Anneke M. Breeman

Effects of temperature on the photoreactivation of ultraviolet-B-induced DNA damage in Palmaria palmata (Rhodophyta)

The accumulation of DNA damage (thymine dimers and 6‐4 photoproducts) induced by ultraviolet‐B radiation was studied in Palmaria palmata (L.) O. Kuntze under different light and temperature conditions, using specific monoclonal antibodies and subsequent chemiluminescent detection. Both types of damage were repaired much faster under ultraviolet‐A radiation (UVAR) plus photosynthetically active radiation (PAR) than in darkness, which indicates photoreactivating activity. At 12° C, all thymine dimers were repaired after 2 h irradiation with UVAR plus PAR, whereas 6‐4 photoproducts were almost completely repaired after 4 h. After 19 h of darkness, almost complete repair of 6‐4 photoproducts was found, and 67% of the thymine dimers were repaired. In a second set of experiments, repair of DNA damage under UVAR plus PAR was compared at three different temperatures (0, 12, and 25° C). Again, thymine dimers were repaired faster than 6‐4 photoproducts at all three temperatures. At 0° C, significant repair of thymine dimers was found but not of 6‐4 photoproducts. Significant repair of both thymine dimers and 6‐4 photoproducts occurred at 12 and 25° C. Optimal repair efficiency was found at 25° C for thymine dimers but at 12° C for 6‐4 photoproducts, which suggests that the two photorepair processes have different temperature characteristics.

Efficient photoreactivation of UVBR-induced DNA damage in the sublittoral macroalga Rhodymenia pseudopalmata (Rhodophyta)

Repair of DNA damage induced by ultraviolet-B radiation (UVBR) was investigated in the sublittoral red alga Rhodymenia pseudopalmata at different temperatures, using immunofluorescent detection of thymine dimers. Photoreactivation of thymine dimers was completed within about 3 h at 6, 12 and 18 °C in the presence of ultraviolet-A radiation (UVAR) and photosynthetically active radiation (PAR) but no repair was found in dark-incubated fragments after 16–17 h. In plants previously exposed to a low UVBR dose (biologically effective dose: BEDDNA300 = 1.6 kJ m−2; unweighted irradiance = 0.72 W m−2 for 4 h), photoreactivation started within the first hour under UVAR + PAR at 18 °C but repair only started after 1–2 h at 12 and 6 °C. At 6 °C, repair was more efficient after exposure to a high UVBR dose (BEDDNA300 = 3.9 kJ m−2; unweighted irradiance = 0.78 W m−2 for 5 h) than to a lower dose (BEDDNA300 = 1.6 kJ m−2); no such difference was found at 18 °C. It is concluded that R. pseudopalmata is able to repair DNA damage induced by high UVBR doses efficiently.

Ultraviolet-B-induced cyclobutane-pyrimidine dimer formation and repair in arctic marine macrophytes

The significance of ultraviolet‐B radiation (UVBR: 280–315 nm)–induced DNA damage as a stress factor for Arctic marine macrophytes was examined in the Kongsfjord (Spitsbergen, 78°55.5′N, 11°56.0′E) in summer. UVBR penetration in the water column was monitored as accumulation of cyclobutane‐pyrimidine dimers (CPD) in bare DNA. This showed that UVBR transparency of the fjord was variable, with 1% depths ranging between 4 and 8 m. In addition, induction and repair kinetics of CPD were studied in several subtidal macrophytes obtained from the Kongsfjord (5–15 m). Surface exposure experiments demonstrated CPD accumulation in Palmaria palmata, Devaleraea ramentacea, Phycodrys rubens, Coccotylus truncatus and Odonthalia dentata. In artificial light, field collected material of P. palmata, D. ramentacea, P. rubens and Laminaria saccharina showed efficient CPD repair, with only 10% of the artificially induced CPD remaining after 5 h. No significant differences in repair rate were observed among these species. CPD repair was slower or absent in O. dentata, C. truncatus and Monostroma arcticum, indicating that fast repair mechanisms such as photolyase were not continuously expressed in these species. CPD repair rates were not directly related to the vertical distribution of algae in the water column and to the reported UV sensitivity of the examined species. Dosimeter incubations showed that maximal exposure to DNA damaging wavelengths was low for all examined species. Furthermore, most species collected below the 1% depth for DNA damage displayed efficient CPD repair, suggesting that UVBR‐induced CPD currently impose a minor threat for mature stages of these species growing in the Kongsfjord, Spitsbergen.

Expected Effects of Changing Seawater Temperatures on the Geographic Distribution of Seaweed Species

Seaweeds are generally kept within their geographic boundaries by limiting effects of temperature. Northern boundaries are set by low lethal winter temperatures, or by summer temperatures too low for growth and/or reproduction. Southern boundaries are set by high lethal summer temperatures, or by winter temperatures too high for induction of a crucial step in the life cycle. Characteristic thermal response types, as identified in laboratory experiments, were found to be responsible for characteristic distribution patterns in the North Atlantic Ocean. Changes in seawater temperature have therefore easily predictable effects on the geographic distribution of seaweed species. Locally, species composition (and community structure) will be altered. Apart from latitudinal displacement and regional extinction, changing seawater temperatures may also cause a shift in selection pressure at a boundary, particularly when summer and winter temperatures change to a different extent. For instance, southern boundaries of several cold temperate brown algae in Europe, which are presently set by ‘winter reproduction’ limits will become ‘summer lethal’ limits following a rise in summer temperatures of only a few degrees. Reconstruction of thermal regimes during glacial and interglacial periods shows that such shifts in selection pressure have probably occurred more often on eastern than on western Atlantic coasts.

Temperature dependence of UV radiation effects in Arctic and temperate isolates of three red macrophytes

The temperature dependence of UV effects was studied for Arctic and temperate isolates of the red macrophytes Palmaria palmata, Coccotylus truncatus and Phycodrys rubens. The effects of daily repeated artificial ultraviolet B and A radiation (UVBR: 280–320 nm, UVAR: 320–400 nm) treatments were examined for all isolates at 6, 12 and 18 °C by measuring growth, optimal quantum yield of PSII (Fv/Fm) and cyclobutane-pyrimidine dimer (CPD) accumulation. Furthermore, possible ecotypic differences in UV sensitivity between Arctic and temperate isolates were evaluated. Large species-specific differences in UV sensitivity were observed for all parameters: the lower subtidal species C. truncatus and P. rubens were highly sensitive to the UV treatments, whereas P. palmata, which predominantly occurs in the upper subtidal zone, was not affected by these treatments. Only minor differences were found between Arctic and temperate isolates, suggesting that no differences in UV sensitivity have evolved in these species. Relative growth rates were temperature-dependent, whereas species-specific UV effects on growth rates were relatively independent of temperature. In contrast, the species-specific decrease in Fv/Fm and its subsequent recovery were temperature-dependent in all species. UV effects on Fv/Fm were lower at 12 and 18 °C compared with 6 °C. In addition, UV effects on Fv/Fm decreased in the course of the experiment at all temperatures, indicating acclimation to the UV treatments. CPDs accumulated during the experiment in both isolates of P. rubens, whereas CPD concentrations remained low for the other two species. CPD accumulation appeared to be independent of temperature. The results suggest that summer temperatures occurring in temperate regions facilitate repair of UV-induced damage and acclimation to UV radiation in these algae compared with Arctic temperatures. Because the differences in UV effects on Fv/Fm, growth and CPD accumulation were relatively small over a broad range of temperatures, it was concluded that the influence of temperature on UV effects is small in these species.

Effects of extreme seasonality on community structure and functional group dynamics of coral reef algae in the southern Red Sea (Eritrea)

Spatial and temporal variation in the biomass of four functional groups of coral reef algae (canopy algae, foliose algae, turf algae and crustose corallines) was investigated in the southern Red Sea. This region is characterised by extremely high summer temperatures (ca. 35°C). Strong seasonal shifts in the relative contribution of each group to the total macroalgal biomass were observed. On the reef flat, canopy and foliose algae dominated in winter, retaining low biomass in summer. On the fore reef, crustose corallines accounted for most of the macroalgal biomass throughout the year. Turf algae contributed least to the total biomass in all reef zones; biomass peaks shifted from midsummer on the inner reef flat to winter in the deeper zones. Biomass correlated negatively with seawater temperature in most groups, but the correlation was positive for turf algae on the shallow reef flat. We hypothesise both direct and indirect effects of the strong seasonality.

A COMPARATIVE STUDY OF TEMPERATURE RESPONSES OF CARIBBEAN SEAWEEDS FROM DIFFERENT BIOGEOGRAPHIC GROUPS1

Temperature tolerances were determined for Caribbean isolates (total 31) of seaureds belonging to three distributional groups: 1) species confined to the tropical western Atlantic (Botryocladia spinulifera, Chamaedoris peniculum, Cladophoropsis sundanensis, Dictyopteris justii, Dictyurus occidentalis, Haloplegma duperreyi, and Heterosiphonia gibbesii); 2) amphi‐Atlantic species with a (sub)tropical distribution that have their northern boundary in the eastern Atlantic at the tropical Cape Verde Islands (Bryothamnion triquetrum and Ceramium nitens) or the subtropical Canary Islands (Ceratodictyon intricatum, Coelothrix irregularis, Dictyopteris delicatula, Ernodesmis verticillata, and Lophocladia trichoclados; and 3) species with an am‐phi‐Atlantic tropical to warm‐temperate distribution also occurring in the Mediterranean (Cladophoropsis membranacea, Digenea simplex, Microdictyon boergesenii, and Wurdemannia miniata). For some isolates, growth response curves and temperature requirements for reproduction were also determined. Growth occurred in the range (18)20–30° C with optimum growth rates at 25°–30°C, irrespective of distribution group. Reproduction generally occurred at (20)25°–30° C although there were some exceptions. Species were extremely stenothermal, with those restricted to the western Atlantic surviving a total range of only 10/13° C (between 18/20° and 30/33° C). Tolerance to high temperatures was correlated with vertical position in the iniertidal/subtidal zone rather than biogeography grouping. Species restricted to the subtidal were the least tolerant, with permanent survival at 30° C but not at 33°C. Tolerance to low temperatures was not different in subtidal and intertidal species but was significantly better in am phi‐Atlantic than in western Atlantic species. In the former group, damage occurred at 15°–18° C but in the latter group at 18°‐20° C. We propose that these differences in low‐temperature tolerances in Caribbean populations of species from different distribution groups reflect adaptations to glacial cold‐stress in the tropical eastern Atlantic and subsequent trans‐Atlantic dispersal.

Effects of wave exposure and depth on biomass, density and fertility of the fucoid seaweed Sargassum polyceratium (Phaeophyta, Sargassaceae)

Sargassum polyceratium is widely distributed around the island of Curaçao (Netherlands Antilles) where it inhabits strongly contrasting habitats. Changes in population structure have been followed in three bays with increasing levels of wave exposure at two depths: shallow (0 m) and deep (18 m). The effects of increasing wave exposure were investigated by studying three deep-water populations; and the effects of depth by studying shallow- and deep-water populations in the two calmer bays. Total density and stage density (reproductive thalli, juvenile thalli) were determined and total and individual thallus biomass was estimated non-destructively. In the most wave-exposed deep-water population thalli were twice as long with more than twice the biomass than in the calmest deep-water population. Total density and juvenile density were highest in the bay with intermediate wave exposure. Depth was an important factor at both the individual and population level. Shallow-water thalli had basal holdfast areas that were four times larger than those from deep water, and thallus biomass was positively correlated with holdfast area. Shallow-water juveniles invested more in the development of a holdfast and lateral growth than deep-water juveniles. Total biomass per quadrat was up to 10-fold higher in shallow- than in deep-water populations. In shallow-water populations reproductive thalli were present throughout the year whereas in deep-water populations they were present only during autumn and winter. We conclude that both wave exposure and depth affect population structure. Thalli were generally bigger and total biomass higher in the more exposed bay(s) and in shallower water, contradicting the general pattern in macroalgae of reduced size and biomass with increasing wave exposure.

TEMPERATURE RESPONSES OF DISJUNCT TEMPERATE BROWN-ALGAE INDICATE LONG-DISTANCE DISPERSAL OF MICROTHALLI ACROSS THE TROPICS

We examined the temperature tolerance of microscopic phases from geographically disjunct isolates of eight species or closely related, putatively conspecific taxa of temperate brown algae with disjunct distributions. Maximum within‐taxon differences were small and ranged from 1.6° to 4.3° C. Desmarestia aculeata and Sphaerotrichia divaricata, both with northern hemisphere amphioceanic distributions, showed little or no significant intraspecific variation between the mean upper survival limits (USL) of Atlantic and Pacific strains (δUSL ≤ 1.4°C), which would agree with a relatively recent separation of the respective populations. Among the plants with bipolar distributions, there was likewise very little difference (δUSL 0–1.1°C) between northern and southern hemisphere strains in Striaria attenuata and in the species pair Desmarestia viridis/D. willii. In Desmarestia ligulata, and in the species pairs Desmarestia firma/D. munda, Dictyosiphon foeniculaceus/D. hirsutus, and Scytothamnus australis/Scytothamnus sp., significant differences occurred, which indicate longer divergence times. δUSL in these cases ranged from 1.7° to 2.7°C, without overlap between strains from the northern and southern hemispheres. All species that passed the equator during cooler epochs had a USL of 26–27°C, at least in some geographical isolates. The NE Asian kelp Undaria pinnatifida, which passed the equator in recent times, had a USL of 29.6°C. We hypothesize that the mechanism of spreading in the amphipolar species studied was migration of vegetative microthalli. The more unlikely alternative hypothesis of continuous populations through the tropics during a cooler epoch would imply a drop in seawater temperatures to approximately 20° C in summer and 15° C in winter, which is not supported by paleoclimatic evidence.

Differences in acclimation potential of photosynthesis in seven isolates of the tropical to warm temperate macrophyte Valonia utricularis (Chlorophyta)

A. Eggert, R.J.W. Visser, P.R. Van Hasselt and A.M. Breeman. 2006. Differences in acclimation potential of photosynthesis in seven isolates of the tropical to warm temperate macrophyte Valonia utricularis (Chlorophyta). Phycologia 45: 546–556. DOI: 10.2216/05-03.1 The potential to acclimate photosynthesis to sub- and supra-optimal temperatures was investigated in seven isolates of Valonia utricularis (Roth) C. Agardh, a green macrophyte with a tropical to warm-temperate distribution. Photosynthesis–light response curves were obtained by measuring chlorophyll a fluorescence characteristics of algae grown at optimal (25°C), sub- and supra-optimal temperatures. Suboptimal temperatures were chosen to support 30% of the maximum relative growth rate in each isolate. Thermal acclimation was investigated by comparing short-term and long-term temperature effects on the initial rate of increase of the relative electron transport rate (rETR) and the maximum rETR under light-saturating conditions. Isolates from the northeast Atlantic and the Mediterranean all showed a strong potential to acclimate maximum rETR to suboptimal growth temperatures, i.e. short-term temperature effects were diminished after acclimation. However, photoinhibition, measured as a decrease of the maximal quantum yield (Fv/Fm), was found when plants were grown at 30°C. The isolates reduced light harvesting at 30°C by decreasing total chlorophyll content and by increasing the chlorophyll a/b ratio. Up-regulation of photoprotective processes by the xanthophyll cycle pigments was not observed. In contrast, isolates from the Indo-west Pacific were unable to acclimate photosynthesis to suboptimal growth temperatures and these temperatures were strongly photoinhibiting, even though adjustments on the pigment level were observed. All Indo-west Pacific isolates reached comparable maximum rETR values at 30° and 25°C. Thus, the Atlantic/Mediterranean isolates had a stronger potential to acclimate photosynthetic rates at suboptimal growth temperatures compared to the Indo-west Pacific isolates, which was accompanied by losses at 30°C. The results are discussed in a biogeographical context.