Products of photosynthesis in natural populations of marine phytoplankton from the Gulf of Maine

We have measured the photosynthetic assimilation of ¹⁴C-carbon dioxide into (1) ethanol-soluble, (2) hot-trichloroacetic acid (TCA)-soluble (polysaccharide), and (3) protein fractions of natural populations of marine phytoplankton. Diurnal studies showed a continuing incorporation of carbon-14 into the protein fraction during hours of darkness. This was accompanied by a concomitant decrease in the proportion assimilated into polysaccharide. When incorporation was measured under constant experimental conditions, the pattern of photosynthesis did not vary from one time of day to another. At one station approximately 12 km south of Boothbay Harbor, the proportion of carbon entering protein showed marked seasonal changes. During the winter, approximately 10 to 20% of the fixed carbon was incorporated into protein. During the summer the value increased to 22 to 35%. Between these times, a transient high value of 37 to 47% of the fixed carbon entering protein coincided with the spring bloom. The increases in proportion incorporated into protein were largely paralleled by equivalent decreases in the polysaccharide fraction. The proportion of carbon incorporated into protein during photosynthesis also increased markedly at reduced light intensities. This increase occurred both when populations were incubated in neutral-density filters and when incubated at increasing depths in the photic zone. There was little consistent and significant difference between the neutral-density filters and depth in the water column, suggesting a minimal role for light quality. The extent of the increased relative rate of protein synthesis at the lower light intensities depended on the nutritional state of the phytoplankton. For example, summer populations from water containing low concentrations of inorganic nutrients responded less dramatically to reduced light intensities than did populations from nutrient-rich waters.     

Feeding and absorption of the toxic dinoflagellate Alexandrium tamarense by two marine bivalves from the South China Sea

Paralytic shellfish poisoning (PSP) toxins can be accumulated by bivalves through the feeding process; therefore, knowledge on feeding and the assimilation of PSP-toxin-containing algae is critical to understand the kinetics of PSP toxins in these bivalves. In the South China Sea, it has been documented that the scallop Chlamys nobilis has a much higher PSP toxin burden than the clam Ruditapes philippinarum. Experiments were therefore carried out to assess whether the difference in toxin burden between these two species of bivalves was due to differences in feeding and absorption. In a mixed diet of Alexandrium tamarense (a PSP-toxin-producing dinoflagellate) and Thalassiosira pseudonana (a non-toxic diatom), the maximum clearance and filtration rates were about two times higher in the scallop C. nobilis than in the clam R. philippinarum. Furthermore, the clams produced pseudofeces at a lower cell density than the scallops. However, we found that the clams were unable to selectively exclude the toxic dinoflagellates by pseudofeces production. The scallop C. nobilis also possessed a greater ability to assimilate A. tamarense with a comparable carbon absorption efficiency to the diatom T. pseudonana. In contrast, the carbon absorption in the clam R. philippinarum was lower when feeding on A. tamarense than on the diatom. In general, the absorption efficiency decreased with increasing concentration of A. tamarense. Thus, it is likely that the higher PSP toxin levels in the scallops compared with clams can be partly explained by differences in their feeding and absorption behavior. Other processes, especially the biotransformation and biokinetics of PSP toxins, may also play a significant role in defining the inter-species differences in PSP body burden in marine bivalves.     

Toxic phytoplankton blooms in the southwestern Gulf of Maine: testing hypotheses of physical control using historical data

Blooms of the toxic dinoflagellate Alexandrium tamarense Lebour have been nearly annual features along the coasts of southern Maine, New Hampshire and Massachusetts, USA, since 1972. In 1990 two hypotheses which have been used to explain the initiation of these blooms in the southwestern portion of the Gulf of Maine were tested using historical records of shellfish toxicity, wind, and river flow. The first hypothesis states that the blooms were initiated or advected to shore by wind-driven coastal upwelling. The second states that established blooms were advected from north to south alongshore in a coastally trapped buoyant plume of water. Of the eleven years examined (1979 to 1989), we found seven cases inconsistent with the wind-driven upwelling hypothesis, and only one case (1985) which contradicts the plume-advection hypothesis. 1985 was an unusual year in many respects, and we suggest that some other mechanism was responsible for the toxic outbreaks. In addition, the wind-driven upwelling hypothesis could not explain the observed north-to-south temporal progression of toxicity each year. The plume-advection hypothesis was found to best explain the datails of the timing and spread of shellfish toxicity in Gulf of Maine waters to the south of Penobscot Bay, Maine. These include the variable north-to-south progression with time, the presence of a toxin-free zone south of Cape Ann, Massachusetts, the sporadic nature of toxic outbreaks south of Massachusetts Bay, and the apparently rare occurrence of high toxicity levels well offshore on Nantucket Shoals and Georges Bank.     

Potential impact of a toxic dinoflagellate (Alexandrium excavatum) bloom on survival of fish and crustacean larvae

During the last 20 yr the western half of the Dutch Wadden Sea has undergone significant eutrophication: concentrations of P and N compounds and planktonic algae have roughly doubled, as has primary production. Though oxygen levels are often low in summer, anoxic areas are small and rare due to strong tidal mixing. During the 1970 to 1990 period, macrozoobenthos was sampled annually at 15 stations at Balgzand, a 50-km² tidal-flat area in the westernmost part of the Wadden Sea. Not only did the estimates of total numbers, biomass, and production double during these two decades, but significant changes in the composition of the benthic community were observed, too: (1) the numerical proportion of polychaetes increased at the expense of molluscs and crustaceans, (2) the overall mean weight per individual of the macrozoobenthos decreased (numbers of individuals of small-sized species increased more rapidly than those of large-sized species), and (3) though absolute numbers and biomass of all feeding types increased, the share of carnivores declined and that of deposit feeders increased; the proportion of suspension feeders showed little change. This study refers to true macrobenthos only (1-mm sieve) and further excludes two taxa (Corophium spp. andHydrobia ulvae) which occasionally exercised an undue influence on numbers. Mass mortalities caused by low oxygen concentrations were of a small-scale nature only. Total number of species fluctuated without a clear trend. As a consequence of the increasing numerical densities, trends in species numbers were slightly increasing when expressed per unit of area and slightly decreasing when estimated per 100 individuals (by rarefaction).     

Nutrient starvation effects on the allelochemical potency of Alexandrium tamarense (Dinophyceae)

Batch culture experiments were performed to investigate potential effects of nutrient starvation on the allelochemical potency of the toxic dinoflagellate Alexandrium tamarense. Triplicate cultures with reduced nitrate (−N) or phosphate (−P) seed were compared to nutrient-replete (+N+P) cultures. Total depletion of the dissolved inorganic limiting nutrient, reduced cell quotas, changed mass ratios of C/N/P and reduced cell yield clearly indicate that treatment cultures at stationary phase were starved by either N or P, whereas growth cessation of +N+P cultures was probably due to carbon limitation and/or a direct effect of high pH. Pulsed addition of the limiting nutrient allowed −N and −P cultures to resume growth. Lytic activity of A. tamarense as quantified by a Rhodomonas bioassay was generally high (EC₅₀ around 100 cells mL⁻¹) and was only slightly modulated by growth phase and/or nutrient starvation. Lytic activity per cell increased with time in both +N+P and −P cultures but not −N cultures. P-starved stationary-phase cells were slightly more lytic than +N+P cultures, but this difference may be due to increased cell size and/or accumulation of extracellular compounds. In conclusion, only slight changes but no general and major increase in lytic activity in response to nutrient starvation was observed.     

Recent Invasions of the Gulf of Maine: Three Contrasting Ecological Histories

Introduced species are common members of estuarine communities where their role as competitors and predators is of concern, This paper examines the invasion of Gulf of Maine benthic habitats by the ecologically similar alien invertebrates Styela clava, Botrylloides diegensis , and Membranipora membranacea .
Styela clava increased slowly in abundance at study sites in Beverly, Massachusetts and Portsmouth, New Hampshire. We found no evidence of competitive dominance by S. clava , even though it is the competitive dominant in similar habitats elsewhere. Botrylloides diegensis rapidly became a dominant species after its arrival in the Great Bay Estuary, but this dominance was short-lived. B. diegensis persists in the estuary as an early colonist of primary space and as an epibiont on secondary substrates in established communities. Membranipora membranacea became the dominant epiphyte on laminarian kelps within two years. Although M. membranacea overgrew the native epiphytes Obelia geniculata and Electra pilosa in the overwhelming majority of encounters these native species are more common on other algal hosts. Therefore, competitive dominance is not likely a factor in the successful invasion of the Gulf of Maine by M. membranacea .
These species provide evidence for opposing views of the role of competition in mediating community invasion. We show that ecological similarity among species is not an accurate criterion to predict either the mechanism of invasion or the means of persistence. In addition, these data indicate that biological invasions must be examined on broad spatial and temporal scales; short-term or narrowly focused studies can lead to incorrect conclusions.     

Benthic response to sedimentation of a spring phytoplankton bloom: Process and budget

The response of benthos to sedimentation of the spring phytoplankton bloom in the Kiel Bight (Western Baltic Sea) is described in terms of biomass (ATP) and activity (heat production and ETS-activity). Input of the bloom (11.5 g C m^-2) over a period from March 25 to April 19, 1980 to the sediment surface was in the form of cells and fresh phytodetritus as indicated by low C/N ratios (7) and high energy charge values (0.78). Benthic microbial activity was immediately stimulated by this input as heat production doubled and the activity of ETS tripled over winter values within 12 d in the absence of a significant increase in ambient temperature. A comparison of the two activity parameters suggests that anaerobic metabolism is more important during the winter (February and March) than after input of the bloom. Meiofauna was not able to take part in the first activity outburst. Benthic ATP-biomass (excluding macrofauna) doubled in late April due to microbial production, and doubled again in early May when meiofauna started reproductive activity. For macrofauna a general statement was not possible, although the sediment surface feeder Macoma baltica commenced a build up of glycogen and lipid resources immediately following bloom input whereas Nephtys ciliata, feeding on sediment and small macrofauna, showed a less pronounced and delayed effect from this input. An energy budget based on heat production measurements was calculated. A daily heat loss of the benthic community of 21.7 KJ m^-2 d^-1 (35.5 KJ m^-2 d^-1) was found, when a depth of 3 cm sediment (5 cm) was assumed. Heat production of macrofauna contributed less than 5% of this activity. The input of the bloom was burned within 21 (13) d. Preliminary estimations for an annual budget suggest that the vertical transport of particulate organic matter via sedimentation can only explain 25% (15%) of the benthic activity in the shallow water ecosystem of the Kiel Bight. This indicates the presence of other sources of organic carbon such as benthic primary production or other transport processes providing carbon to the sediments.Publication No. 384 of the Joint Research Program of Kiel University (Sonderforschungsbereich 95)     

Copepod grazing during a declining spring phytoplankton bloom in the Northern North Sea

Grazing rates of larger (Calanus finmarchicus) and smaller (Acartia clausii Pseudocalanus elongatus etc.) copepods on naturally occurring phytoplankton populations were measured during a declining spring phytoplankton bloom. During the initial period, dominated by Chaetoceros spp. diatoms, constant ingestion rates were observed in Calanus finmarchicus at suspended particulate concentrations above 300 g carbon l^-1. Average daily intake during this time amounted to 35 to 40% of body carbon and reached a maximum of 50%. The feeding response of the smaller copepods was not so well defined, although a maximum daily intake of 56% body carbon was recorded. In both groups, feeding thresholds were at particulate concentrations around 50 g C l^-1. The feeding response of C. finmarchicus was correlated with both a change in their own population and in the food cell type. Linear regressions describing the concentration-dependent feeding response were: ingestion rate (IR)=1.16 total particulate volume (TPV)-36.15 during the initial part of the period compared with IR=0.41 TPV-12.18 for the latter period. C. finmarchicus filtered out slightly larger (x 1.2 diameter) particles than the small copepods and, in both groups, some filtering adjustment was made to accomodate to modal changes in the phytoplankton population from 20–30 m to 10 m diameter cells. Particle production during feeding was frequently evident in the smallest size ranges of particles and the ratio of particle production to ingestion rate was greater at low feeding rates.     

The Baltic Sea spring phytoplankton bloom in a changing climate: an experimental approach

The response of the Baltic Sea spring bloom was studied in mesocosm experiments, where temperatures were elevated up to 6°C above the present-day sea surface temperature of the spring bloom season. Four of the seven experiments were carried out at different light levels (32–202?Wh?m^?2 at the start of the experiments) in the different experimental years. In one further experiment, the factors light and temperature were crossed, and in one experiment, the factors density of overwintering zooplankton and temperature were crossed. Overall, there was a slight temporal acceleration of the phytoplankton spring bloom, a decline of peak biomass and a decline of mean cell size with warming. The temperature influence on phytoplankton bloom timing, biomass and size structure was qualitatively highly robust across experiments. The dependence of timing, biomass, and size structure on initial conditions was tested by multiple regression analysis of the y-temperature regressions with the candidate independent variables initial light, initial phytoplankton biomass, initial microzooplankton biomass, and initial mesozooplankton (=copepod) biomass. The bloom timing predicted for mean temperatures (5.28°C) depended on light. The peak biomass showed a strong positive dependence on light and a weaker negative dependence on initial copepod density. Mean phytoplankton cell size predicted for the mean temperature responded positively to light and negatively to copepod density. The anticipated mismatch between phytoplankton supply and food demand by newly hatched copepod nauplii occurred only under the combination of low light and warm temperatures. The analysis presented here confirms earlier conclusions about temperature responses that are based on subsets of our experimental series. However, only the comprehensive analysis across all experiments highlights the importance of the factor light.     

Further studies of short-term variation in the pigment composition of a spring phytoplankton bloom

Phytoplankton sampled at the chlorophyll maximum during the spring bloom at Loch Ewe, Scotland during 1986, were analysed using high-performance liquid chromatography for chloropigments and carotenoids. The day-to-day proportions of the pigments remained relatively stable throughout the bloom, with good preservation of chlorophyll a even at the sediment surface. Chlorophyllide a and phaeophorbide a appeared towards the end of the bloom. The major carotenoids remained stable throughout the bloom, but became rapidly degraded on sedimentation under the oxic conditions. The pigment data is related to the nutrient status of the bloom, when slow steady growth occurred without nutrient limitation. These data contrast sharply with data from the 1983 spring bloom at Loch Ewe when acute nutrient limitation took place.     

Naked Dictyocha speculum — a new type of phytoplankton bloom in the Western Baltic

Chlamydomonas pulsatilla Wollenweber, a euryhaline, marine flagellate (isolated from rockpool at St. Andrew's, New Brunswick, Canada in 1980 by J. A. Hellebust), shows decreasing rates of activity of its four contractile vacuoles in the salinity range of 0 to 15% artificial seawater (ASW). Electron microscopy shows that the contractile vacuole complex persists as a spongiome (collection of small vesicles or tubules) in cells grown at salinities above the range for operation of contractile vacuoles. From calculations of rates of water expulsion, based on size and frequency of contraction of individual vacuoles determined by light microscopy, the time necessary to empty one cell volume increased from ca 20 min at 1% ASW to ca 600 min at 15% ASW. Analysis of inorganic and organic solute contents of cells grown at 1 and 5% ASW allowed the calculation of internal osmotic pressures. Estimates of hydraulic conductivities based on rates of water expulsion via contractile vacuoles and differences in internal and external osmotic pressures resulted in values ranging from 1.1 to 1.4×10^-14 m s^-1 Pa^-1 for individual cells. Growth experiments at low photon flux densities over a salinity range of 1 to 15% ASW, over which contractile vacuole activity varied by a factor of 30, showed little difference in growth rates. This indicates that the cost for operation of contractile vacuoles must be very low. The secretion of large molecular weight organic substances does not appear to be associated with the functioning of contractile vacuoles.     

Growth and collapse of a spring phytoplankton bloom in the Firth of Clyde,Scotland

A range of physical and chemical parameters were measured through the water column at two previously unstudied shallow-water sites in the Firth of Clyde, Scotland, in the spring of 1991. Sediment traps were also deployed at one of the sites. The results of this survey are presented and discussed. A bloom of Skeletonema costatum was observed at one site through March and into April, when it collapsed completely, the phytoplanktonic cells sedimenting out of the water column. No significant bloom or sedimentation was observed at the second study site.     

Change in a bacterial population during the process of degradation of a phytoplankton bloom in a brackish lake

Change in a bacterial population during the process of degradation of a phytoplankton bloom was investigated at Lake Hamana, Japan in June 1981. The predominant phytoplankton were Prorocentrum micans Ehrenberg and P. triestinum Schiller. While most phytoplankton cells were living and moving actively, most bacteria were those in a free-living state (free-living bacteria) and the number of bacteria associated with particulate materials (attached bacteria) was less than a few percent of the total bacterial number. As the decline process proceeded, the number of free-living bacteria remained almost constant or decreased slightly; on the other hand, the number of attached bacteria increased gradually and reached about 40% of the total bacterial number. These results indicate that some of the free-living bacteria become attached to particulate organic matter and grow on the surface of the particles.     

Sedimentation of particulate matter during a phytoplankton spring bloom in relation to the hydrographical regime

Data presented and discussed here were collected continuously during April/May 1975 in the Bornholm Basin of the Baltic Sea. Sedimentation rates of particulate matter were recorded with 5 multisample sediment traps from different depths in the water column at 2 positions 170 km apart. Current meter data collected during the same period and depths indicated that the positions remained hydrographically distinct during the investigation. Particulate matter from the euphotic zone including diatom cells formed the bulk of the material collected by all traps. This flux of organic particles to the bottom was unimpeded by the strong density stratification present in the water column. The upper traps always collected less material than lower ones. This paradox has been ascribed to diminishing current speeds with depth, concomitant with an increase in sinking rates of phytoplankton and phytodetritus. Both factors influence the sampling efficiency of sediment traps, which are thought to have underestimated actual sedimentation rates here. A time lag of 2 to 3 weeks in bloom development seemed responsible for the characteristic differences between the two positions. The phase of major sedimentation at one position covered about 18 days, and a distinct sequence in the composition of the material collected by the 6 glasses of each trap indicated phases of a progressively deteriorating phytoplankton population in the water column contributing the particulate material. A total of 6.2 g C m^-2 in 34 days was recorded at this station. Apart from a trap situated in an oxygen deficient layer which collected 0.44 g C m^-2 of zooplankton corpses, zooplankton mortality was overestimated by the traps. Large-scale sedimencation of fresh organic matter produced by the spring bloom is probably a regular feature in areas with low over-wintering zooplankton populations and, as such, possibly has a direct stimulatory effect on growth and reproduction of the benthos.Contribution No. 185 of the Joint Research Programme 95, Kiel University.     

Shading facilitates sessile invertebrate dominance in the rocky subtidal Gulf of Maine

Dramatic shifts in community composition occur between vertical and horizontal rocky surfaces in subtidal environments worldwide, yet the forces mediating this transition are poorly understood. Vertical rock walls are often covered by lush, diverse communities of sessile suspension-feeding invertebrates, while adjacent horizontal substrates are dominated by algae, or corals in the tropics. Multiple factors, including light, sedimentation, water flow, and predation have been proposed to explain this pattern, but experimental tests of these hypotheses are lacking. We manipulated light level and predation to test whether variation in these mechanisms could be responsible for the shift in composition of sessile communities between vertical and horizontal surfaces in the rocky subtidal Gulf of Maine. Shaded horizontally oriented granite plots were dominated by invertebrates (e.g., ascidians, barnacles, bryozoans) after 25 months. Unshaded plots were dominated by macroalgae, which was virtually absent in shaded plots. Exclusion of grazers with cages had no effect on percent cover of invertebrates or algae. Preferential settlement of invertebrate larvae to shaded plots, due to larval behaviors such as negative phototaxis, did not seem to play a role. Shading likely affects post-settlement mortality of invertebrates by alleviating competition for space with algae, although greater abundance of micropredators in algal-dominated communities could also be important. Communities on shaded plots lacked many taxa present on natural wall communities, likely due to greater disturbance on horizontal substrates and/or lack of sufficient time for colonization of these taxa. These results suggest that light plays a key role in controlling the structure, composition, and function of shallow subtidal communities.     

Interannual variability in the spring phytoplankton bloom in Auke Bay,Alaska

Data on phytoplankton primary production, biomass, and species composition were collected during a 5 yr (1985–1989) study of Auke Bay, Alaska. The data were used to examine the interannual differences in the timing, duration, and magnitude of the spring phytoplankton blooms during each year and to relate these differences to interannual variations in weather patterns. Within any given year, a pre-bloom phase was characterized by low available light, low rates of primary production, low biomass, and predominantly small (<10µm) diatoms. During the primary bloom, integrated production rates rose to 4 to 4.5 g C m^–2 d^–1, and integrated biomass levels reached 415 to 972 mg chlorophyll m^–2. Primary blooms were usually dominated by large diatoms (Thalassiosira spp.), and in a single year (1989) byChaetoceros spp. The primary blooms terminated upon nutrient depletion in the euphotic zone. Secondary blooms, triggered by nutrient resupply from below, occurred sporadically after the primary bloom and accounted for 4 to 31% of total spring production. The date of initiation and the duration of the primary bloom varied little from year to year (standard deviation 3 and 5 d, respectively). Seasonal production rates and biomass levels varied interannually by a factor of 2 to 3. In contrast, intra-annual variations of more than an order of magnitude, especially in biomass, occurred over periods as short as 10 d. These large variations over short time periods indicate the importance of synchronous timing between spring blooms and the production of larval fish and shellfish, which depend on an appropriate and adequate food supply for growth and survival. Parameters describing primary production (e.g. peak daily production, mean daily production, and total production during the primary bloom and the entire season) exhibited little interannual variation (coefficient of variation, CV = 10 to 19%), but a large degree of intra-annual variation (CV = 77 to 116%). Similarly, interannual variations in biomass (peak chlorophyll, mean chlorophyll) were also lower (CV = 20 to 33%) than intra-annual variations (CV = 85 to 120%).     

Short-term variations in the pigment composition of a spring phytoplankton bloom from an enclosed experimental ecosystem

Phytoplankton samples taken during the spring bloom in the experimental enclosed ecosystem bags at Loch Ewe, Scotland, during 1983 were analysed for carotenoids and chlorophyll compounds using high-performance liquidchromatography (HPLC). Changes in the relative proportions of these pigments were related to day-to-day changes in the composition of the bloom and the physiological state of the algae. There is clear evidence for a change in the chlorophyllide a:chlorophyll a ratio, which reached a maximum as nutrient limitation occurred. No major qualitative changes in the carotenoid components were seen during the bloom; the relative proportion, however, of some carotenoids does provide useful information on the relative abundance of certain algal type in the phytoplankton.     

Supply of organic matter to the sediment in the northern North Sea during a spring phytoplankton bloom

Strings of moored sediment traps were deployed in a 150 m water column over a period covering the growth and collapse of the spring bloom (4 April–3 June 1976) in an area of the northern North Sea. The efficiency of collection of material in the moored traps was compared to collections in free-drifting traps in the same area of deployment. The ways in which the data from the trap collections may be interpreted was considered at some length and a best estimate of the flux of organic carbon and nitrogen to the sediment was made. For the period prior to the spring bloom (4–23 April) this flux was 50 mg C m^–2 d^–1 (about 20% of primary production). During the bloom (24 April–19 May) it was about 185 mg C m^–2 d^–1 (35% of production) and during early summer (20 May–3 June) it was 115 mg C m^–2 d^–1, about 25% of the overlying production. The organic carbon and nitrogen content of the material collected was measured and the material was examined microscopically. There was evidence of a large settlement of diatoms immediately after the spring bloom which was reflected in changes in the C:N and C:chlorophyll ratios of the material collected. This change in biochemical composition of the material may affect its nutritional quality and have a stimulatory effect on the growth and reproduction of the animals living in the sediment.     

Genetic variability in bloodworm (Glycera dibranchiata) populations in the Gulf of Maine

Genetic structure of eight Northwest Atlantic populations of the marine polychaeteGlycera dibranchiata Ehlers was examined with starch gel electrophoresis. Samples were collected during summer and fall 1981, and seven polymorphic and four monomorphic loci were consistently scored. Average heterozygosity (0.126) and percent polymorphic loci (59.3) were comparable to the averages reported for marine invertebrates. Minimum genetic distances between populations ranged from 0.003 to 0.093, levels typically associated with local populations of the same species in other taxa. Based on these data, inter- and intra-estuarine migration and gene flow appear to be low. Only two populations, separated by 13 km along the same river in New Brunswick, Canada, were not genetically different from each other. These findings may have relevance for management strategies in bloodworms.