 1995). During the first major glaciation in East fall (Davey 1989; Schroeter et al. 1995) or during Antarctica 14 Ma ago water temperatures de- high tides. Salinity changes strongly in the supr- creased and they have been low in the Southern alittoral due to the effects of tides, salt spray, Ocean since then (Crame 1993). In contrast, the desiccation, overflow with melt water and pre- broad shelf areas of the Arctic Ocean have had a cipitation. In the eulittoral salinity rises are less continuous connection to the temperate coasts of strong and less frequent than in the supralittoral. America and Eurasia, and a perennial ice cover On the other hand, low salinities are quite com- did not develop before 0.7–2.0 Ma ago (Clarke mon during low tides, precipitation and meltwater 1990). These distinctions are the major reasons discharge. Klo¨ ser (1994) determined salinities for the differences in seaweed biodiversity of both between 27 and 41 PSU in the eulittoral on King polar regions. George Island. At low tide temperatures in tide The strong isolation of the benthic seaweed pools may rise far above the coastal water tem- flora of the Southern Ocean has resulted in a high peratures up to almost 14 C in summer (Klo¨ ser degree of endemism in Antarctica. 33% of all 1994; Moore et al. 1995). Winter temperatures seaweed species are endemic to the Antarctic may be very low and depend, apart from the air region. Within the Heterokontophyta 44% of the
123 Rev Environ Sci Biotechnol species are endemic, within the Rhodophyta 32% mated due to the infrequency of scientific col- and within the Chlorophyta 18% (Wiencke and lections, the extreme remoteness and logistic Clayton 2002). There is one endemic order, the difficulties. In Antarctica most species occur in kelp-like brown algal order Ascoseirales, and the Antarctic Peninsula region and only very few there are several endemic genera: among the species are recorded at the southernmost distri- brown algae, Himantothallus, Cystosphaera and bution limit in the Ross Sea. A similar decrease in Phaeurus, among the red algae Gainia, Noto- species richness has been detected in East phycus and Antarcticothamnion, and among the Greenland between Scoresby Sound, Franz green algae Lambia and Lola (Wiencke and Josephs Fjord and Jo¨ rgen Bro¨ nlunds Fjord (70, 74 Clayton 2002). Well-known Antarctic endemic and 82 N, respectively; Lund 1951, 1959a, b). On species include the brown algae Himantothallus the panarctic level, macroalgal species richness grandifolius, Cystosphaera jacquinotii, the red seems to dramatically decrease from the western alga Porphyra endiviifolium and the green alga (Atlantic) sector to the eastern (Pacific) sector. Lambia antarctica. The Antarctic region is the While about 70 species have been recorded from only region in the world devoid of kelps, brown the Svalbard region (Weslawski et al. 1993, 1997; algae of the order Laminariales (Moe and Silva Vinogradova 1995), only about 10 species are 1977). This order is ecologically replaced by the known from the rocky littoral regions in the Desmarestiales. According to phylogenetic and Alaskan Beaufort Sea (Dunton and Schonberg morphological analyses and studies on ecophysi- 2000). ological traits this order is considered to have As a result of the strong effect of the Antarctic originated in the Southern Ocean and subse- Circumpolar Current on the dispersal of seaweed quently radiated into the Northern Hemisphere propagules (Lu¨ ning 1990) many non-endemic (Peters et al. 1997). A conspicuous character of species of the Antarctic seaweed flora have a the Antarctic seaweed flora is the scarcity of small circumpolar distribution. Among the species also macroalgal epiphytes compared to temperate re- occurring on sub-Antarctic islands and Tierra del gions. In fact, these epiphytes are not absent, they Fuego are the red alga Iridaea cordata, the brown rather occur as endophytes inside larger sea- alga Geminocarpus geminatus and the green alga weeds, well protected against herbivory by mes- Monostroma hariotii. Some species, e.g. the red ograzers (Peters 2003). This suggests that alga Ballia callitricha and the brown alga mesoherbivory can be quite intense in Antarctica. Adenocystis utricularis, even occur in New Zea- In contrast to the strong endemism in Antarctic land and Australia. A similar connection between macroalgae only very few endemic Arctic species the Antarctic and the cold temperate region of have been found so far. About half a dozen species South America has also been recorded for marine are restricted to the Arctic including the brown invertebrates (Clarke et al. 2005). At least 20 algae Punctaria glacialis, Platysiphon verticillatus algal species from the Antarctic are cosmopolitan, and the red alga Petrocelis polygyna (Wilce 1990). e.g. the red alga Plocamium cartilagineum, the Most species have a distribution that extends well brown alga Petalonia fascia and the green alga into the temperate region, e.g. the kelp Laminaria Ulothrix flacca (Papenfuss 1964; Wiencke and solidungula and the red algae Devaleraea Clayton 2002). It is possible that some such spe- ramentacea, Turnerella pennyi, Neodilsea integra cies may be recent invaders from temperate and Pantoneura baerii (Lu¨ ning 1990). regions (Clayton et al. 1997). Compared to rich seaweed floras like those in A few seaweed species have a disjunct amphi- temperate southern Australia with about 1155 equatorial distribution and occur both in the species (Womersley 1991), low species richness is Antarctic and the Arctic, e. g. Acrosiphonia arcta characteristic for both polar seaweed floras. In the and Desmarestia viridis/confervoides. Molecu- Antarctic, 119 species have been recorded so far lar studies indicate that the biogeographic (Wiencke and Clayton 2002) and in the Arctic disjunctions of these species are recent and there are about 150 species (Wilce 1994). These probably date back to the maximum of the numbers are, however, likely to be underesti- Wu¨ rm/Wisconsin glaciation 18,00 years ago (van
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Oppen et al. 1993). The units of dispersal were common (Westermeier et al. 1992; Wiencke and certainly the microscopic stages in the life cycle Clayton 2002). Tide pools and crevices in the because they are more resistant to high temper- lower sublittoral are often colonized by upper atures allowing the possibility of a passage sublittoral species such as the red algae Palmaria through the tropics during times of lowered water decipiens and Iridaea cordata. The upper 5–15 m temperatures (Peters and Breeman 1992; of the sublittoral are exposed to ice floes and are Wiencke et al. 1994; Bischoff and Wiencke 1995a). often devoid of large, perennial algae. Only Apart from the few species endemic to the crustose species or developmental stages can Arctic and various cosmopolitan species such as persist here. Below this zone, large brown algae the red alga Audouinella purpurea, the brown dominate the sublittoral in West Antarctica: As- alga Scytosiphon lomentaria and the green alga coseira mirabilis and Desmarestia menziesii occur Blidingia minima, the Arctic seaweed flora has in the upper sublittoral, D. anceps in the mid affinities to the Atlantic, the Pacific and the sublittoral and Himantothallus grandifolius grows Indo-Pacific region (Wilce 1990). An example of in the lower sublittoral (DeLaca and Lipps 1976; an invader from the Pacific may be Acrosiphonia Lamb and Zimmermann 1977; Amsler et al. 1995; arcta. Populations of this species from the Arctic Klo¨ ser et al. 1996; Quartino et al. 2001, 2005). At and the North Atlantic seem to originate from the higher latitudes in East Antarctica only few spe- Pacific according to molecular studies (van cies occur, in particular Palmaria decipiens, Oppen et al. 1994). But over 90% of the species Phyllophora antarctica and I. cordata (Zaneveld in the Arctic originate from Atlantic populations 1968; Miller and Pearse 1991; Cormaci et al. (Dunton 1992). This is particularly obvious in 1992). regions with strong influx of Atlantic waters, e.g. In the Arctic the barren zone heavily exposed in Svalbard (Svendsen et al. 2002, Hop et al. to floating ice extends down to about 2 m water 2002). However, even in the coastal areas of the depth. The upper sublittoral on Spitsbergen is Beaufort Sea there is a strong Atlantic influence, characterized by the brown algae Fucus distichus, marked by the kelps Laminaria solidungula and Pylaiella littoralis, Chordaria flagelliformis, the Alaria esculenta (Dunton 1992) while the Cana- kelp Saccorhiza dermatodea, the red alga dian Arctic also has a high proportion of macro- Devaleraea ramentacea and green algae of the algae of Pacific origin (Cross et al. 1987). genus Acrosiphonia. The zone below is dominated In both polar regions seaweeds are almost by the kelps Alaria esculenta, Laminaria digitata entirely subtidal. However, there are some spe- and L. saccharina. Characteristic for the lower cialized species with a bipolar distribution that sublittoral are the red algae Phycodrys rubens and occur exclusively in the supralittoral, i.e. in the Ptilota gunneri. The Arctic kelp, L. solidungula, spray zone. These are the green alga Prasiola occurs in this zone as well but only in the inner crispa, which also grows more inland close to part of the fjords (Svendsen 1959; Hop et al. 2002; seabird rockeries under conditions of low pH and Wiencke et al. 2004). The seaweed vegetation in high nutrient concentrations (Knebel 1936) and the Canadian Arctic (Baffin Island) is similar to the red alga Bangia atropurpurea (Bird and Mc that in Spitsbergen with a shallow F. distichus Lachlan 1992; Clayton et al. 1997). The green zone, the upper sublittoral characterized by Stic- alga Urospora penicilliformis and species of the tyosiphon tortilis, P. littoralis and Dictyosiphon genus Ulothrix grow just around the high tide foeniculaceus (Cross et al. 1987). Deeper com- level both in the Antarctic and the Arctic. munities are dominated by the kelps L. saccha- Acrosiphonia arcta is a species typical for the rina, L. solidungula, A. esculenta and Agarum lower eulittoral in both polar regions. cribrosum, interspersed with the red algae Dilsea A conspicuous species in the upper eulittoral integra, D. ramentacea and Rhodomela confervo- in the Antarctic is the red alga Porphyra ides. In contrast, no supralittoral or intertidal endiviifolium and in the lower eulittoral/upper algae have been recorded from the Alaskan sublittoral the green alga Enteromorpha bulbosa Beaufort Sea. Here, algae are restricted to scat- and the brown alga Adenocystis utricularis are tered rocky habitats in shallow waters (about
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5–10 m), which are protected by barrier islands know today these taxa are characterized by a from iceberg scouring. Laminaria solidungula is highly diversified structure and complex morpho- the dominant kelp species, although Alaria escul- functional processes including a temporal syn- enta and L. saccharina can also be found regularly chronization between photosynthesis and growth (Dunton and Schonberg 2000). Characteristic red as well as the long-distance transport of organic algal species are Phycodrys rubens, Odonthalia substances (Lu¨ ning et al. 1973; Schmitz 1981; dentata, Dilsea integra, Phyllophora truncata and Clayton and Ashburner 1990; Drew and Hastings Rhodomela subfusca. Exposed rock is usually 1992; Go´ mez et al. 1996). Such characteristics covered by encrusting coralline red algae, Litho- represent strategies to cope with the marked thamnion spp. (Konar and Iken 2005). seasonality in polar and cold-temperate regions (Chapman and Lindley 1980; Go´ mez and Wiencke 1998; Go´ mez and Lu¨ ning 2001). Reproductive and physiological thallus anatomy As in other species of Laminaria the blade of L. solidungula has a basally located meristem, The enigma of reproduction and life histories of which is active only in winter and forms—com- endemic Antarctic Desmarestiales and of parable with L. hyperborea—a new blade at the Ascoseira mirabilis has been clarified. The sorus distal end (Taylor 1966; Dunton and Jodwalis structure of H. grandifolius (Moe and Silva 1981; 1988). Up to three generations of blades may be Wiencke and Clayton 1990), D. anceps (Moe and found in one individual. As in species of Lami- Silva 1981; Wiencke et al. 1996) and D. antarctica naria, blades of Himantothallus grandifolius grow (Moe and Silva 1989; Wiencke et al. 1991) is in their lower part (Dieckmann et al. 1985; Drew similar, indicating an evolutionary relationship. and Hastings 1992). Punch-hole experiments with Unilocular sporangia are cylindrical, borne ter- A. mirabilis indicate that the blade elongates minally on 2–4 celled stalks and are interspersed longitudinally as in Laminaria solidungula with paraphyses composed of 2–4 cells with many through a seasonally active intercalary meristem physodes. With respect to sorus morphology, D. (Go´ mez et al. 1995a). menziesii exhibits a closer similarity to the Arctic Carbon fixation rates in kelps and kelp-like cold-temperate species D. aculeata (Wiencke brown algae differ between blade parts (Arnold et al. 1995), whereas Phaeurus antarcticus and Manley 1985; Go´ mez et al. 1995a, b; Cabello- resembles the North Atlantic-Mediterranean Pasini and Alberte 2001). During the growth species Arthrocladia villosa (Clayton and Wie- phase in late winter-spring, net photosynthetic ncke 1990). In P. antarcticus, sporangia are cate- rates (net Pmax)inA. mirabilis are slightly higher nate and develop in rows in adjacent cells as in the middle region compared to the basal and filamentous outgrowths of the cortex, inter- distal regions (Go´ mez et al. 1995a). In compari- spersed with club-shaped sterile hairs. These son, in L. solidungula, C-fixation rates are lowest phylogenetic relationships have been confirmed in meristematic tissue, highest in first year tissue meanwhile by molecular data (Peters et al. 1997). and intermediate in second-blade tissue (Dunton Ascoseira mirabilis, whose exact phylogenetic and Jodwalis 1988). This pattern is related to the relationships are still unresolved, has a fucalean ontogeny within the blade, i.e. photosynthetic type of life history (Clayton 1987). There is one activity increases with age of the tissues reaching free-living diploid generation with conceptacles a maximum but then decreases with further aging. scattered over both surfaces. These contain den- In apical regions, erosion and senescence take sely packed chains of gametangia that release place. biflagellate isomorphic gametes. Zygotes develop Over the years, the blade in Ascoseira becomes into new individuals. thicker and more complex as new tissue is formed A striking feature of several Antarctic Des- each growth season, resulting in modifications not marestiales and A. mirabilis is their anatomical only of the photosynthetic gradients but also of complexity resembling that of Laminaria species the photosynthetic capacity and efficiency along from the northern Hemisphere. As far as we the thallus. Two age-components must be
123 Rev Environ Sci Biotechnol considered here: The age of the different blade The patterns of C-fixation in Ascoseira exhibit tissues and the age of the whole plant. In this also intra-blade variations (Go´ mez et al. 1995a) context, 2-year old plants of Ascoseira are although some differences with respect to pat- characterized by net Pmax and a-values almost terns reported in Laminaria are observed. Both twice that of 3-year old individuals. However, light dependent and light independent C-fixation other parameters such as dark respiration, satu- increase with tissue age reaching a maximum in ration (Ek) and compensation (Ec) points do not the middle/distal parts of the blade. In contrast, show obvious differences (Go´ mez et al. 1996). members of the Laminariales studied to date The photosynthetic variability correlated with show highest rates of light dependent carbon fix- tissue age may also be seen in terms of the ation in distal and highest light independent C development of the photosynthetic apparatus fixation in the basal parts (Ku¨ ppers and Kremer with ontogeny. In both age classes, middle regions 1978). The different thallus allocation of light have a higher net Pmax than basal and distal re- independent C fixation in A. mirabilis may be gions, suggesting that photosynthesis is low due to related to the high dark respiration rates observed the presence of a non-developed photosynthetic in distal blade regions (Go´ mez et al. 1995a, 1996). apparatus in the basal region, and decreases in the It is not clear, however, whether light indepen- oldest distal tissues due to senescence processes. dent C-fixation may compensate for C losses due Similar results were obtained in young and adult to respiration as reported by Kremer (1981b). plants of L. solidungula (Dunton and Jodwalis Thomas and Wiencke (1991) could not conclu- 1988). sively demonstrate a relationship between light Ku¨ ppers and Kremer (1978) associated the independent C-fixation and dark respiration in increased 14C-assmilation in the middle and distal Antarctic marine algae. In general, dark C-fixa- regions of Laminaria species with a higher activ- tion varied between 4.9% and 31% of dark ity of the Calvin cycle enzyme ribulose 1,5-bis- respiration in five brown algae and one red alga. phosphate carboxylase-oxygenase (RUBISCO). In species such as H. grandifolius and D. anceps, Moreover, these authors demonstrated longitu- low dark C-assimilation rates were coupled to dinal profiles in light independent C-fixation in high respiration rates as in Ascophyllum nodosum these species coupled to a high activity of the indicating a net C loss due to respiration in the enzyme phosphoenolpyruvate carboxykinase dark (Johnston and Raven 1986). (PEP-CK) in the meristematic region (b-carbox- In kelps sugars are synthesized and stored as ylation). The activities of these carboxylating polysaccharides (e.g. laminaran) in the middle enzymes apparently respond to the growth char- and distal assimilatory tissues of the algae, from acteristics of Laminaria. In fact, Laminaria spe- which they are then translocated as low-molecu- cies from cold-temperate and Arctic regions grow lar-weight compounds (e.g. mannitol) in trumpet in winter or in dim light and it is likely that such hyphae to the growth region (Kremer 1981a, b). an alternative carboxylating mechanism is The trumpet hyphae of Laminariales are elon- advantageous for these species (Ku¨ ppers and gated, longitudinally oriented cells in the medulla Kremer 1978). b-carboxylation is also linked to with trumpet like ends. The cross walls are per- the growth requirements of these algae. For forated by numerous pits resembling the sieve example, light-independent carbon fixation pro- plates of sieve tubes in higher plants (Schmitz vides C-skeletons (preferentially amino-acids) for 1981, 1990; Buggeln 1983). Similar trumpet hy- both biosynthesis and anabolic processes, thus phae are present in the medulla of H. grandifolius replenishing some carbon intermediates in e.g. (Moe and Silva 1981) and in the other Desma- the Krebs cycle (Kremer 1981b; Falkowski and restiales Phaeurus antarcticus (Clayton and Wie- Raven 1997). Particularly, in the meristematic ncke 1990), Desmarestia antarctica (Moe and region of Laminaria, PEP-CK uses CO2 lost in Silva 1989; Wiencke et al. 1991) and D. menziesii glycolysis of mannitol translocated from the distal (Scrosati 1992; Wiencke et al. 1995). The trumpet region to the meristem (Kremer 1981a; Kerby and hyphae can be interconnected by sieve plates and Evans 1983). are always surrounded by numerous small cells
123 Rev Environ Sci Biotechnol that probably function as transfer cells. In 15 C, whereas Kallymenia antarctica, Gymno- A. mirabilis longitudinally arranged ‘‘conducting gongrus antarcticus and Phyllophora ahnfeltioides channels’’ comparable to the trumpet cells found exhibit broad optima between 10 and 20 (to 25) C in Laminariales are present in the medulla (Eggert and Wiencke 2000). Studies on the few (Clayton and Ashburner 1990). The channels are Arctic seaweeds show a temperature optimum at aseptate, multinucleate structures with ensheath- 20 C (Healey 1972). For comparison, in cold-and ing filaments often interconnected through sieve- warm-temperate species optimum values of like wall perforations. Although no conclusive 20–25 C and 25–35 C were determined, respec- evidence for a possible transport function of the tively (Lu¨ ning 1990). The temperature optima for conducting channels in A. mirabilis is available, respiration are clearly above the optima for pho- differential allocation of reserve carbohydrates tosynthesis but temperatures higher than 30 C associated to meristem activity strongly suggest have never been tested in Antarctic seaweeds the involvement of these structures in long dis- (Drew 1977; Wiencke et al. 1993; Eggert and tance transport (Go´ mez and Wiencke 1998). Wiencke 2000). Photosynthesis:respiration ratios Overall, the findings that photosynthesis and are highest at the lowest tested temperature, 0 C, carbon allocation vary as a function of blade and decrease with increasing temperatures due to development add new evidence to a convergent different Q10 values for photosynthesis (1.4–3.5) morpho-functional evolution between large and respiration (2.5–5.1). Antarctic brown algae and Laminariales of the The high P:R ratios at low temperatures are northern Hemisphere. In this case not only mor- the major reason for the high growth rates of phological organization, but also the metabolic Antarctic species at low temperatures. In partic- differentiation along the blade, are common ular red and brown algal species from both polar characteristics of the taxa. Such characteristics regions exhibit temperature growth optima at certainly reflect adaptive mechanisms to with- 0–5 C or even at –2 C (Wiencke and tom Dieck stand resource limitation in seasonally changing 1989, 1990; Novaczek et al. 1990; Bischoff and environments, which have ultimately led to the Wiencke 1993; Bischoff-Ba¨smann and Wiencke ecological success of these algae in polar regions. 1996; Eggert and Wiencke 2000; McKamey and Amsler 2006). Some species like Georgiella con- fluens, Gigartina skottsbergii and Plocamium Temperature demands and geographical cartilagineum from the Antarctic grow only at distribution 0 C, the lowest temperature tested, but not at 5 C (Bischoff-Ba¨smann and Wiencke 1996). The up- Photosynthesis of polar seaweeds shows a con- per survival temperatures (USTs), determined siderable adaptation to the low temperatures of after 2-week-exposures to different temperatures, the environment. Maximum photosynthetic rates are as low as 7–11 C. Other Antarctic red algae of endemic Antarctic species are at a temperature grow up to 5 Cor10 C and have USTs of £19 C of 0 C similar to values from temperate species (Bischoff-Ba¨smann and Wiencke 1996). The measured at higher temperatures (Drew 1977; sporophytes of endemic Antarctic Desmarestiales Thomas and Wiencke 1991; Wiencke et al. 1993; grow up to 5 C and exhibit USTs of 11–13 C. In Weykam et al. 1996; Eggert and Wiencke 2000). contrast, their gametophytes grow up to 10 Cor Moreover, the temperature optima for photosyn- 15 C and have USTs between 15 C and 18 C thesis at least in some species from the Antarctic (Wiencke and tom Dieck 1989, 1990). The upper are well below values determined in temperate limit for gametogenesis (ULG) in D. antarctica is species. The lowest temperature optima have 5 C (Wiencke et al. 1991). Antarctic cold-tem- been determined in the brown algae Ascoseira perate species (especially from the eulittoral) mirabilis (1–10 C) and Himantothallus grandifo- have higher temperature requirements. They lius (10–15 C; Drew 1977; Wiencke et al. 1993). grow up to 10–15 (or 20) C and show USTs The red algae Ballia callitricha and Gigartina between 13.5 C and 19 C. Microthalli of skottsbergii also exhibit values between 10 and Antarctic cold-temperate brown algae exhibit
123 Rev Environ Sci Biotechnol
USTs between 21 C and 25 C and ULGs between and gametophytes as well as the temperature 13 Cand15 C (Wiencke and tom Dieck 1990; demands for growth of the gametophytes are Peters and Breeman 1993). irrelevant for the explanation of the geographic As far as we know today the temperature de- distribution of these species. mands for growth of Arctic seaweeds are some- The distribution of Arctic North Atlantic spe- what higher than endemic Antarctic species. It cies is often limited both by the USTs and the must, however, be pointed out that the tempera- ULGs (van den Hoek 1982a, b; Breeman 1988; ture demands of truly endemic Arctic species (see Lu¨ ning 1990). In such taxa, distribution limits in chapter 3) have not been investigated so far. The the West Atlantic are determined by lethal, high sporophyte of the kelp Laminaria solidungula, summer temperatures, whereas they are deter- whose distribution extends into the cold-temper- mined in the East Atlantic by high winter tem- ate region as far as Newfoundland, grows at peratures inhibiting reproduction. Examples for temperatures up to 15 C with an optimum at species from this group are Laminaria digitata, 5–10 C and USTs of 16 C (tom Dieck 1992). The Chorda filum and Halosiphon tomentosus. male and female gametophytes of this species During the ice ages both polar regions were exhibit an UST of 18 C and lower survival tem- inhospitable for seaweeds. In the Southern peratures (LSTs) of £–1.5 C (Bolton and Lu¨ ning Hemisphere the sub-Antarctic islands probably 1982; tom Dieck 1993). The red alga Devaleraea served as refugia. The South American Archipel- ramentacea, which is distributed from the Arctic ago may also have hosted species escaping from to the cold temperate North Atlantic region, the coasts of the Antarctic continent (Skottsberg grows at up to 10 C with an optimum at 0 C and 1964). At the maximum of the last ice age the 5 C exhibits an UST of 18–20 C and an LST of £–5 C. summer isotherm, the boundary of the Antarctic The ULG of this species is 8 C (Novaczek et al. region just touched the southern tip of South 1990; Bischoff and Wiencke 1993). Macrothalli of America (CLIMAP project members 1981). species with a prominent distribution in both, the Migration of species from the Antarctic continent Arctic and the cold-temperate region, grow at up to South America and vice versa probably to 15 or 20 (to 25) C with optima between 5 and occurred along the Scotia Arc, a well-recognized 15 (to 20) C and exhibit USTs between 17 and 25 route for animals (Knox and Lowry 1978). In the (to 26) C. The LSTs are £–1.5 or 2 C (Wiencke Northern Hemisphere cold water seaweeds of the et al. 1994). The microscopic gametophytes of Atlantic with ULGs and upper temperature limits Arctic cold-temperate Laminariales grow at up to for growth at 10 or 15 C experienced an extreme 20 C and have USTs between 22 and 25 (to reduction in the distribution area during the ice 28) C. Gametophytes of Alaria esculenta and ages (van den Hoek and Breeman 1989). The dis- Agarum cribrosum, however, exhibit USTs of 19– tribution of these species was compressed by the 21 C, as low as those of the more Arctic species glaciers in the North and the 10–15 C winter Laminaria solidungula. The LSTs are either 0, isotherm, their southern reproduction boundary. –1.5 or –2 C, the few data on ULGs vary between This is the likely explanation for the present 10 C and 17 C (Wiencke et al. 1994). depauperate flora in the North West Atlantic. The northern distribution of endemic Antarctic Comparable conditions did not exist in the North species is often limited by the temperature de- Pacific, probably a major reason for the richness of mands for growth. This applies especially to the cold North Pacific. members of the endemic Antarctic species of the During periods of lowered temperatures taxa order Desmarestiales. In these taxa the northern with relatively high temperature demands were distribution limit is determined by the tempera- able to extend their distribution limits towards ture requirements for growth of the sporophytes the equator. Species with an amphiequatorial (Wiencke and tom Dieck 1989), which occur only distribution e.g. Acrosiphonia arcta (Bischoff and south of the Antarctic convergence in areas with Wiencke 1995a), Urospora penicilliformis (Bischoff maximum temperatures £5 C allowing growth of and Wiencke 1995b) and Desmarestia viridis/ their sporophytes. The USTs of their sporophytes confervoides (Peters and Breeman 1992) have
123 Rev Environ Sci Biotechnol probably crossed the equator during the Pleisto- (Wiencke et al. 1993; Eggert and Wiencke 2000). cene lowering of the water temperatures in the The highest degree of shade adaptation with –2 –1 tropics (Wiencke et al. 1994). The USTs of these average Ek values around 3 lmol m s has taxa are with 25–27 C slightly above the mini- been demonstrated in coralline algae from the mum tropical sea surface temperatures of Ross Sea (Schwarz et al. 2005). 23–25 C during the last glaciation (CLIMAP Pro- The vertical distribution of dominant Antarctic ject members 1981). These results are supported by seaweeds such as Desmarestia or Himantothallus molecular studies indicating an almost complete can be extremely wide in contrast to the algal sequence identity in amphiequatorial populations zonation patterns from cold-temperate and tem- of A. arcta and D. viridis/confervoides in the fast- perate regions, where zonation patterns are evolving internal transcribed spacer regions of the characterized by narrow belts of species (Lu¨ ning ribosomal DNA (van Oppen et al. 1993). 1990). However, no evidence of an acclimation to the prevailing light conditions at different depths could be demonstrated in five species of seaweeds Light demands and depth zonation along a depth gradient between 10 m and 30 m (Go´ mez et al. 1997). Apparently, the intrinsic low At high latitudes, the radiation regime imposes light requirements for photosynthesis account for severe constraints not only in terms of seasonal these patterns. In the Antarctic spring-summer, light availability but also in regard to the vertical due to high water transparency irradiances of distribution of benthic algae (Go´ mez et al. 1997). PAR around 20 lmol m–2 s–1 reach the depth of Because of the extreme environmental conditions 30 m, with 1% of the surface irradiance present at in the eulittoral, polar algae are mainly sublittoral depths >40 m (Go´ mez et al. 1997). Although and thus low light demands and tolerance to these levels are clearly lower than average darkness are a pre-requisite for occurrence down midday irradiances (30–325 lmol photon m–2 s–1) to great depths (Arnoud 1974; Zielinski 1981; at 30 m in some clear temperate and tropical Richardson 1979; Klo¨ ser et al. 1993; Amsler et al. waters (Peckol and Ramus 1988), they exceed 1995). An important feature is the dark tolerance reported saturation and compensation points of of the microscopic developmental stages. Various photosynthesis in many Antarctic seaweeds Antarctic and Arctic seaweeds tolerate a dark (Weykam et al. 1996). period of up to 18 months (tom Dieck 1993; As for photosynthesis, the light demands for Wiencke 1988, 1990a). Further evaluation of the growth are similarly very low. In microscopic relation between photosynthetic characteristics developmental stages of Antarctic seaweeds and algal zonation in 36 macroalgal species from growth is light saturated already at 4–12 lmol King George Island (Weykam et al. 1996, Go´ mez m–2 s–1 (Wiencke 1990a). In young sporophytes of et al. 1997) indicates a high degree of shade Antarctic Desmarestiales growth is saturated at adaptation: (a) photosynthetic efficiency (a)is 15–20 lmol m–2 s–1 (Wiencke and Fischer 1990). high in all the studied species, reflecting a clear In the case of Arctic species, low light shade adaptation over a broad range of depth; requirements for photosynthesis have also been (b) seaweeds growing at depths >10 m exhibit found in nine species from Spitsbergen (Latala low saturation points for photosynthesis (Ek;<40 1990) and in crustose coralline red algae from the lmol m–2 s–1) irrespective of their taxonomic high Arctic (Roberts et al. 2002). Meristematic position; (c) the highest Ek values (>50 lmol tissue of both juvenile and adult individuals of m–2 s–1) are found in species common in upper Laminaria solidungula from the Alaskan high sublittoral or eulittoral; (d) shallow water species Arctic exhibits Ek values between 20 and –2 –1 have higher photosynthetic capacity (Pmax) than 30 lmol m s , while the average Ek value of species from deeper waters. These data obtained vegetative blade tissue in adult plants is using field material are supported also by results 38 lmol m–2 s–1 (Dunton and Jodwalis 1988). obtained in studies using specimens grown from Photosynthetic efficiency (a) is higher than in unialgal cultures from the same study area Laminariales from the temperate region. Both the
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low Ek and a values indicate strong adaptation to 12 h at 30 m depth (Go´ mez et al. 1997). For the the long period of exposure to darkness in winter red algae Palmaria decipiens, Kallymenia antarc- under ice cover and in summer during times of tica and Gigartina skottsbergii a metabolic carbon high water turbidity. Another feature characte- balance between 0.6 and 0.8 mg C g–1 FW d–1 sets rising the dark adaptation of L. solidungula is the the limits for growth at >30 m. For Himanto- low compensation point (Ec) for growth close to thallus grandifolius, which dominates depths be- 0.6 lmol m–2 s–1 (Chapman and Lindley 1980). low 15 m, the daily carbon balance was low but Seaweeds able to grow in deep waters have relatively similar over a range between 10 m and developed metabolic strategies to maximize car- 30 m, indicating that this species can potentially bon fixation by avoiding excessive carbon losses grow even considerably deeper. Only in Des- due to respiration. Because at great depths, Ec for marestia anceps is growth clearly limited at 30 m photosynthesis exceed Ec values for growth and due to its negative carbon balance at this depth available irradiances are normally below the lev- (–1.9 mg C g–1 FW d–1;Go´ mez et al. 1997). The els required for saturation of photosynthesis, lower depth distribution limit of the red alga carbon assimilation may be just compensating Myriogramme mangini from the South Orkney dark respiration. In Antarctic brown algae, dark Islands has been predicted by photosynthetic respiration has a strong seasonal component and measurements to be at 23 m water depth during the growth period, respiratory activity may (Brouwer 1996). account for a considerable proportion of the gross Overall, polar seaweeds by virtue of their low photosynthesis (Go´ mez et al. 1995a, b). If one light demands are potentially able to grow over relates the daily light course of the irradiance to large ranges of depths. Depending on the water the Ek value, then the daily period for which characteristics the lower depth distribution limit of plants are exposed to irradiances >Ek (denomi- seaweeds both in the Antarctic and the Arctic is nated Hsat) can be estimated. The obtained located between 30 m and 90 m (Wilce 1994; metabolic daily carbon balance can be regarded Wiencke and Clayton 2002). However, other con- as a physiological indicator for the ability to grow straints such as competition also control algal in deep waters (Go´ mez et al. 1997). zonation. For example, red algae are metabolically Polar seaweeds exposed to marked seasonal able to live at great depths, however, they can be changes in daylength exhibit generally Hsat outcompeted by the large canopy brown alga values >0 h only during the short open water sea- Himantothallus (Klo¨ ser et al. 1996). Furthermore, son. Laminaria solidungula in a kelp bed in the ice abrasion and grazers, e.g. some invertebrate Alaskan Beaufort Sea at 70 N was exposed during and demersal fishes, have a strong influence on
August to September 1986 to total Hsat periods of zonation patterns (Iken 1996; Iken et al. 1997). up to 148 h (Dunton 1990). This value corresponds Antarctic seaweeds are not only strongly shade- to an average daily Hsat of 3 h. However, adapted but can also cope with high light condi- depending on the year, the average daily Hsat may tions in summer due to their ability for dynamic decrease down to < 0.5 h. Year-round underwater photoinhibition, a photoprotective mechanism by light measurements have yielded annual quantum which excessive energy absorbed is rendered budgets of 45 mol m–2 yr–1, the lowest ever docu- harmless by thermal dissipation (Krause and Weis mented for kelp populations globally (Dunton 1991; Demmig-Adams and Adams III 1992). This 1990). A similar low value, 49 mol m–2 yr–1, was capability is best expressed in species from the already obtained earlier by Chapman and Lindley eulittoral. Upper and mid sublittoral species show (1980), values considerably lower than in the a more or less pronounced decrease in photosyn- temperate L. hyperborea, which receives thetic activity during high light stress and full 71 mol m–2 yr–1 (Lu¨ ning and Dring 1979). recovery during subsequent exposure to dim light
For Antarctic seaweeds, Hsat measured during (Hanelt et al. 1997). In contrast, deep water and optimum light conditions in spring in five brown understory species recover only slightly and slowly, and red algae decreases with depth from values indicating photodamage. Similar findings as these close to 14 h at 10 m to values between 7 h and on Antarctic seaweeds have been demonstrated
123 Rev Environ Sci Biotechnol also in a detailed analysis of seaweeds from Spits- All Antarctic Chlorophyta studied possess as bergen (Hanelt 1998). Similarly, UV radiation is main organic osmolytes the carbohydrate sucrose now also regarded as a key factor affecting the and the imino acid proline, and—with the depth zonation of seaweed assemblages. This topic exception of Prasiola—a third compound, will be treated in detail in a separate paper in this b-dimethylsulphoniumpropionate (DMSP). issue (Bischof et al. in press). Prasiola is able to synthesize polyols such as sorbitol and ribitol instead of DMSP. The con- centrations of all osmolytes are actively regulated Effect of salinity, temperature and desiccation as a function of the external salinity. Because of on supra-and eulittoral seaweeds its physicochemical properties proline is one of the most potent organic osmolytes, which not Until now few ecophysiological studies have only balances salinity stress, but also may stimu- been undertaken on the salinity acclimation in late enzymatic activity. This imino acid is the polar seaweeds (Karsten et al. 1991a, b; Jacob most important osmolyte in ice-algae too (Tho- et al. 1991, 1992a). These papers indicate that mas and Dieckmann 2002). Sucrose is also a well- cells of eulittoral Chlorophyta from the Antarc- known osmotically active compound in many tic survive salinities between 7 psu and 102 psu higher and lower plants, and also exhibits a with a low rate of mortality, and that most taxa cryoprotective function. The osmotic function of grow, photosynthesize and respire optimally un- DMSP seems to be unique to Antarctic Chloro- der normal seawater conditions with rather broad phyta in comparison with temperate ones, be- tolerances between 7 psu and 68 psu. The supra- cause of very high intracellular concentrations littoral Prasiola crispa ssp. antarctica even grows and the strong biosynthesis and accumulation between 0.3 psu and 105 psu. Consequently, with increasing salinities. In addition, DMSP acts eulittoral and supralittoral macroalgae from as compatible solute and cryoprotectant (Karsten Antarctica can be characterized as euryhaline et al. 1996a). Polyols such as sorbitol are the most organisms. water-like molecules, and therefore represent not Osmotic acclimation in response to salinity only ideal osmolytes and compatible solutes, but changes is a fundamental mechanism of salinity exert a function as rapidly available respiratory tolerance that conserves intracellular homeostasis substrate (e.g. under desiccation) and as antioxi- (Kirst 1990). The acclimation process in Antarctic dant (Karsten et al. 1996b). The presence of high Chlorophyta involves the metabolic control of the concentrations of three organic osmolytes in cellular concentrations of osmolytes. The major Antarctic Chlorophyta may be related to the inorganic osmolytes are potassium, sodium and extremely cold habitat suggesting that, besides chloride (Karsten et al. 1991b; Jacob et al. 1991), their osmotic role, these solutes are playing mul- the cellular concentrations of which can be rap- tiple functions in metabolism such as cryopro- idly adjusted with low metabolic energy costs, tectants. In the case of P. crispa ssp. antarctica the especially compared to the cost of organic osm- broad salinity tolerance is also assisted by the olyte biosynthesis or degradation (Kirst 1990). thickness and mechanical properties of the cell However, protein and organelle function, enzyme walls (Jacob et al. 1992a). Another ultrastructual activity and membrane integrity in seaweeds are feature of Prasiola cells is the absence of vacuoles adversely affected by increased electrolyte con- under hypososmotic conditions up to full seawa- centration. Hence, the biosynthesis and accumu- ter and the formation of vacuoles at high salini- lation of organic osmolytes in the cytoplasm ties. Under the latter conditions, they may serve permits the generation of low water potentials as compartments accumulating inorganic ions. without incurring metabolic damage. For these Compared to the eulittoral Chlorophyta, much organic compounds that are tolerated by less is known of the ecophysiology of the the metabolism even at high intracellular red algae Bangia atropurpurea and Porphyra concentrations, the term ‘compatible solute’ was endiviifolium from Antarctica. The few data on introduced by Brown and Simpson (1972). temperature requirements for growth and
123 Rev Environ Sci Biotechnol survival indicate eurythermal characteristics for are chronic photoinhibition/photoinactivation, both Rhodophyta, i.e. they survive temperatures bleaching of photosynthetic pigments, peroxida- up to 21–22 C (Bischoff-Ba¨smann and Wiencke tion of membrane lipids and enhanced degrada- 1996). Studies on closely related species of both tion of D1 protein (Aro et al. 1993; Osmond genera from other biogeographic regions clearly 1994). Hitherto this phenomenon is hardly stud- indicate an extremely broad tolerance of all ied in Antarctic macroalgae (Hanelt et al. 1994, environmental factors, which is based on a high 1997). However, the limited information available metabolic flexibility (Karsten et al. 1993; Karsten suggests that polar algae from the eulittoral, such and West 2000). Bangia and Porphyra synthesize as the brown alga Adenocystis utricularis, may and accumulate three isomeric heterosides with overcome radiation stress at low temperatures by different physiological functions as osmolytes, their ability for dynamic photoinhibition/photo- compatible solutes and soluble carbon reserve. protection (Osmond 1994), which proceeds much Besides hypersaline conditions decreasing faster than in sublittoral algae (Hanelt et al. 1994, temperatures also strongly stimulate the biosyn- 1997). The rate of inhibition seems to be inde- thesis and accumulation of DMSP in Antarctic pendent of temperature. The underlying mecha- Chlorophyta (Karsten et al. 1996a). In addition, nism is still unexplored, but possible explanations DMSP not only stabilises the cold-labile model include the adaptation of enzymes involved in the enzyme lactate dehydrogenase and malate dehy- D1 repair cycle at low temperatures, and the drogenase extracted from Acrosiphonia arcta insignificant role of D1 in photoinhibition and during several freezing and thawing cycles, but recovery of photosynthesis in Antarctic macroal- also stimulates both enzyme activities at in situ gae (Hanelt et al. 1994). The ability for fast concentrations. Consequently, DMSP acts as an photoinhibition and to completely halt photo- effective cryoprotectant (Nishiguchi and Somero synthesis under steadily decreasing temperatures 1992). Recent studies on Antarctic Prasiola and at constant irradiance levels was also found in sea ice diatoms indicate the presence of ice-bind- eulittoral Fucus distichus from Arctic Spitsbergen ing proteins (IBP) that modify the shape of (Bischof and Walter, unpublished data). Here, a growing intracellular ice crystals during freezing critical temperature level to initiate pronounced (Raymond and Fritsen 2001). IBPs do not lower photoinhibition was found to be –3 C. As soon as the freezing point, they rather seem to prevent temperatures fall below this threshold, photo- damage to membranes by the inhibition of the synthesis becomes rapidly inhibited, and photo- recrystallization of ice (Raymond and Knight synthetic quantum yield completely ceases at 2003). During recrystallization small ice particles –15 C. Recovery from freezing temperature pro- typically grow to large grains of ice, which may ceeds almost in reverse, with a rapid increase in physically injure cell membranes. Consequently, quantum yield as soon as temperatures climb IBPs act as effective structural cryoprotectants. above –3 C. By their ability to reduce photosyn- In the eulittoral and supralittoral zone, low thetic quantum yield, polar eulittoral algae seem temperatures combined with high irradiance to be able to avoid increasing oxidative stress represent a particular challenge to algal physiol- under low temperature conditions. However, ogy. At low temperature, and, thus, reduced en- some species seem to apply other strategies of zyme activities and decreased turn-over velocity photoprotection under low temperature, since of D1 reaction centre protein in photosystem II Becker (1982) reported for Antarctic Prasiola (Davison 1991; Andersson et al. 1992; Aro et al. photosynthetic activity down to –15 C. The 1993), a persisting high irradiance of PAR capacity to photosynthesize as efficiently in air may result in increased electron pressure in pho- (when hydrated) as in water, in combination with tosynthesis. This may ultimately result in the a high affinity for inorganic carbon, has been generation of reactive oxygen species within the described for a temperate species of this genus Mehler reaction (Polle 1996) and increase (Raven and Johnston 1991). oxidative stress (Asada and Takahashi 1987). Desiccation is a strong stress parameter in The consequences of increased oxidative stress supralittoral species. Air exposed thalli of
123 Rev Environ Sci Biotechnol
Prasiola crispa loose 75% of the cellular water perennial sporophytes and a reduction of the during the first 6 h of desiccation (Jacob et al. gametophyte generation (Clayton 1988). The 1992b). A water loss of more than 90% leads to ultimate step in this evolutionary trend is irreversible damage. Growth rates after reim- observed in members of the Fucales and Asco- mersion in seawater depend on the thallus water seirales, which lack free-living gametophytes. In content and the length of the desiccation period. Laminariales and Desmarestiales, free-living Few ultrastructural changes were found after gametophytes are still present; however, they are desiccation. As after salinity stress, the very thick morphologically inconspicuous, generally con- cell walls of the species and the absence of vac- sisting of microscopic filaments and they are uoles are regarded as prerequisites to survive important mainly in sexual reproduction. It has periods of desiccation (Jacob et al. 1992b). been suggested that the dissimilar reproductive Although there is a lack of knowledge of the phase expression in large kelps may be primarily ecophysiological performance of many eulittoral associated with a differential response to wave macroalgae from Antarctica, the known data action (Neushul 1972), herbivory (Slocum 1980; clearly indicate broad tolerances against the pre- Lubchenco and Cubit 1980; Dethier 1981) or vailing environmental, often extreme parameters. physical factors such as temperature and light In particular, the biochemical capability to syn- (Kain 1964; Lu¨ ning and Neushul 1978; Lu¨ ning thesize and accumulate various protective com- 1980b; Fain and Murray 1982; Novaczek 1984; pounds seems to be the main prerequisite for tom Dieck 1993). Early developmental stages of long-term survival. seaweeds (zoospores, gametophytes and small The response of polar seaweeds to inorganic sporophytes) are shade-adapted organisms unlike and organic pollutants has only randomly been the adult sporophytes (Kain 1964; Amsler and investigated so far. Especially brown algae take up Neushul 1991; Go´ mez and Wiencke 1996a; Dring the radionuclide contaminant 99Tc very strongly et al. 1996). The different physiological perfor- (Topcuoglu and Fowler 1984; Gwynn et al. 2004). mance of the heteromorphic phases has implica- The uptake mechanisms and the actual effect of tions for algal ecology: reproduction, metabolic 99Tc are, however, not yet investigated. With re- performance (e.g. photosynthesis) and growth are spect to the oil spill of the Bahia Paraiso near seasonally synchronized improving survival under Anvers Island, Antarctic Peninsula (Kennicutt II changing environmental conditions (Lu¨ ning et al. 1990), there were no observable differences 1990). Thus, light adaptation is an important between oiled and non-oiled sites with respect to functional character connecting the different the percentage cover of either sublittoral macro- stages of life in these species. algal overstory or crustose coralline algae (Amsler In Antarctic Desmarestiales reproduction and et al. 1990). Similarly, Dunton et al. (1990) could further development of gametophytes and not determine significant effects on photosynthe- sporophytes are governed by the photoperiod. sis in Porphyra endiviifolium and Palmaria deci- Culture studies carried out on all members of the piens. On the other hand, Stockton (1990) Antarctic Desmarestiales indicate that life history reported that the principal intertidal alga, Uros- depends strongly on the seasonal variation of pora sp. turned brown soon after the spill. The daylengths. In general, the development of gam- degree of damage certainly depends on the etangia, fertilization (oogamy) and the formation amount and type of material released. of the early stages of sporophytes take place in winter in all Antarctic species of Desmarestiales, whereas growth of sporophytes begins with Seasonality of reproduction and the physiological increasing daylengths in late winter-spring. In characteristics of microscopic developmental Himantothallus grandifolius, Desmarestia anceps stages and D. menziesii, gametophytes become fertile under short day conditions only (Wiencke 1990a; The heteromorphic life history of large brown Wiencke and Clayton 1990; Wiencke et al. 1995, algae is characterized by the development of 1996). In D. antarctica and Phaeurus antarcticus
123 Rev Environ Sci Biotechnol gametogenesis occurs both in short and long days. development between the different stages ac- In these species seasonality is controlled by the count for the light harvesting efficiency at low sporophytic stage. Sporophytes become fertile in irradiance (Ramus 1981). In filamentous or thin culture at daylengths between 6 h and 8 h light sheet-like thalli, pigment-based photosynthesis per day and the developing gametophytes formed follows a linear curve, whereas in thick morphs, gametangia soon after germination (Clayton and characterized by several cell layers and low ratios Wiencke 1990; Wiencke 1990a; Wiencke et al. of photosynthetic to non-photosynthetic tissues, 1991). Similarly, in the Arctic kelp, Laminaria photosynthesis becomes uncoupled from the pig- solidungula, sori are produced in winter ment content due to a greater self-shading (November) just before the growth of the lamina (Ramus 1978). begins, but spore release does not occur until the In general, early life stages have higher dark following spring (Hooper 1984). Gametophytes respiration rates than adult ones, with conse- become fertile in this species under short day quences for light compensation points (Ec). conditions only, not under long days and short Because of their high respiration rates, Ec in ga- days combined with a night-break regime (Bartsch, metophytes and small sporophytes are not signif- pers. comm.). Irradiance levels < 5 lmol m–2 s–1 icantly lower than in adult sporophytes, whereas are necessary to induce gametogenesis and fer- the photon fluence rate required for saturation tilization in Antarctic Desmarestiales (Wiencke (Ek) is considerably higher in adult sporophytes 1990a; Wiencke and Clayton 1990; Wiencke et al. due to lower a values. Photosynthesis in adult 1995, 1996). The upper temperature limit for sporophytes is saturated at significantly higher ir- gametogenesis is 5 CinD. antarctica (Wiencke radiances (30 lmol m–2 s–1) than in gametophytes et al. 1991), a feature probably common in or juvenile sporophytes (16 lmol m–2 s–1). De- Desmarestiales from Antarctica. spite their very high respiratory activities sporo- Interestingly, all of the Antarctic Desmaresti- phytes and gametophytes from several Antarctic ales studied to date show in situ fertilization, i. e. Desmarestiales show light saturation of growth at the juvenile sporophytes remain attached to the irradiances close to 10 lmol m–2 s–1 (Wiencke gametophytes (Wiencke et al. 1995, 1996). This 1990a; Wiencke and Fischer 1990) indicating that adds new evidence for the importance of the growth is not constrained by such low irradiances gametophytic generation on the early stages of (Go´ mez and Wiencke 1996b). the large sporophytes. In terms of ecological The capacity of gametophytes and small significance, one may speculate that the recruit- sporophytes to grow and photosynthesize under ment of sporophytes and consequently the ob- low light conditions may be regarded as adaptive served dominance of these species may be and allows the algae to survive under the sea- conditioned by the survival (or mortality) of the sonally changing light environment in polar re- gametophytes. gions. During winter, when incident irradiance is The development of gametophytes or at least low and daylength is short, high photosynthetic their reproductive capacity appears to be con- rates and growth of gametophytes and juvenile strained by high light conditions suggesting that sporophytes are favoured in virtue of their higher the fitness associated with the winter develop- surface-area/volume ratio, higher pigment ment of gametophytes lies partly in a differenti- content and more efficient light use. ation of light requirements for photosynthesis. For example, in Desmarestia menziesii early stages of sporophytes and gametophytes are bet- Seasonal growth and photosynthesis ter suited to live under low light conditions than adult sporophytes: photosynthetic efficiency (a) In polar regions, seasons are characterized by measured in these phases is five times higher than short periods of favourable light conditions and in adult sporophytes (Go´mez and Wiencke 1996a). extended periods of darkness due to polar nights The differences in pigment allocation, cross and sea ice covering during winter (see chapter 2). section pathlength of radiation and general The seasonal development of macroalgae is
123 Rev Environ Sci Biotechnol generally triggered by light, temperature and/or Antarctic-cold temperate species, are season nutrient conditions (Chapman and Craigie 1977; responders sensu Kain (1989). Species in this Lu¨ ning 1980a; Lu¨ ning and tom Dieck 1989). As group start growth later coinciding with favour- temperatures and nutrient levels show only a able light conditions in spring and summer. They small variation over the year in Antarctic waters react directly to changing environmental condi- (see chapter 2), seasonality of Antarctic seaweeds tions and show an opportunistic life strategy. To depends mainly on variable light conditions and, this group belong the brown alga Adenocystis especially, daylengths. Thus, assessment of the utricularis (Wiencke 1990a), the red algae Iridaea seasonal development of Antarctic species in cordata (Weykam et al. 1997) and Gigartina long-term culture experiments is possible simply skottsbergii (Wiencke 1990b), and the green algae by mimicking the seasonally fluctuating day- Enteromorpha bulbosa and Acrosiphonia arcta lengths at the collecting site (Wiencke 1990a, b). (Wiencke 1990b). Seasonality of growth and photosynthesis as well As for growth, a strong seasonal pattern of as seasonal formation of gametes/spores can be photosynthetic performance was found in long- monitored much more closely than possible in the term culture studies (Weykam and Wiencke 1996; field. The results of these studies complement the Weykam et al. 1997; Go´ mez and Wiencke 1997; available fragmentary field observations and Lu¨ der et al. 2001a, 2002,2003) and in field indicate that the phenology of Antarctic macro- experiments (Gutkowski and Maleszewski 1989; algae can be controlled in the laboratory. Data on Drew and Hastings 1992; Go´ mez et al. 1995b, Arctic species are so far based on field studies 1997). In the brown algal season anticipators only. optimal photosynthetic rates are highest in late Antarctic seaweeds follow two different winter (September) for A. mirabilis (Go´ mez et al. growth strategies in order to cope with the strong 1995b) or in spring (November) for Himanto- seasonality of the light regime (Wiencke 1990a, b; thallus grandifolius (Drew and Hastings 1992) and Dummermuth and Wiencke 2003). One group, D. menziesii (Go´ mez et al. 1997). In these spe- mainly endemics, begins to grow under short day cies, morpho-functional processes strongly regu- conditions in late winter-spring, even under sea late photosynthetic seasonality: In spring ice, and reaches maximal growth in spring. Some respiration rates increase in all thallus parts, species even reproduce in winter. This group has indicating growth activity in the basal meristem been classified as season anticipators sensu Kain powered by remobilization of carbohydrates from (1989). In these species annual growth and the distal thallus part (Go´ mez et al. 1995b) as in reproduction is most probably based on photo- Laminaria species (Lu¨ ning et al. 1973; Schmitz periodism and circannual rhythms, triggered or 1981). This is supported by the decrease of the synchronized by daylength as shown for species storage carbohydrate laminaran in late winter and from other phytogeographic regions (Lu¨ ning and spring in A. mirabilis (Go´ mez and Wiencke 1998). tom Dieck 1989; tom Dieck 1991; Lu¨ ning and The low molecular weight compound, mannitol, is Kadel 1993; Schaffelke and Lu¨ ning 1994). To this presumably used as substrate for respiration group belong the brown algae Desmarestia men- during the period of active growth. This is ziesii, D. antarctica, D. anceps, Himantothallus reflected by its low levels during the main growth grandifolius, Phaeurus antarcticus, Ascoseira period. In late summer, the mannitol content in- mirabilis (Wiencke 1990a; Drew and Hastings creases significantly in the basal and middle 1992; Go´ mez et al. 1995a, 1996b; Go´ mez and region. In the distal region it may serve as sub- Wiencke 1997) and the red algae Palmaria deci- strate for light independent carbon fixation or is piens, Delesseria salicifolia, Gymnogongrus ant- stored as laminaran which attains its highest arcticus, G. turquetii, Hymenocladiopsis content in the distal thallus part (Go´ mez and crustigena, Kallymenia antarctica, Phyllophora Wiencke 1998). Similar results have been ob- ahnfeltioides (Gain 1912; Wiencke 1990b; Wey- tained in D. menziesii (Go´ mez and Wiencke 1997; kam et al. 1997; Dummermuth and Wiencke Go´ mez et al. 1998). In contrast, the season re- 2003). The second group, mainly composed of sponder Adenocystis utricularis (Gutkowski and
123 Rev Environ Sci Biotechnol
Maleszewski 1989) features lowest photosynthetic Antarctic season anticipator P. decipiens are low capacity in spring and highest in autumn (no data or even negative during darkness but increase in summer available). strongly after re-illumination with maximal In red algae, seasonality has been studied in growth in early spring. The content of floridean particular with respect to the acclimation of light starch decreases gradually in the dark and drops harvesting capacities. The light requirements for suddenly powering the formation of new blades in growth and photosynthesis of the Antarctic sea- winter (early August) after 6 months exposure to son anticipator Palmaria decipiens and in the darkness (Weykam et al. 1997). This feature Antarctic season responder Iridaea cordata are supports the theory that seasonal growth is con- very low (Wiencke 1990b; Wiencke et al. 1993; trolled in season anticipators either by photo- Weykam et al. 1997). P. decipiens develops new periodism or cirannual rhythms. In contrast, the blades during Antarctic late winter/spring (Wie- Antarctic season responder Iridaea cordata ncke 1990b) and starts growth in Antarctic winter develops no blades during darkness and starts (July) with optimum in spring (Wiencke 1990b). growth more slowly after re-illumination with
The photosynthetic capacity (Pmax and ETRmax) maximal growth rates in late spring. and photosynthetic efficiency (a and Fv/Fm) are, Photosynthetic capacity and efficiency in as growth, maximal in Antarctic spring (Weykam P. decipiens is almost unaffected by 2 months in and Wiencke 1996; Lu¨ der et al. 2001a). A strong darkness albeit an initial increase in pigments relationship between the seasonal patterns of (Weykam et al. 1997; Lu¨ der et al. 2002; Lu¨ der photosynthesis and pigment contents has been 2003). After 4 months in darkness the light har- demonstrated in P. decipiens (Lu¨ der et al. 2001a). vesting antennae, the phycobilisomes, are de- Photosynthetic capacity and pigment contents graded. One of the two forms of phycobilisomes increase in parallel continuously during the entire in P. decipiens disappears (Lu¨ der 2003). This is mid autumn, winter and spring. There is a positive followed later by a degradation of the chl a-con- correlation between phycobiliproteins and pho- taining inner antennae (Lu¨ der et al. 2002). At the tosynthetic capacity, but a weaker correlation end of the 6 months dark period, P. decipiens has between Chl a and photosynthetic capacity. lost its ability to photosynthesize (Lu¨ der et al. Phycobiliproteins are used to increase number 2002; Weykam et al. 1997). After re-exposure to and size of phycobilisomes, the main light har- light, pigments are synthesized rapidly and en- vesting antennae of red algae (Lu¨ der 2003). hance photosynthetic performance to normal Photosynthetic efficiency is optimal in autumn, values within a week (Lu¨ der et al. 2002). The winter and spring. During Antarctic summer, P. season responder I. cordata, in contrast, maintains decipiens reduces its photosynthetic apparatus to its photosynthetic apparatus functional during a minimum: Photosynthetic efficiency, photosyn- exposure to darkness (Weykam et al. 1997). This thetic capacity, and the contents of phycobili- species is therefore better able to grow in regions proteins and Chl a tissue are low (Lu¨ der et al. with less predictable light conditions. 2001a). The existence of two phycobilisome forms In contrast to the Antarctic there is a great with different aggregation states in P. decipiens seasonal variation in the Arctic not only with might be considered as an advantage for a rapid respect to daylength but also with respect to the acclimation to changes in environmental light macronutrient levels, which are high in winter and conditions (Lu¨ der et al. 2001b). Studies on sea- low in summer (see chapter 2). Nevertheless, the sonal assembly of the light harvesting antennae in seasonal growth of the few seaweeds from the P. decipiens have shown that both phycobilisome Arctic studied so far is triggered primarily by forms are extremely variable in size and number daylength and is supported by high nutrient levels during the entire year (Lu¨ der 2003). in winter, as discussed below. The Arctic kelp The effect of darkness on the seasonal growth Laminaria solidungula and the Arctic-cold tem- pattern in two Antarctic red macroalgae has been perate L. saccharina are clear season anticipators. examined in long-term culture experiments by In L. solidungula new blade formation is initiated Weykam et al. (1997). Growth rates in the in autumn under conditions of decreasing
123 Rev Environ Sci Biotechnol daylengths. Maximal growth rates occur in late- of inorganic-N were important cues that led to winter to early spring under thick ice and decline both sorus formation (Lu¨ ning, 1988) and new in summer and autumn in the ice-free period blade formation in several species of kelp (Lu¨ ning (Chapman and Lindley 1980; Dunton 1985). In and tom Dieck 1989). But of all these cues, the Alaskan Beaufort Sea, L. solidungula fronds elaborate experimental studies demonstrated that continue to grow under a turbid ice canopy that daylength was most important in the setting of produces conditions of nearly complete darkness, internal clocks in species that possess circannual even under continuous daylight (Dunton 1990). rhythms which control the periodicity in linear In comparison, L. saccharina appears to delay growth (Lu¨ ning 1991; Lu¨ ning and Kadel 1993). nearly all of its annual growth to a brief period in late spring when light first starts to penetrate the water column during sea ice break-up (Dunton Elemental and nutritional contents 1985). The energy required to survive darkness and to The most commonly used indicator of nutrient start blade formation in winter is provided by limitation in marine algae is the carbon to nitro- mobilization of stored carbon reserves, accumu- gen ratio (C:N), with low values indicative of lated during the previous summer, when inorganic nitrogen replete growth conditions. To date, C:N nitrogen becomes available similar as in L. longi- data have been reported from 54 species of cruris (Hatcher et al. 1977; Gagne et al. 1982; macroalgae in Antarctica including 8 species of Chapman and Craigie 1978; Dunton and Dayton green algae, 36 species of red algae, and 10 spe- 1995). In L. solidungula, mobilization of these re- cies of brown algae (Dhargalkar et al. 1987; serves occurs during the dark 9-month ice covered Weykam et al. 1996; Dunton 2001; Peters et al. period, when the plant completes over 90% of its 2005). Reported C:N ratios (on a weight:weight annual linear growth, and results in a carbon deficit basis) range from a minimum of 5.0 to a maxi- where up to 30% of its original total carbon content mum of 23.6 with an overall mean of 10.2, indi- is depleted before photosynthetic production be- cating that most if not all of the macroalgal gins in early summer (Dunton and Schell 1986). species are not nitrogen limited (Peters et al. During the summer open-water period (July to 2005). Likewise, tissue nitrogen levels are rela- October), when the concentration of inorganic-N is tively high and almost always above the 1.5% nearly undetectable in coastal waters, high rates of level thought to be indicative of nitrogen replete photosynthetic carbon fixation result in carbon growth conditions (Rakusa-Suszczewski and storage and not in blade elongation in L. solidun- Zielinski 1993; Weykam et al. 1996; Peters et al. gula (Dunton and Schell 1986). 2005). Generally, C:N values are much lower than The utilization of stored photosynthate for most reported outside of Antarctica (a mean C:N growth was first reported by Lu¨ ning (1971), who value for temperate and tropical marine plants is found that Laminaria hyperborea in northern approximately 19; Atkinson and Smith 1983) and Europe accumulated reserves during its period of presumably result from the high nitrate concen- slow growth in summer to support the formation trations present in coastal Antarctic waters and growth of a new blade the following spring. throughout the year (Weykam et al. 1996; Peters Subsequent work by Lu¨ ning (1979) on three et al. 2005), although morpho-functional pro- Laminaria species in the North Sea confirmed the cesses such as storage and remobilization of C importance of these reserves in L. hyperborea, and N in response to growth requirements are but he also suggested that a circannual rhythm also important (Go´ mez and Wiencke 1998). was involved in the regulation of seasonal growth Along the Antarctic Peninsula, there is a slight since no one particular factor appeared respon- trend for somewhat lower C:N values at King sible for triggering the onset of new growth. George Island (62 14¢ S, 58 40¢ W) compared to Lu¨ ning’s hypothesis was later proved correct; the Anvers Island (64 46¢ S, 64 03¢ W), suggesting a onset of short daylengths in autumn, combined possibility of minor geographically based varia- with lower temperatures and normally low levels tion, but there was no apparent variation between
123 Rev Environ Sci Biotechnol early and late growing seasons (Weykam et al. reported that there was no significant correlation 1996; Dunton 2001; Peters et al. 2005). between protein and nitrogen contents across all We are aware of only one published report of 40 species they examined, brown algae alone, or C:N ratios or nitrogen contents in macroalgae red algae late in the growing season but that there from the Arctic. Henley and Dunton (1995) was a significant, positive correlation for red algae reported on seasonal and within-thallus variation early in the growing season. In a more detailed in the kelps Laminaria solidungula and L. sac- study focused on the endemic brown alga As- charina from the Alaskan Arctic. C:N ratios were coseira mirabilis,Go´ mez and Wiencke (1998) relatively low (approximately 11.6–13.5, con- reported a significant, positive correlation be- verted from atom:atom to weight:weight basis) tween protein and nitrogen content in the distal and tissue nitrogen levels relatively high portion of the thallus but not in middle or basal (1.9–3.0%) in second year blades of both species portions. The general lack of correlation between regardless of season. In first year blades, however, protein and nitrogen content indicates that pro- C:N ratios increased significantly from early to tein production is not constrained by nitrogen late growing seasons in both species (from approx. availability and is probably another reflection of 9.4 to 18.3 in L. solidungula and 9.8 to 24.8 in L. the high nutrient environment present in coastal saccharina). This correlated with significant de- antarctic waters. This general lack of correlation creases in tissue nitrogen (Henley and Dunton also indicates that older methods which estimate 1995) but laboratory studies suggest important protein concentrations in macroalgae based on roles for both light and nitrogen availability in nitrogen contents are less appropriate for use with driving these patterns (Henley and Dunton 1997). Antarctic macroalgae. Macroalgae are a potentially important nutri- tional source for a variety of Antarctic animals (Iken et al. 1998; Dunton 2001) and macroalgal Chemical and physical defences against herbivory nutritional parameters, particularly protein con- and fouling tent, can be important determinants of palatabil- ity to consumers (e.g., Horn and Neighbors 1984; Defence mechanisms against grazing pressure, Duffy and Paul 1992; Bolser and Hay 1996). Al- and fouling organisms, including bacteria and though we are unaware of any published reports pathogens can be critical to the success and sur- of protein or other nutritional parameters in vival of polar seaweeds. Seaweeds constitute a macroalgae from the Arctic, protein and other potential food and carbon source for many kinds nutritional content data are available from 44 of heterotrophic organisms, e.g. amphipods, species of Antarctic macroalgae including 7 spe- gastropods, sea urchins or fishes. Tropical and cies of green algae, 28 species of red algae, and 9 temperate algal species often display physical species of brown algae (Czerpak et al. 1981; defensive mechanisms such as structural tough- Dhargalkar et al. 1987; Rakusa-Suszczewski and ness, physiological defensive mechanisms such as Zielinski 1993; Go´ mez and Westermeier 1995; low nutritional content (see chapter 10 of this Go´ mez and Wiencke 1998; Peters et al. 2005). review) or chemical defensive mechanisms such Protein levels are usually considerably higher as a high content or an induction of allelopathic when compared to temperate or tropical macro- chemicals. Allelopathy refers to the usually det- algae in which protein contents were determined rimental effects that seaweeds have on other with similar methodology (Peters et al. 2005) interacting organisms through the production of although this is not always true (Go´ mez and secondary metabolites. Westermeier 1995). By itself, this would suggest The incidence of herbivory in Arctic as well as that Antarctic macroalgae should be relatively Antarctic shallow water systems is low but several palatable to consumers and the fact that this is not organisms depend fully or in part on seaweeds as so for a majority of species (Amsler et al. 2005a, a food source in the Antarctic (Brand 1974; b) is probably related to chemical defenses as Richardson 1977; Iken et al. 1997, 1999; Iken described in chapter 11. Peters et al. (2005) 1999; Dunton 2001; Graeve et al. 2001) and the
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Arctic (Lippert et al. 2001; Wessels et al. 2006; optimal defence theory (Rhoades 1979), which Dunton and Schell 1987). A comprehensive assumes that defences are costly and therefore investigation of palatability in 35 fleshy seaweeds should be allocated to the most valuable and from the Antarctic Peninsula (Anvers Island) vulnerable tissue types. against a sympatric (occurring within the same A recent study of palatability using 19 abun- geographical region) fish and sea star algal con- dant macroalgal species from Spitsbergen (Arc- sumer showed that about 60% and 80%, respec- tic) showed that most species were at least tively, of the algae were unpalatable (Amsler moderately palatable to a sympatric amphipod et al. 2005a). These included all dominant over- and sea urchin (Wessels et al. 2006). Consump- story brown algae and a variety of abundant red tion by both herbivores differed among algal algal species of the region. Unpalatable algal species and preference patterns for algae differed species were extracted and the palatability of or- for both herbivores, indicating species-specific ganic extracts was tested after incorporation into preference patterns. Tissue-specific palatability of artificial foods (Amsler et al. 2005a). Again, the stipe and blade tissues of the kelp species differed majority of species were unpalatable as at least for both herbivores with no preference in sea one extract type to the fish, sea star and an urchins and a preference for Laminaria blades amphipod consumer. No overall correlation in and Alaria stipes in the amphipod (Wessels et al. feeding patterns could be established with tissue 2006). Although not explicitly discussed by the toughness or nutritional content of the algae authors, higher defences in kelp stipes compared (Amsler et al. 2005a; Peters et al. 2005) although to blades could be explained by resource alloca- toughness could play a role in the unpalatability tion considerations as mentioned above for Ant- of some particular macroalgal species to amphi- arctic brown algae. Generally, however, and in pods (Huang et al. 2006). contrast to the findings for Antarctic seaweeds, Only two fleshy red macroalgae, Iridaea cor- unpalatability in Arctic seaweeds seems to be data and Phyllophora antarctica, occur in more related to structural than chemical proper- McMurdo Sound, the southernmost location of ties of the algae (Wessels et al. 2006). Only one open ocean conditions (Miller and Pearse 1991). red algal species, Ptilota gunneri, showed indica- Thallus fragments and paper disks laced with or- tions of being chemically defended against the ganic extracts of these species were tested in a two grazers. phagostimulation assay where the retention time In addition to deterring grazers, organic ex- of a test or control food was measured over the tracts of all Antarctic macroalgal species tested mouth of the sympatric sea urchin, Sterechinus (2 from McMurdo, 22 from Anvers Island) also neumayeri. Algal treatments were retained for were toxic to sympatric diatoms (Amsler et al. significantly shorter times compared to controls 2005b). To the best of our knowledge, no com- (blank paper disks and disks with a feeding parable information is available on antifouling stimulant), indicating the presence of deterrent properties in Arctic seaweeds. chemicals in both red algal species (Amsler et al. Little is known about the particular com- 1998). pounds that may be active in chemical defence Along the Antarctic Peninsula, within-thallus against herbivores and epiphytes in either of the variation of chemical and physical defences was two polar regions. Phlorotannins are a class of tested for the ecologically important brown polyphenolic compounds found exclusively in macroalgae Desmarestia anceps and D. menziesii brown algae. Their ecological functions, espe- (Fairhead et al. 2005a). This study found that cially as anti-herbivore agents for temperate and overall chemical defences are prevalent, but some tropical species have frequently been discussed tissue types depend more on physical than (Targett and Arnold 2001; Amsler and Fairhead chemical protection, such as holdfasts. In the 2006). Phlorotannins were shown to be present in highly differentiated D. anceps, high allocation of Antarctic brown algae (Iken 1996; Iken et al. chemical and physical defences to holdfast and 2001; Fairhead et al. 2005b), but their ecological stipe tissue was consistent with predictions of significance remains ambiguous (Iken et al. 2001;
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Iken unpubl. data). Microscopic studies in the Hoyer et al. 2001; Aguilera et al. 2002). For de- Arctic brown seaweed, Laminaria solidungula, tailed review on MAAs in polar seaweeds see have shown that phlorotannins play an important Bischof et al. in press. role in wound healing (Lu¨ der unpubl. data) as in the temperate Australasian Ecklonia radiata (Lu¨ der and Clayton 2004). An induction of Future perspectives phlorotannin production in the cells of the wound area was evident after mechanical wounding Although considerable progress has been simulating a grazer attack. Phlorotannins at the achieved in recent years, our present knowledge wound area probably deter bacteria or other mi- of seaweeds from polar regions is still fragmen- crobes and may prevent the algae from being tary. Due to the extreme remoteness of the polar eaten further. In addition, phlorotannins bound in regions and the infrequency of scientific studies cell walls (Schoenwaelder 2002) may form a bar- even the basic features of the polar seaweed floras rier for grazers or fouling organisms in L. such as the numbers of recorded species are not solidungula (Lu¨ der unpubl. data). firmly established. More studies are therefore A variety of other secondary metabolites such needed to precisely document the biodiversity of as terpenes, furanones and acetogenins have been Arctic and Antarctic seaweeds. If such studies are isolated and structurally resolved in Antarctic combined with molecular investigations it should seaweeds (esp. red algae, for review see Amsler be possible to demonstrate, for example, the et al. 2001; Ankisetty et al. 2004), although the presence of gene flow between populations of the ecological significance of most of these com- same species in the Antarctic/Arctic and the pounds in grazer or fouler deterrence remains to adjacent cold-temperate regions. Alternatively, be established. Chemical screening of organic where gene flow is absent, divergence times be- extracts of Antarctic seaweeds revealed that no tween the populations can be estimated. chemicals containing nitrogen are present (Ams- Furthermore, molecular studies could definitively ler et al. 2005a) even though it had been demonstrate seaweed dispersal routes and give a hypothesized that the nitrogen-replete conditions much clearer pattern of the biogeographic rela- in Antarctic coastal waters should promote the tionships between the polar and cold-temperate synthesis of nitrogenous compounds. regions than is presently available. Another group of compounds shown to be More culture studies are necessary especially present in Arctic and Antarctic seaweeds are on seaweeds from the Arctic. None of the truly volatile halogenated organic compounds endemic Arctic species is in culture today and no (VHOC) (Laturnus 1996, 2001; Laturnus et al. data are available on the ecophysiological prop- 1996). These compounds are released continu- erties of these species. In this context it would be ously in substantial amounts by Arctic brown very interesting to know whether the relatively algae, while red algae release only trace amounts. short cold water history of the Arctic could have The deterrent effect of VHOC on grazers is often promoted the evolution of species with tempera- assumed but so far has been detected only at ture demands as low as in the Antarctic region. exceptionally high and probably ecologically Further, culture studies have been proven to give irrelevant concentrations (Amsler and Fairhead pertinent insights into the life strategies of polar 2006). seaweeds not only with respect to the tempera- Chemical defences in polar seaweeds may also ture requirements and geographic distribution but be employed for protection against deleterious also with respect to the light requirements and environmental conditions. In polar regions, UVB depth zonation. Even the phenology of seaweeds radiation due to the thinning ozone layer can be could be monitored in culture studies under sim- particularly harmful. Red algae from both polar ulated polar light conditions. regions have been shown to produce mycospo- Such studies should ideally be combined with rine-like amino acids (MAA) as photoprotective field experiments. Data on the underwater radi- substances (e.g., McClintock and Karentz 1997; ation regime would allow an estimate of benthic
123 Rev Environ Sci Biotechnol primary production in different water depths extended to obtain a more comprehensive through the determination of the metabolic car- understanding of their importance in seaweeds on bon balance. Apart from studies with the Arctic an ocean-wide basis. Few compounds have been Laminaria solidungula, the physiological perfor- identified so far as being active in chemical de- mance of seaweeds in winter is obscure. Only fence. Detailed knowledge will allow better baseline field studies are available together with a comparisons with what is known from temperate few papers based on laboratory studies. Repro- and tropical systems. A question of interest con- duction, growth and photosynthetic rates, the cerning seaweeds from all regions is whether content of pigments and cryoprotective sub- chemical defenses are constitutive, i.e. consis- stances, the elemental and nutritional composi- tently present in the alga, or induced by the attack tion as well as enzyme activities must be of herbivores? This may be particularly useful for monitored over the entire year to understand the answering the question of the yet unsolved roles life strategy of these species in more detail. of phlorotannins in brown algae: constitutive With respect to elemental and nutritional levels did not show clear patterns in herbivore content the major questions are, first, whether the deterrence, but microscopic studies show that greater availability of nitrogen in Antarctic wa- wounding can lead to high local accumulation of ters and the apparent uncoupling of nitrogen phlorotannins. Whether this has broader impact availability and protein content alter our under- needs to be addressed. standing about resource allocation in seaweeds The ecophysiology of supra- and eulittoral that come from studies in other systems. Sec- species needs to be investigated in more detail in ondly, if the higher overall protein concentrations field studies. To survive in the intertidal zone, in Antarctic macroalgae indeed makes them more algae need to protect their metabolism and par- nutritious to herbivores compared to algae from ticularly their photosynthetic apparatus against other regions (which remains to be experimen- temporary light stress conditions, heat stress, tally tested), does the response of herbivores to cold, freezing and also against pollution. Virtually the (often few) palatable Antarctic seaweeds alter nothing is known about protective mechanisms in ideas about herbivore feeding ecology that are polar seaweeds. Therefore, a detailed analysis of based on lower latitude systems? In this respect such mechanisms ensuring homeostasis and the functioning of the internal long distance functional integrity of the photosynthetic appa- transport system in members of the Desmaresti- ratus in supra-and eulittoral polar seaweeds is ales and Ascoseirales in comparison with mem- necessary. Changes in the expression of photo- bers of the Laminariales is obscure and must be synthetic key proteins (D1, RubisCO, ATP- investigated with respect to the allocation of synthase), and the synthesis of specific protective storage compounds. proteins (Heat Shock Proteins, Chaperonins, The few data available on community ecology Cryoproteins) and protective metabolites (osmo- make further studies in this area very urgent. In lytes, cryoprotectants, antioxidants, sunscreens this respect, the interesting hypothesis that the etc.) in relation to stress exposure should be relative lack of filamentous epiphytic seaweeds in studied in the field, mesocosms and controlled Antarctica could be due to a relatively high level laboratory experiments. So far, gene expression, of mesoherbivory needs to be tested. biosynthetic pathways and metabolic regulation, In this context more studies are needed on for example, are scientific fields almost unex- herbivory and chemical defence of seaweeds. plored in polar seaweeds. In particular, the quest Chemical deterrence should be tested against a for potential cryoproteins represents a novel as- larger set of potential herbivores so that the pect in plant research in general. The results of importance of chemical defence can be inter- such studies will substantially increase the preted on a community-wide scale; this also re- understanding of biochemical adaptation to plant quires a better understanding of herbivore life in extreme environments. abundances and grazing rates. Spatial coverage of All these studies need to be complemented by a chemical defences against herbivores should be detailed monitoring of the environmental
123 Rev Environ Sci Biotechnol conditions especially in the supra-and eulittoral. Ankisetty S, Nandiraju S, Win H, Park YC, Amsler CD, Our knowledge in this area is also still fragmentary. McClintock JB, Baker JA, Diyabalanage TK, Pasari- bu A, Singh MP, Maiese WM, Walsh RD, Zaworotko MJ, Baker BJ (2004) Chemical investigation of Acknowledgements Many results described in this paper predator-deterred macroalgae from the Antarctic would not have been possible without the generous Peninsula. J Nat Prod 67:1295–1302 financial support by the Deutsche Forschungsgemeins- Arnoud PM (1974) Contributions a` la binomie marine chaft, the German Academic Exchange Service, the bentique des re´gions Antarctiques et subantarctiques. European Commission, the Alexander von Humboldt Thethys 6:465–653 Foundation, the Australian Research Council and the US Arnold KE, Manley SL (1985) Carbon allocation in National Science Foundation. 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