MORPHOLOGICAL VARIATION,SPECIES CONCEPTS,AND CLASSIFICATION OF AN UNUSUAL FOSSIL CENTRIC DIATOM (BACILLARIOPHYTA) FROM WESTERN NORTH AMERICA1

The classification system of diatoms (Bacillariophyta) is based almost entirely on the organization and structure of their silica cell walls. We have discovered Miocene freshwater fossils that contain valves of two different orders within the same organism. Within frustules of the genus Ellerbeckia Crawford, a genus of the order Melosirales, are contained frustules of the genus Actinocyclus Ehrenberg, a member of the Coscinodiscales. Based on the abundance of each morphotype, they appear to be able to reproduce themselves. The ability of a single diatom taxon to express this degree of morphological variability is unprecedented. These results suggest species concepts in diatoms may be in need of review and challenge the basis of the classification system for this widely distributed and ecologically important group of organisms.     

VARIABILITY IN CELL SIZE,NUTRIENT DEPLETION,AND GROWTH RATES OF THE SOUTHERN OCEAN DIATOM FRAGILARIOPSIS KERGUELENSIS (BACILLARIOPHYCEAE) AFTER PROLONGED IRON LIMITATION1

Diatoms are the main primary producers in the Southern Ocean, governing the major nutrient cycles. Fragilariopsis kerguelensis (O’Meara) Hust. is the most abundant diatom species in the Southern Ocean and its paleo‐oceanographic record is frequently used to reconstruct the past position and nutrient characteristics of the Antarctic polar front. Here we report on the responses of F. kerguelensis on prolonged exposure to a range of iron concentrations, allowing a characterization of morphological and nutrient‐depletion changes in relation to iron status. Under iron limitation, F. kerguelensis grew slower, cells became smaller, chains became shorter, and the nutrient‐depletion ratios changed. Prolonged exposure to iron limitation caused F. kerguelensis to decrease its surface area and volume 2‐fold, and to increase its surface‐to‐volume ratio by 25%. With the decrease in growth rates, silicon (Si) and phosphorus (P) depletion per cell remained fairly constant, but when normalized per surface area (Si) or per cell volume (P), depletion increased. In contrast, nitrogen (N) depletion per cell decreased significantly together with the decrease in growth rates but was constant when normalized per cell volume. The different response in Si, P, and N depletion resulted in changes in the nutrient‐depletion ratios, most notably in the Si:N ratio, which significantly increased, and in the N:P ratio, which significantly decreased with decreasing growth rates. It is concluded that under iron limitation, variation in cell size and/or nutrient depletion ultimately can cause changes in oceanic biogeochemical nutrient cycles. It enables the use of cell size of F. kerguelensis as a paleo‐oceanographic proxy.     

THE ROLE OF PHYTOPLANKTON SIZE ON PHOTOCHEMICAL RECOVERY DURING THE SOUTHERN OCEAN IRON EXPERIMENT1

Phytoplankton primary productivity in the Southern Ocean is controlled by complex interactions among iron, light, and grazing. This project interfaced with the Southern Ocean iron experiment (SOFeX) that created two iron‐enriched patches north and south of the Polar Front each with distinct silicic acid concentrations. We used pulse amplitude modulated fluorometry and measured the recovery of the maximum quantum yield of photochemistry (F_v/F_m) for three size fractions (whole, <5, <20 μm) and light adapted quantum yield (ΔF/F′_m) for single phytoplankton cells. The rates of recovery from iron stress were found to be unrelated to average cell size for both size‐fractioned and single‐celled measurements. The smallest cells appeared to exhibit more severe iron stress at the onset of the experiment than the larger taxa. The largest response detected in regression parameters was that of the pennate diatoms, which took only ～3.4 days to reach the maximum quantum yield, whereas the centric diatom Asteromphalus sp. reached maximum ΔF/F′_m after ～10.4 days. The north patch measurements showed a different response; the smallest cells never reached maximum ΔF/F′_m, whereas the size fraction containing the largest cells did. Single‐celled measurements made nearly 30 days after the initial iron enrichment suggested that diatoms were experiencing either silicic acid or iron limitation, whereas measurements of Phaeocystis sp. did not. These data represent the first study of in situ recovery rates of PSII for groups of diatoms, and may help elucidate the mechanisms of species change in response to environmental perturbation.     

Diatom elemental and morphological changes in response to iron limitation: a brief review with potential paleoceanographic applications

Diatoms are a major group of phytoplankton that account for approximately 40% of the ocean carbon fixation and the vast majority of biogenic silica production through the construction of their cell walls (termed frustules). These frustules accumulate and are partially preserved in the ocean sediments. Diatom growth and nutrient utilization in high‐nitrate, low‐chlorophyll regions of the world’s oceans are mostly regulated by iron availability. Diatoms acclimate to iron limitation by decreasing cell size. The associated increase in surface area‐to‐volume ratio and decrease in diffusive boundary layer thickness may improve nutrient uptake kinetics. In parallel, cellular silicon (Si) contents are elevated in iron‐limited diatoms relative to nitrogen (N) and carbon (C). Variations in degree of silicification and nutritional requirements of iron‐limited diatoms have been hypothesized to account for higher cellular Si and/or lower cellular N and C, respectively. However, in some diatoms, frustule silicification does not significantly change when cells are iron‐limited. Instead, changes in the Si‐containing valve surface area relative to volume within these diatoms is hypothesized to be responsible for the variations in the cellular Si : N and Si : C ratios. In particular, some examined iron‐limited pennate diatoms have reduced widths relative to their lengths (i.e. lower length‐normalized widths, LNW) compared to iron‐replete cells. In the pennate diatom Fragilariopsis kerguelensis, the mean LNWs of valves preserved in sediments throughout the Southern Ocean (a well‐characterized iron‐limited region) is positively correlated with satellite‐derived, climatological net primary productivity in the overlying waters. Because of the specific morphological changes in pennate diatom frustules in response to iron availability, the valve morphometerics (e.g. LNWs) can potentially be used as a diagnostic tool for iron‐limited diatom growth and relative changes in the Si : N (and Si : C) ratios in extant diatom assemblages as well as those preserved in the sediments.     

OBSERVATIONS ON THE SURVIVAL AND GERMINATION OF RESTING SPORES OF THREE CHAETOCEROS (BACILLARIOPHYCEAE) SPECIES1,2

Resting spores (hypnospores) of Chaetoceros diadema (Ehrenberg) Gran, Chaetoceros vanheurckii Gran, and Chaetoceros didymus Ehrenberg were collected from a large plastic enclosure moored in Saanich Inlet, B.C., Canada. The effects of combinations of temperature and irradiance on the germination of these resting spores were investigated. Nutrient uptake, carbon fixation, and changes in the photosynthetic capacity of the germinating spores were also examined. Resting spores germinated optimally at combinations of temperature and irradiance similar to those in the environment during sporulation. They did not germinate at irradiances 1.3 μEin m^?2 s^?1 or temperatures >25.3° C. Nitrate, phosphate and silicate were taken up after the resting spores had germinated and resumed vegetative growth. Chlorophyll a fluorescence in vivo, and the DCMU-induced increase in in vivo fluorescence also increased after the resting spores had germinated. Resting spores began to fix carbon as soon as they were placed in light. Spores remained viable for at least 645 d. The length of time between first exposure to light and germination did not change during this period; however, the percentage of viable resting spores decreased markedly. None of the Chaetoceros spores germinated after 737 d of storage at 2–4° C in darkness.     

Two Southern Ocean diatoms are more sensitive to ocean acidification and changes in irradiance than the prymnesiophyte Phaeocystis antarctica

To better understand the impact of ocean acidification (OA) and changes in light availability on Southern Ocean phytoplankton physiology, we investigated the effects of pCO₂ (380 and 800 µatm) in combination with low and high irradiance (20 or 50 and 200 µmol photons m^?2 s^?1) on growth, particulate organic carbon (POC) fixation and photophysiology in the three ecologically relevant species Chaetoceros debilis, Fragilariopsis kerguelensis and Phaeocystis antarctica. Irrespective of the light scenario, neither growth nor POC per cell was stimulated by OA in any of the tested species and the two diatoms even displayed negative responses in growth (e.g. C. debilis) or POC content (e.g. F. kerguelensis) under OA in conjunction with high light. For both diatoms, also maximum quantum yields of photosystem II (F_v/F_m) were decreased under these conditions, indicating lowered photochemical efficiencies. To counteract the negative effects by OA and high light, the two diatoms showed diverging photoacclimation strategies. While cellular chlorophyll a (Chl a) and fucoxanthin contents were enhanced in C. debilis to potentially maximize light absorption, F. kerguelensis exhibited reduced Chl a per cell, increased disconnection of antennae from photosystem II reaction centers and strongly lowered absolute electron transport rates (ETR). The decline in ETRs in F. kerguelensis might be explained in terms of different species‐specific strategies for tuning the available flux of adenosine triphosphate and nicotinamide adenine dinucleotide phosphate. Overall, our results revealed that P. antarctica was more tolerant to OA and changes in irradiance than the two diatoms, which may have important implications for biogeochemical cycling.     

Iron Limitation Modulates Ocean Acidification Effects on Southern Ocean Phytoplankton Communities

The potential interactive effects of iron (Fe) limitation and Ocean Acidification in the Southern Ocean (SO) are largely unknown. Here we present results of a long-term incubation experiment investigating the combined effects of CO₂ and Fe availability on natural phytoplankton assemblages from the Weddell Sea, Antarctica. Active Chl a fluorescence measurements revealed that we successfully cultured phytoplankton under both Fe-depleted and Fe-enriched conditions. Fe treatments had significant effects on photosynthetic efficiency (F_v/F_m; 0.3 for Fe-depleted and 0.5 for Fe-enriched conditions), non-photochemical quenching (NPQ), and relative electron transport rates (rETR). pCO₂ treatments significantly affected NPQ and rETR, but had no effect on F_v/F_m. Under Fe limitation, increased pCO₂ had no influence on C fixation whereas under Fe enrichment, primary production increased with increasing pCO₂ levels. These CO₂-dependent changes in productivity under Fe-enriched conditions were accompanied by a pronounced taxonomic shift from weakly to heavily silicified diatoms (i.e. from Pseudo-nitzschia sp. to Fragilariopsis sp.). Under Fe-depleted conditions, this functional shift was absent and thinly silicified species dominated all pCO₂ treatments (Pseudo-nitzschia sp. and Synedropsis sp. for low and high pCO₂, respectively). Our results suggest that Ocean Acidification could increase primary productivity and the abundance of heavily silicified, fast sinking diatoms in Fe-enriched areas, both potentially leading to a stimulation of the biological pump. Over much of the SO, however, Fe limitation could restrict this possible CO₂ fertilization effect.     

DIATOMS AS HOSTS FOR OTHER DIATOMS: OBSERVATIONS FROM SOUTHERN CALIFORNIA

Large epiphytic and epilithic diatom species hosting other diatoms were observed in several fresh‐ and brackish water sites in Southern California. The most commonly encountered hosts were species forming long filaments attached to rocks or macroalgae, Hydrosera whampoensis (Schwarz) Hendey, Melosira varians Agardh, Pleurosira laevis (Ehrenberg) Compere and Terpsinoe musica Ehrenberg. These large diatoms often had smaller diatoms attached, usually to the girdle bands and occasionally to the mucilage pads connecting the cells. For example, cells of T. musica were observed supporting growth of a diverse diatom assemblage composed of species of the genera Achnanthes, Achnanthidium, Amphora, Cocconeis and Tabularia; Synedra sp. was attached to M. varians and B. paxillifer; and Cocconeis placentula was seen on H. whampoensis. Thus, large epiphytic and epilithic diatoms seem to provide suitable sites for attachment of small epiphytic diatom species, and it appears that this phenomenon is more common than previously thought.     

Phenotypic Plasticity of Southern Ocean Diatoms: Key to Success in the Sea Ice Habitat?

Diatoms are the primary source of nutrition and energy for the Southern Ocean ecosystem. Microalgae, including diatoms, synthesise biological macromolecules such as lipids, proteins and carbohydrates for growth, reproduction and acclimation to prevailing environmental conditions. Here we show that three key species of Southern Ocean diatom (Fragilariopsis cylindrus, Chaetoceros simplex and Pseudo-nitzschia subcurvata) exhibited phenotypic plasticity in response to salinity and temperature regimes experienced during the seasonal formation and decay of sea ice. The degree of phenotypic plasticity, in terms of changes in macromolecular composition, was highly species-specific and consistent with each species’ known distribution and abundance throughout sea ice, meltwater and pelagic habitats, suggesting that phenotypic plasticity may have been selected for by the extreme variability of the polar marine environment. We argue that changes in diatom macromolecular composition and shifts in species dominance in response to a changing climate have the potential to alter nutrient and energy fluxes throughout the Southern Ocean ecosystem.     

THE EFFECT OF IRON LIMITATION ON THE PHOTOPHYSIOLOGY OF PHAEOCYSTIS ANTARCTICA (PRYMNESIOPHYCEAE) AND FRAGILARIOPSIS CYLINDRUS (BACILLARIOPHYCEAE) UNDER DYNAMIC IRRADIANCE1

The effects of iron limitation on photoacclimation to dynamic irradiance were studied in Phaeocystis antarctica G. Karst. and Fragilariopsis cylindrus (Grunow) W. Krieg. in terms of growth rate, photosynthetic parameters, pigment composition, and fluorescence characteristics. Under dynamic light conditions mimicking vertical mixing below the euphotic zone, P. antarctica displayed higher growth rates than F. cylindrus both under iron (Fe)–replete and Fe‐limiting conditions. Both species showed xanthophyll de‐epoxidation that was accompanied by low levels of nonphotochemical quenching (NPQ) during the irradiance maximum of the light cycle. The potential for NPQ at light levels corresponding to full sunlight was substantial in both species and increased under Fe limitation in F. cylindrus. Although the decline in F_v/F_m under Fe limitation was similar in both species, the accompanying decrease in the maximum rate of photosynthesis and growth rate was much stronger in F. cylindrus. Analysis of the electron transport rates through PSII and on to carbon (C) fixation revealed a large potential for photoprotective cyclic electron transport (CET) in F. cylindrus, particularly under Fe limitation. Probably, CET aided the photoprotection in F. cylindrus, but it also reduced photosynthetic efficiency at higher light intensities. P. antarctica, on the other hand, was able to efficiently use electrons flowing through PSII for C fixation at all light levels, particularly under Fe limitation. Thus, Fe limitation enhanced the photophysiological differences between P. antarctica and diatoms, supporting field observations where P. antarctica is found to dominate deeply mixed water columns, whereas diatoms dominate shallower mixed layers.     

IMPORTANCE OF RESTING STAGES IN DIATOM SEASONAL SUCCESSION1

The role of environmental factors in seasonal succession of six clones of marine diatoms was examined by testing effects of various combinations of temperature (5°, 10°, 15°, 20°C) and photoperiod (10, 12, 14, 16 h) on time to germination of resting stages and subsequent vegetative cell division rates. Resting stages were induced in batch cultures using a low nutrient medium and a cold, dark period. A three-factor ANOVA showed that species, temperature, daylength, and their interactions signficantly (P =0.0001) injuenced germination time and division rate. Resting stages of Chaetoceros similis Cleve and Odontella aurita (Lyngbye) Agardh were most successful in producing populations of cells on warm, long days (20°C/16 h). Chaetoceros didymus Ehrenberg and C. cinctus Gran were most successful under more moderate conditions (15°C/14 h). Resting stages of Ditylum bright-wellii (West) Grunow germinated and cells divided rapidly under all conditions. No consistent pattern was evident with Thalassiosira rotula Meunier. We compared results of the laboratory study with environmental conditions prevailing during the presence of these species in a British Columbia fjord. Favorable growth conditions determined for C. didymus, D. brightwellii, and T. rotula were similar to conditions present when these species were commonly found in the fjord.     

COMPARATIVE PHYSIOLOGICAL STUDY OF MARINE DIATOMS AND DINOFLAGELLATES IN RELATION TO IRRADIANCE AND CELL SIZE. I. GROWTH UNDER CONTINUOUS LIGHT1,2

Cell division rates and chlorophyll a and protein contents for ten diatom and dinoflagellate species were measured. Species were chosen to include a wide range of cell size in terms of both cell volume and cell protein: from 0.004 ng protein/cell for a small Chaetoceros sp. to 2.2 ng protein/cell for Prorocentrum micans Ehrenberg. Experiments were conducted in batch or semi-continuous cultures at 21 C under continuous illumination from 8–256 μEin ^.m^-2'^.s^-1. Light saturation of cell division occurred at 32–80 μEin m^-1 s^-1 for all species, with no observable difference between the two phylogenetic groups. When the light-saturated cell division rates were plotted against cell size as protein/cell, the diatoms and dinoflagellates fell on two separate lines with the diatoms having higher rates. Chl a /protein ratios (μg/μg) decreased with increasing irradiance. The diatoms had higher chl a per unit protein. The relationship between cell division rate and the chl a/protein ratio is discussed.     

PHYTOPLANKTON SELENIUM REQUIREMENTS: THE CASE FOR SPECIES ISOLATED FROM TEMPERATE AND POLAR REGIONS OF THE SOUTHERN HEMISPHERE1

A series of laboratory culture experiments was used to investigate the effect of selenium (Se, 0–10 nM) on the growth, cellular volume, photophysiology, and pigments of two temperate and four polar oceanic phytoplankton species [coccolithophore Emiliania huxleyi (Lohmann) W. W. Hay et H. P. Mohler, cyanobacterium Synechococcus sp., prymnesiophyte Phaeocystis sp., and three diatoms—Fragilariopsis cylindrus (Grunow) Kriegar, Chaetoceros sp., and Thalassiosira antarctica G. Karst.]. Only Synechoccocus sp. and Phaeocystis sp. did not show any requirement for Se. Under Se‐deficient conditions, the growth rate of E. huxleyi was decreased by 1.6‐fold, whereas cellular volume was increased by 1.9‐fold. Se limitation also decreased chl a (2.5‐fold), maximum relative electron transport rate (1.9‐fold), and saturating light intensity (2.8‐fold), suggesting that Se plays a role in photosynthesis or high‐light acclimation. Pigment analysis for Antarctic taxa provided an interesting counterpoint to the physiology of E. huxleyi. For all Se‐dependent Antarctic diatoms, Se limitation decreased growth rate and chl a content, whereas cellular volume was not affected. Pigment analysis revealed that other pigments were affected under Se deficiency. Photoprotective pigments increased by 1.4‐fold, while diadinoxanthin:diatoxanthin ratios decreased by 1.5‐ to 4.9‐fold under Se limitation, supporting a role for Se in photoprotection. Our results demonstrate an Se growth requirement for polar diatoms and indicate that Se could play a role in the biogeochemical cycles of other nutrients, such as silicic acid in the Southern Ocean. Se measurements made during the austral summer in the Southern Ocean and Se biological requirement were used to discuss possible Se limitation in phytoplankton from contrasting oceanographic regions.     

The use of outdoor phytoplankton continuous cultures to analyse factors influencing species selection

Natural phytoplankton populations have been grown in outdoor continuous cultures at three dilution rates (D = 0.5, 0.25, and 0.1 · day^?1) under nitrogen (N) or silicon (Si) limitation and two light intensities. At a high specific nutrient flux (high dilution rate) under N limitation an assemblage of primarily small, fast growing centric diatoms such as Skeletonema costatum (Grev.) Cleve and Chaetoceros spp. dominated with a low percentage of flagellates. At a low specific nutrient flux, a mixture of larger, slower growing centric diatoms, small flagellates, and pennate diatoms was obtained. Similar trends were observed under silicate limitation. Decreasing the light intensity at the lowest dilution rate selected for an assemblage similar to that observed at the high dilution rate and high light intensity.The results of these competition experiments suggest that specific nutrient flux (dilution rate) is an important factor in determining between group dominance (e.g., centric and pennate diatoms and small flagellates). Successful competitors representing broad phytoplankton groups can be arranged along a resource gradient of specific nutrient flux (dilution rate), with groups such as centric and pennate diatoms, represented as high and medium flux species, respectively.     

Pigment distribution in the Pacific region of the Southern Ocean (autumn 1995)

Phytoplankton distribution patterns are still largely unknown for the Pacific region of the Southern Ocean. Pigment distributions were determined by HPLC on 40-m samples collected from the mixed layer during the ANTXII/4 cruise in March–May 1995 aboard RV “Polarstern”. A transect was covered (90°W, from 51°S to 70°S), crossing the Subantarctic Front in the north, the Polar Front, and the Southern Polar Front in the south. Coinciding with high concentrations of silicate, diatoms dominated in the Antarctic waters south of the Polar Front. North of the Polar Front, silicate concentrations dropped to values less than 10 μM. In this area flagellates (Prymnesiophyceae and green algae) were the dominant phytoplankton group. Nutrient depletion of the surface waters near the Southern Polar Front indicated formerly enhanced productivity. These findings confirmed previous observations by the British Sterna expedition, which described locally elevated chlorophyll a biomass near the southern boundary of the Southern Polar Front. We propose a role for supply of bioavailable iron via the front, and emphasise the importance of frontal systems for phytoplankton productivity in the Southern Ocean. Received: 11 June 1997 / Accepted: 16 November 1997     

Influence of sea ice on the composition of the spring phytoplankton bloom in the northern Baltic Sea

During the late winter and spring of 1994, the influence of sea ice on phytoplankton succession in the water was studied at a coastal station in the northern Baltic Sea. Ice cores were taken together with water samples from the underlying water and analysed for algal composition, chlorophyll a and nutrients. Sediment traps were placed under the ice and near the bottom, and the sedimented material was analysed for algal composition. The highest concentration of ice algae (4.1 mmol C m⁻²) was found shortly before ice break-up in the middle of April, coincidental with the onset of an under-ice phytoplankton bloom. The ice algae were dominated by the diatoms Chaetoceros wighamii Brightwell, Melosira arctica (Ehrenberg) Dickie and Nitzschia frigida Grunow. Under the ice the diatom Achnanthes taeniata Grunow and the dinoflagellate Peridiniella catenata (Levander) Balech were dominant. Calculations of sinking rates and residence times of the dominant ice algal species in the photic water column indicated that only one ice algal species (Chaetoceros wighamii) had a seeding effect on the water column: this diatom dominated the spring phytoplankton bloom in the water together with Achnanthes taeniata and Peridiniella catenata. Received: 9 May 1997 / Accepted: 15 February 1998     

Photoadaptation in marine Arctic diatoms

Summary Photoadaptation in some marine Arctic diatoms has been studied. Thalassiosira antarctica, Nitzschia delicatissima and Chaetoceros furcellatus were grown at-0.5°C and various irradiances and continuous light. Growth and cellular chlorophyll were followed during transitional phase after the algae had been transferred from one irradiance to another. Adaptation time for cellular chlorophyll was linearly related to the gradient in irradiance, and adaptation to transfer from high to low light was faster than from low to high light. Adaptation time was found to be species dependent, and Arctic diatoms growing at low temperature seemed to adapt as fast as temperate species.Contribution No. 243 from Trondhjem Biological Station