Phosphorus metabolism of oceanic dinoflagellates: phosphate uptake,chemical composition and growth of Pyrocystis noctiluca

The phosphorus metabolism of Pyrocystis noctiluca Murray (Schuett) 1886 has characteristics which may enhance its potential for success in orthophosphate impoverished waters. The steady-state phosphate uptake rates were equal in the light and dark, and were directly proportional to both the phosphorus cell quota and the cell division rate. In contrast, nutrient-saturated uptake rates were multiphasic, faster in the light than the dark, 2 to 4 orders of magnitude greater than steady-state rates, and were inversely proportional to both the phosphorus cell quota and the cell division rate. These uptake characteristics suggest that P. noctiluca may take up phosphate coincidently at their typically low ambient concentrations as well as to exploit episodic nutrient events in nature. Cell division rates were a hyperbolic function of the ambient orthophosphate concentration. The shortest doubling time was 8.7 d, the phosphate concentration at half the maximum division rate was 0.15 M and the threshold, concentration for cell division was ca 0.05 M PO ₄ ^3- . Division rates of P. noctiluca in the ocean are much faster than predicted from the measured ambient orthophosphate concentrations. Since this dinoflagellate has high naturally occurring alkaline phosphatase activities, and can utilize organic-P compounds, we suggest that organic-P can be as important as orthophosphate in supporting the observed division rates of P. noctiluca in the sea.     

Characterization of alkaline phosphatase and organic phosphorous utilization in the oceanic dinoflagellate Pyrocystis noctiluca

Phosphate depleted Pyrocystis noctiluca (Murray) Schuett 1895 has at least one phosphomonoesterase (EC 3:1:3:1) which is triphasic between 0.1 and 222 mol P. The enzyme has a broad temperature range with maximum activity at 50 °C and a Q₁₀ of 1.4 to 1.5. A break in the Arrhenius plot at 35 °C implies the enzyme is membrane-bound. Cytological staining of whole cells and cell fractionation studies (showing 26 times higher specific activity in the particulate compared with the cytoplasmic fraction) suggest the enzyme is plasmalemma-bound. The enzyme has an absolute metal requirement which would be satisfied by Mg⁺⁺ but not Mn⁺⁺, Zn⁺⁺, Fe⁺⁺, or Co⁺⁺ at seawater concentrations. Alkaline phosphatase is a stable enzyme whose activity is not altered by inhibitors of protein synthesis. Orthophosphate inhibition of enzyme activity was largely eliminated in the presence of these inhibitors. Apparently, a protein induced by PO₄ ^3-, rather than PO₄ ^3- itself, inhibits alkaline phosphatase. Cell-free alkaline phosphatase can hydrolyze a variety of phosphate esters and linear polymers of inorganic phosphorus as well as disolved organic phosphorus from tropical oceanic waters. These same hydrolysable organic and inorganic phosphorus compounds support the axenic culture growth of P. noctiluca, suggesting that naturally occurring hydrolysable organic phosphorus compounds may also support the growth of this alga.     

Cell-wall morphology correlated with vertical migration in the non-motile marine dinoflagellate Pyrocystis noctiluca

 We report an ultrastructural study of the morphological changes in cells of the marine dinoflagellate Pyrocystis noctiluca Murray, which correlate with its vertical migration pattern. Cells alternate between a large, highly vacuolated, positively buoyant, vegetative cyst surrounded by a dinosporin-containing wall and a smaller, more compact, negatively buoyant, cellulose-bounded cell. The cyst wall is composed of two layers: a thin smooth outer layer, thought to be composed of dinosporin, and a thick inner layer that likely to be cellulosic. One or two thecate cells are formed from within the cysts. Thecate cells are smaller, more compact and contain many small translucent bodies. They are surrounded by a typical dinoflagellate amphiesmal layer composed of membranes and cellulose plates. The amphiesmal layer appears only in recently divided cells and exists for only one night. By the following day, the cellulose wall has been replaced by a new dinosporin wall synthesized from beneath the cellulose thecal layer. The cyst stage is suggested as being optimized for photosynthesis, whereas the compact, negatively buoyant, thecate form is thought to allow nutrient uptake in deeper waters. Vertical migration in this species is thus correlated with the presence of dinosporin wall during most of its stay in the upper waters, alternating with a brief thecate wall in deeper nutrient-rich waters. This is the first report correlating dinoflagellate vertical migration with changes in cell-wall composition. Received: 28 July 1999 / Accepted: 8 May 2000     

Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll–protein complexes to different photon-flux densities

The response of chlorophyll–protein complexes to super- and sub-saturating photon-flux densities, PFD (250?μmol quanta m^?2?s^?1 and 40?μmol quanta m^?2?s^?1, respectively) were analyzed for Symbiodinium microadriaticum Freudenthal, the symbiont of the Caribbean jellyfish Cassiopeia xamachana; S. kawagutii Trench and Blank, the symbiont of the Indo-Pacific scleractinian Montipora verrucosa; and S. pilosum Trench and Blank, the symbiont of the Carribbean zoanthid Zoanthus sociatus. The results indicate that each species exhibits a quantitatively distinct chlorophyll (chl) a distribution among its chl–protein complexes when cultured under standardized high and low light conditions. In response to sub-saturating PFD, the three species differentially increased the cellular concentrations of most of the chl–protein complexes. Increases in P₇₀₀ (reaction center of Photosystem I) under sub-saturating PFD correlate with an increase in the cellular concentrations of the Photosystem I-enriched complexes. Similarly, increases in photosynthetic unit (PSU) size correlate with an increase in the cellular concentrations of the water-soluble peridinin–chl-a–protein (PCP) complexes and the membrane-bound chl a–chl c ₂–peridinin–protein (acpPC) complexes, which together represent the light-harvesting components of this group. In S. microadriaticum, acclimation to sub-saturating PFD uniquely includes the preferential enrichment of the dimeric form of PCP. Under super-saturating PFD, an enrichment in photo-protective xanthophylls was detected in acpPC from S. microadriaticum and S. pilosum, but not from S. kawagutii. Each species demonstrated a characteristic photo-acclimatory response which correlates with its distribution as endosymbiont in nature, supporting the concept that different species of symbiotic dinoflagellates are adapted (sensu Björkman 1981) to different photic environments. The study was conducted between May 1992 and November 1994.     

Growth and herbivory by heterotrophic dinoflagellates in the Southern Ocean,studied by microcosm experiments

Growth and herbivory of heterotrophic dinoflagellates (Gymnodinium sp.) from the Weddell Sea and the Weddell/Scotia Confluence were studied in 1988 in 100-liter microcosms. The microcosms were screened through 200-µm or 20-µm mesh nets and incubated for 12 d at 1 °C under artificial light. Mean cell volume of dinoflagellates was 1 000 to 1 500µm³, and that of their phytoplankton prey 360 to 430µm³. Dinoflagellate growth rate followed a Holling type II functional response, with a maximum growth rate of 0.3 d^–1 and half-saturation food concentrations of 1.0µg chlorophylla l^–1, 50µg C l^–1, or 1 500 cells ml^–1. Carbon budgets based on¹⁴CO₂ assimilation and biomasses of phytoplankton and heterotrophic dinoflagellates suggested a balance between phytoplankton grazing loss and dinoflagellate consumption, assuming a dinoflagellate carbon conversion efficiency of 40%. Applying this to the functional response yielded estimates of maximum ingestion rate (0.8µg Cµg^–1 C d^–1, or 6 pg C dinoflagellate^–1 h^–1) and maximum clearance (0.8 to 1.2 × 10⁵ body volumes h^–1, or 80 to 120 nl ind.^–1 h^–1). The microcosm experiments suggested that heterotrophic dinoflagellates may contribute significantly to maintenance of low phytoplankton biomass in the Southern Ocean.     

Vertical habitat-partitioning by copepodites and adults of subtropical oceanic copepods

Vertical distributions of the abundant larger copepods, both adults and late copepodites, were observed day and night in the upper 500 m of the North Pacific central gyre in early November, 1971. Densities of the copepodites usually equalled or exceeded those of the adults. Copepod species with maximum densities at or above 100 m (Calanus spp., Nannocalanus minor f. major, Undinula darwini, and Euchaeta rimana) usually had no ontogenetic or diel migration. Neocalanus spp. and Haloptilus longicornis exhibited ontogenetic but not diel migrations. Nannocalanus minor f. minor, Aetideus acutus, Euchaeta media, Scolecithrix spp. and Pleuromamma spp., had both ontogenetic and diel migrations. Adults and copepodites of E. media and Pleuromamma spp. usually had their night modes at the same depth, but the daytime modes were at progressively deeper depths for progressively older stages. Daytime modes for adults and copepodites of A. acutus and Scolecithrix bradyi were at the same depth, but the nighttime modes were at shallower depths for progressively older stages. Night modes of all these migrators were usually in the mixed layer (75 m), where primary production rates were maximal. Congeners usually had similar migratory behavior, but competition probably has been a significant determinant of vertical distribution, since congeners, particularly sibling species, consistently had different depths of maximum occurrence during both day and night.     

Variation among congeneric dinoflagellates from the northeastern United States and Canada

Relationships among dinoflagellates of the genus Alexandrium (=Protogonyaulax) from Long Island, New England, USA, and northeastern Canada were investigated between 1983 and 1987 using enzyme electrophoresis. A relative lack of heterogeneity among toxic isolates was observed despite large geographic separations of source populations. This observation is in marked contrast to observations on toxic members of this genus from the west coast of Canada and the United States. These different enzyme variability patterns support the proposal that dispersal of toxic strains in the east from a common source has occurred recently, presumably from established populations in northern Maine, USA, or Canada. Non-toxic strains from the study area were only distantly related to toxic isolates, consistent with their different morphology and separate species designations. One non-toxic isolate from a different region, that is conspecific with a number of the toxic strains, was more similar to these isolates than to other non-toxic clones.     

Biogeography of toxic dinoflagellates in the genusAlexandrium from the northeastern United States and Canada

Twenty-eight strains of toxic dinoflagellates in the genusAlexandrium from the northeastern United States and Canada were characterized on the basis of morphology, bioluminescence capacity, mating compatibility, and toxin composition. The distributions of these characters were evaluated in the context of regional patterns of paralytic shellfish poisoning (PSP) and coastal hydrography. Two morphospecies were identified-A. tamarense Lebour andA. fundyense Balech. The two are interspersed geographically though there are areas, such as the Gulf of Maine, where apparently onlyA. fundyense occurs. Southern waters (Cape Cod, Connecticut, and Long Island) have especially diverse populations. The two species are sexually compatible. Virtually all northern isolates are bioluminescent, whereas southern isolates include bioluminescent and non-bioluminescent strains. Cluster analyses, based on high performance liquid chromatography (HPLC) determinations of the suite of toxins produced by each isolate, revealed two and perhaps three distinct groups. One is comprised almost exclusively of northern strains, and the other of southern strains. A Cape Cod cluster may be separable from the southern group. These analyses explain a previously reported north-to-south trend of decreasing toxicity, as the northern isolates produce greater proportions of the more potent toxins than do southern forms. The overall perspective is that the biogeography of toxicAlexandrium spp. in the study region is not that of a single, widespread, homogeneous population, but rather is comprised of several sub-populations, each with its own physiological characteristics and history. Two scenarios are considered with respect to this regional biogeography. The first invokes recent and continuing dispersal of isolates to the south from a center of origin in the north, followed by recombination and strong selection. The second holds that the northern and southern populations diverged from a common ancestor (vicariance), but now represent localized populations with little mixing of genotypes. Neither hypothesis can be completely refuted by the data presented here, though the weight of the evidence favors the latter. The correct scenario may be a combination of both, with recent and continuous speading occuring within the Gulf of Maine and perphaps the Gulf of St. Laerence, but with endemic localized populations persisting without genetic exchange in most southern locations. These data also indicate that although morphological criteria separate toxicAlexandrim isolates from the study region into two morphospecies, these assignments do not coincide with clusterings based on toxin composition or allozyme electrophoresis, and they are further violated by mating results. A revision of taxon designations to the varietal level could be justified.     

Stable isotope and biochemical fractionation in the marine pelagic food chain: the jellyfish Pelagia noctiluca and net zooplankton

In our field study we analyzed the C and H isotopic and biochemical (C, N, P, protein, lipid, carbohydrate) composition of the jellyfish Pelagia noctiluca (collected from the Gulf of Trieste in 1985 to 1986) and its presumed diet-net zooplankton. The mean ¹³C (-18.8) and D (-58.4) ratios of P. noctiluca showed enrichment in heavy isotopes relative to net zooplankton (2 for carbon and 30 for hydrogen). Both the jellyfish and net zooplankton were characterized by a linear correlation between ¹³C and D. C. N, P, protein, lipid, and carbohydrate contents of P. noctiluca were low on a dry weight basis as compared to net zooplankton. Significantly lower C:N and C:P ratios were found in jellyfish indicating a greater loss of carbon relative to nitrogen and phosphorus along the passage to a higher trophic level. Isotopic and biochemical evidence indicate that, though collected in nearshore waters, P. noctiluca depended on autochthonous marine organic matter.     

On the role of physical modelling in atmospheric and oceanic forecast

We discuss how physical modelling can be used to reproduce atmospheric or oceanic flows in the laboratory. The similarity conditions for the effects of density stratification and Earth rotation are first presented. Then examples of results obtained on the large ‘Coriolis’ platform in Grenoble are described. These include topographic wakes in a stratified fluid and gravity currents. Physical modelling is not used to get direct results of practical relevance, but rather to test numerical models on specific processes of environmental flows. Therefore it must be performed in close relationship with theory and numerical modelling, using advanced measurement and data assimilation techniques.     

Toxic dinoflagellates (Alexandrium fundyense and A. catenella) have minimal apparent effects on oyster hemocytes

The possible effect of Alexandrium spp. containing paralytic shellfish poisoning (PSP) toxins on the hemocytes of oysters was tested experimentally. In one trial, eastern oysters, Crassostrea virginica Gmelin, were exposed to bloom concentrations of the sympatric dinoflagellate, Alexandrium fundyense Balech, alone and in a mixture with a non-toxic diatom, Thalassiosira weissflogii (Grun) Fryxell et Hasle. Subsequently, another experiment exposed Pacific oysters, Crassostrea gigas Thunberg, to a mixed suspension of the sympatric, toxic species Alexandrium catenella (Whedon et Kofoid) Balech, with T. weissflogii. Measurements of numbers of oyster hemocytes, percentages of different cell types, and functions (phagocytosis, reactive oxygen species (ROS) production, and mortality) were made using flow-cytometry. During and after exposure, almost no significant effects of Alexandrium spp. upon hemocyte numbers, morphology, or functions were detected, despite observations of adductor-muscle paralysis in C. virginica and measured toxin accumulation in C. gigas. The only significant correlation found was between toxin accumulation at one temperature and higher numbers of circulating live and dead hemocytes in C. gigas. The PSP toxins are known to interfere specifically with sodium-channel function; therefore, the finding that the toxins had no effect on measured hemocyte functions suggests that sodium-channel physiology is not important in these hemocyte functions. Finally, because oysters were exposed to the living algae, not purified toxins, there was no evidence of bioactive compounds other than PSP toxins affecting hemocytes in the two species of Alexandrium studied.     

Asymmetric genetic exchange in the brown seaweed Sargassum fusiforme (Phaeophyceae) driven by oceanic currents

Geological phenomena (e.g. drastic sea level fluctuations during the Quaternary Ice Age in the Northern Hemisphere) have been demonstrated to intensively affect the biogeographic patterns and tempo-spatial compositions of genetic diversity of marine organisms. However, it is poorly understood whether contemporary factors such as oceanic surface currents have also shaped inter-regional population genetics of specific coastal marine flora, with or without limited dispersal capability. In this study, we determined mtDNA Cox1 gene sequences of the brown seaweed Sargassum fusiforme from nine populations along the Chinese coast and one population from the west coast of South Korea, in an effort to understand what factors are contributing to their current genetic structure and geographic distribution patterns. Genetic analyses indicated a deep genetic break between the Yellow-Bohai Sea (YBS) and the other two marginal seas, the East China Sea (ECS) and the South China Sea (SCS). In particular, the amount of genetic exchange from the SCS to each of the ECS and YBS was significantly higher than that from the opposite directions. Our analyses supports the hypothesis that biogeographic patterns of genetic variation in S. fusiforme are probably an interactive consequence of post-glacial colonization from two scattered refugia driven by the offshore Kuroshio Current and asymmetric gene flow among adjacent sea margins.     

Onset of symbiosis and distribution patterns of symbiotic dinoflagellates in the larvae of scleractinian corals

The establishment of symbiosis in early developmental stages is important for reef-building corals because of the need for photosynthetically derived nutrition. Corals spawn eggs and sperm, or brood planula larvae and shed them into the water. Some coral eggs or planulae directly inherit symbiotic dinoflagellates (Symbiodinium spp.) from their parents, while others acquire them at each generation. In most species examined to date, the larvae without dinoflagellates (aposymbiotic larvae) can acquire symbionts during the larval stage, but little is known regarding the timing and detailed process of the onset of symbiosis. We examined larval uptake of symbiotic dinoflagellates in nine species of scleractinian corals, the onset of symbiosis through the early larval stages, and the distribution pattern of symbionts within the larval host, while living and with histology, of two acroporid corals under laboratory conditions. The larvae acquired symbiotic dinoflagellates during the planktonic phase in all corals examined which included Acropora digitifera, A. florida, A. intermedia, A. tenuis, Isopora palifera, Favia pallida, F. lizardensis, Pseudosiderastrea tayamai, and Ctenactis echinata. The larvae of A. digitifera and A. tenuis first acquired symbionts 6 and 5 days after fertilization, respectively. In A. digitifera larvae, this coincided with the formation of an oral pore and coelenteron. The number of symbiotic dinoflagellates increased over the experimental periods in both species. To test the hypothesis that nutrients promotes symbiotic uptake, the number of incorporated dinoflagellates was compared in the presence and absence of homogenized Artemia sp. A likelihood ratio test assuming a log-linear model indicated that Artemia sp. had a significantly positive effect on symbiont acquisition. These results suggest that the acquisition of symbiotic dinoflagellates during larval stages is in common with many coral species, and that the development of both a mouth and coelenteron play important roles in symbiont acquisition.     

Separation of the two Atlantic species of Pomatoceros,P. lamarckii and P. triqueter (Annelida: Serpulidae) by means of biochemical genetics

In order to confirm the status of two proposed species of the serpulid Pomatoceros, the electrophoretic mobilities of 13 enzymes encoded at 19 loci in P. lamarckii (Quatrefages) and P. triqueter (L.) were compared using horizontal starch gel electrophoresis. The serpulids were sampled from Menai Bridge (North Wales), Plymouth (England) and the Isle of Man in the winter of 1981/1982. Six loci were monomorphic or nearly so and showed no useful or significant difference between species. At a further 7 loci, some of the allozymes common to both species were present, though usually at significantly different frquencies, while others were species-specific. The remaining 6 loci presented species-specific allozymes. In P. lamarckii, 61% of the loci were polymorphic compared with 50% in P. triqueter. The mean observed heterozygosity was 0.169 for P. lamarckii and 0.208 for P. triqueter. Calculation of genetic distance and identity gave values of 0.821 and 0.440, respectively. This study, therefore, confirms the existence of two separate species of Pomatoceros as has been previously proposed on the basis of opercular structure and supported by ecological separation where these species occur sympatrically.     

Vertical distributions and photosynthetic action spectre of two oceanic picophytopianlcters,Prochlorococcus marinus andSynechococcus sp.

Two picophytoplankters,Prochlorococcus marinus andSynechococcus sp., were isolated from the bottom of the euphotic zone (150 m depth) in the western Pacifie Ocean. The concentration ofP. marinus at this depth was more than 10⁴ cells ml^–1 while that ofSynechococcus sp. was less than 10² cells ml^–1. TheP. marinus isolate has a high divinyl-chlorophylla:b ratio similar to that of the Mediterranean strain, while theSynechococcus sp. isolate is of the phycourobilinrich type. The growth rate ofP. marinus was higher thanSynechococcus sp. when both were cultured under weak blue-green to blue-violet light (ca. 2 E m^–2 s^–1). While the chlorophyll-specific absorption spectra showed higher values inSynechococcus sp., the photosynthetic action spectre revealed thatP. marinus was able to use blue-violet light, whereasSynechococcus sp. was able to use blue-green light, more efficiently for photosynthesis. The photosynthetic quantum yield ofP. marinus was higher than that ofSynechococcus sp. at any wavelength between 400 and 700 nm. The calculated in situ photosynthesis rates per Gell volume forP. marinus were estimated to be higher than forSynechococcus sp. at 50 and 150 m depth. These results indicate thatP. marinus photosynthetically surpassesSynechococcus sp. in the blue-light-rieh environment of the oceanic euphotic zone. This may be why the former predominates at depths in temperate to tropical open ocean waters.     

The interaction between reproductive cost and individual quality is mediated by oceanic conditions in a long-lived bird

Environmental variability, costs of reproduction, and heterogeneity in individual quality are three important sources of the temporal and interindividual variations in vital rates of wild populations. Based on an 18-year monitoring of an endangered, recently described, long-lived seabird, Monteiro's Storm-Petrel (Oceanodroma monteiroi), we designed multistate survival models to separate the effects of the reproductive cost (breeders vs. nonbreeders) and individual quality (successful vs. unsuccessful breeders) in relation to temporally variable demographic and oceanographic properties. The analysis revealed a gradient of individual quality from nonbreeders, to unsuccessful breeders, to successful breeders. The survival rates of unsuccessful breeders (0.90 +/- 0.023, mean +/- SE) tended to decrease in years of high average breeding success and were more sensitive to oceanographic variation than those of both (high-quality) successful breeders (0.97 +/- 0.015) and (low-quality) nonbreeders (0.83 +/- 0.028). Overall, our results indicate that reproductive costs act on individuals of intermediate quality and are mediated by environmental harshness.     

Cessation of hole-digging by the crab Helograpsus haswellianus: A resource-conserving adaptation

Cases where the mud crab Helograpsus haswellianus (Whitelegge) have dug too many holes and collapsed the mud surface are not observed in the field. Experiments have shown that there is a specific density of holes above which the mud collapses. H. haswellianus at different densities in closed cages do not dig holes over this density. Instead, two or more individuals occupy existing holes on a short-term basis. The significance of this behaviour is discussed.     

Weight and chemical composition of some important oceanic zooplankton in the North Pacific Ocean

Wet and dry weight, total carbon, nitrogen, hydrogen, and ash contents were determined on 33 species of zooplankton distributed predominantly in the open sea region of the North Pacific. Sampling covered the waters from 44°N to the equator. Average percentage of dry weight to wet weight was about 19% of all samples from the whole area. Percentage dry weight of carbon in copepods was on an average 51.5%. The highest value, 66.6%, was obtained in eggs of the copepod Pareuchaeta sarsi. Mixed zooplankton was assumed to contain carbon comprising about 35 to 45% of the dry weight. Carbon contained in the zooplankton biomass existing in the upper 200 m in the western parts of the northern North Pacific and Bering Sea during spring and summer was estimated to range from 20 to 85 mg C/m³. Nitrogen content varied considerably with localities. Average ratio of carbon to nitrogen was 8.5 in subarctic copepods, and 4.1 in subtropic-tropic copepods. This ratio also varied with season. In the copepod Calanus cristatus the ratio was highest (10.0) in May, immediately after the spring bloom of phytoplankton, when the animals contained much fat. The ratio fell to 5.1 in December. There seemed to be a large seasonal variation in boreal zooplankton due to great fluctuations of environmental conditions, especially the amount of food available; in tropical species the range was small because of environmental uniformity. Average hydrogen content was about 6 to 10%. The percentage of ash to dry weight amounted to 39.3% in pteropods and 3.4% in copepods.