Modem organic-walled dinoflagellate cysts in arctic marine environments and their (paleo-) environmental significance

The Arctic Ocean is one of the least known marine regions of the world. Because of its major influence on global climate and its hostile environmental conditions it is a fascinating area for paleoecological, paleoclimatic and paleoceanographic research. The composition of planktic microfossil assemblages, and both the trace-element and stable isotope compositions of hard parts, provide us with valuable information about the physical and biochemical parameters of surface waters in the high northern latitudes. Calcareous and biosiliceous microfossils that are traditionally used in Quaternary paleoenvironmental studies are of limited value in the Arctic Ocean because of their low abundances, low diversity and/or low preservation potential. The past several decades have seen considerable progress in our knowledge of the ecology and biogeography of dinoflagellates and their organic-walled cysts in the high northern latitudes, and these dinoflagellate cysts are now important proxies for reconstructing surface water conditions in the Quaternary. This arcticle gives an overview of the ecology of dinoflagellates and their cysts, the processes that transform the living communities into sediment communities, and the environmental gradients that may be reconstructed from fossil dinoflagellate cysts assemblages in the high northern latitudes.      

The (palaeo) environmental significance of modern calcareous dinoflagellate cysts: a review

Increased interest in the environmental applicability of calcareous dinoflagellate cysts for palaeo-environmental studies arose in the last two decades, when it was discovered that they constitute a widespread and abundant group within the calcareous phytoplankton. As primary producers they are directly influenced by environmental Parameters of the surrounding water masses, and therefore extremely suitable for detailed palaeo-environmental and -oceanographical reconstructions. During the last years, detailed investigations on their distribution in surface sediments of the South Atlantic Ocean, the Mediterranean Sea and the Arabian Sea were carried out, in order to reveal which environmental parameters influence their distribution. This, in turn, formed the base for palaeo-environmental and -oceanographical reconstructions. The compilation of the available data on calcareous dinoflagellate ecology, morphology, taxonomy and palaeo-environmental application presented here demonstrates their ample application potential as palaeo-environmental tools.      

Calcareous dinoflagellate cysts in surface sediments from the Mediterranean Sea: distribution patterns and influence of main environmental gradients

The distribution of calcareous dinoflagellate cysts in surface sediments from the Mediterranean Sea was quantitatively analysed. The samples contain 11 cyst species and the vegetative coccoid Thoracosphaera heimii. Cyst abundance increases towards the deeper parts of the basins and is generally higher in the eastern Mediterranean Sea. Three major distribution characteristics exist: (1) different assemblages in oceanic and neritic regions, (2) little agreement with the associations of areas studied so far like the Atlantic Ocean, and (3) a unique oceanic assemblage in the eastern Mediterranean Sea. A gradual change in cyst assemblages from the western to the eastern Mediterranean Sea was observed and statistically compared with the main environmental gradients in the upper water column. Temperature, nitrate concentration and possibly salinity appear to be the most important factors controlling cyst production. Three groups containing cysts with similar environmental preferences can be distinguished: (1) an eastern Mediterranean group related to relatively high temperature and salinity but low nitrate concentration, (2) a group of more or less consistently abundant cosmopolitan species tolerating or even preferring relatively low temperature and salinity but high nitrate concentration, and (3) a group containing species that are possibly adapted to neritic environments and have probably been transported from coastal areas into the studied regions. In contrast to other calcareous plankton, calcareous dinoflagellate cysts correlate strongly with the main environmental gradients in the Mediterranean Sea, bearing a high potential for palaeoenvironmental reconstructions.     

Paleoenvironmental change at the Danian–Selandian transition in Tunisia: Foraminifera, organic-walled dinoflagellate cyst and calcareous nannofossil records

In the present study, we document paleoenvironmental change across the Danian–Selandian transition (planktic foraminiferal interval P2–P3b; calcareous nannofossil Zone NP4, Subzones NTp6–NTp8A; 61–59 Ma) in NW Tunisia. Diversifications of Paleogene planktic foraminifera with the evolution of the muricate and photosymbiotic lineages Morozovella, Acarinina and Igorina and of the biostratigraphically important nannofossils genus Fasciculithus are recorded within this interval. The present study aims to understand early Paleogene environmental changes in the southern Tethys, by analyzing the evolution of surface-water and–to a lesser extent–seafloor conditions. Three localities were investigated: Ain Settara, Elles and El Kef, all representing outer neritic deposition in the same basin, the Tunisian Trough. Paleoenvironmental changes are explored by combining planktic foraminiferal, organic dinocyst and calcareous nannofossils assemblages and several proxy parameters (planktic/benthic ratio, numbers of planktic foraminifera per gram, peridinioid/gonyaulacoid ratio; terrestrial/marine palynomorph ratio). In addition, also some geochemical parameters (calcite content and stable isotopes) are examined. Our records indicate that the environment evolved from an initially oligotrophic, open marine, deep outer neritic setting in P2–P3a towards a shallower and nutrient-rich setting from the base of Subzone P3b. This change is seen in the foraminiferal assemblages, with the substitution of Praemurica by Morozovella among the planktic foraminifera and an upward decrease in deeper benthic taxa. Also the organic-dinocyst assemblages show a peak of peridinioid cysts (Cerodinium and Lejeunecysta). Associated to these dinocyst assemblages, the lowest occurrence of Apectodinium is recorded, which seem to have evolved in this region, possibly in response to enhanced nutrient levels on the shelf. Additionally, a distinct change in calcareous nannofossil assemblages is also described, marked by the lowest appearance of Chiasmolithus edentulus, the lowest consistent occurrence of Fasciculithus and a slight increase in near-shore taxa (essentially Pontosphaera).This project provides an accurate understanding of paleoenvironmental change across the Danian–Selandian transition in Tunisia. Especially, integrating different proxies demonstrates a paleobathymetric shallowing from the Danian to the Selandian, associated to increase surface paleoproductivity. Furthermore, the results are compared with those from other localities along the Southern Tethyan margin (Egypt and Jordan) and a more regional paleoclimatic/paleoceanographic perturbation in the Southern Tethys is suggested.     

Late Holocene variability in pelagic fish scales and dinoflagellate cysts along the west coast of Vancouver Island, NE Pacific Ocean

Fish stocks and dinoflagellates are essential components of the marine food chain. Sediment cores from a predominantly anoxic basin in Effingham Inlet, Vancouver Island, British Columbia, archive a late Holocene (500–5300 years BP) record of paleoproductivity in the North American Coastal Upwelling Domain (CUD). We present evidence that late Holocene changes in the dinoflagellate cyst assemblages, sedimentary record, and fish stocks in the northeastern Pacific Ocean fluctuated, at least partially, in accordance with regional and global climate cycles.Principal components analysis (PCA), and trend, wavelet and spectral analyses were used to identify relationships, cycles and trends in sediment grey-scale values, and the abundances of fish scales and dinoflagellate cysts on centennial to millennial time scales. Most observed cycles fluctuated in intensity over time, particularly following transition of the regional climate to a higher rainfall phase that impacted coastal oceanic dynamics 3400 ± 150 years ago. Correlation of the marine paleoproductivity records observed in Effingham Inlet with solar influenced climate proxy cycles observed in the North Atlantic region indicates that solar forcing at different scales might have influenced the climate in the northeast Pacific as well. In particular an 1100- to 1400-year cycle in regional climate is well represented in the fish productivity proxy and sedimentological record. It was also observed that colder water, high-productivity, Selenopemphix nephroides and anchovy-dominated “Anchovy Regime” ecosystems alternate with warmer water, herring-dominated “Herring Regime” ecosystems at millennial time scales. The fish scale record preserved in Effingham Inlet indicates that the NE Pacific is now in transition from an ‘anchovy-’ to a ‘herring’-dominated regime.     

Orbital signatures in a late Miocene dinoflagellate record from Crete (Greece)

A high-resolution palynological study of the cyclically bedded Faneromeni section (upper Tortonian-lower Messinian) on Crete (Greece) is presented. This study aims to recognize orbitally-driven variations in the palynological record and to validate the age model based on the astronomical calibration of the sedimentary cycles. Four palynology-based environmental proxies were utilised using interpretations of fossil dinoflagellate associations based on modern ecological characteristics. Cross-spectral analysis between the proxy records and astronomical target curve, the 65°N summer insolation, yielded in most cases significant spectral power and coherence in the precession and/or obliquity frequency bands. Precession-controlled variations in the proxy records are related to lithology and indicate that maxima in continental input and minima in sea surface salinity coincide with sapropel formation. The influence of obliquity is most clearly reflected in the index of continental versus marine palynomorphs (S-D). The absence of a distinct time lag relative to obliquity indicates that the 41-kyr component in continental input is controlled by oscillations in regional Mediterranean climate rather than by glacial cyclicity. Phase relations in the different astronomical frequency bands of the spectrum, as compared with the Mediterranean Pliocene, essentially confirm the validity of the Miocene astronomical time scale. Finally, a major non-cyclic change in the palynological assemblage at 6.68 Ma indicates enhanced salinity and decreased river discharge. This shift coincides with a significant drop in sedimentation rate informally termed the “Early Messinian Sediment starvation Event”.     

The potential of organic-walled dinoflagellate cysts for the reconstruction of past sea-surface conditions in the Southern Ocean

In this study we investigate the potential of organic-walled dinoflagellate cysts (dinocysts) as tools for quantifying past sea-surface temperatures (SST) in the Southern Ocean. For this purpose, a dinocyst reference dataset has been formed, based on 138 surface sediment samples from different circum-Antarctic environments. The dinocyst assemblages of these samples are composed of phototrophic (gonyaulacoid) and heterotrophic (protoperidinioid) species that provide a broad spectrum of palaeoenvironmental information. The relationship between the environmental parameters in the upper water column and the dinocyst distribution patterns of individual species has been established using the statistical method of Canonical Correspondence Analysis (CCA). Among the variables tested, summer SST appeared to correspond to the maximum variance represented in the dataset.To establish quantitative summer SST reconstructions, a Modern Analogue Technique (MAT) has been performed on data from three Late Quaternary dinocyst records recovered from locations adjacent to prominent oceanic fronts in the Atlantic sector of the Southern Ocean. These dinocyst time series exhibit periodic changes in the dinocyst assemblage during the last two glacial/interglacial-cycles. During glacial conditions the relative abundance of protoperidinioid cysts was highest, whereas interglacial conditions are characterised by generally lower cyst concentrations and increased relative abundance of gonyaulacoid cysts. The MAT palaeotemperature estimates show trends in summer SST changes following the global oxygen isotope signal and a strong correlation with past temperatures of the last 140 000 years based on other proxies. However, by comparing the dinocyst results to quantitative estimates of summer SSTs based on diatoms, radiolarians and foraminifer-derived stable isotope records it can be shown that in several core intervals the dinocyst-based summer SSTs appeared to be extremely high. In these intervals the dinocyst record seems to be highly influenced by selective degradation, leading to unusual temperature ranges and to unrealistic palaeotemperatures. We used the selective degradation index (kt-index) to determine those intervals that have been biased by selective degradation in order to correct the palaeotemperature estimates. We show that after correction the dinocyst based SSTs correspond reasonably well with other palaeotemperature estimates for this region, supporting the great potential of dinoflagellate cysts as a basis for quantitative palaeoenvironmental studies.     

Organic-walled dinoflagellate cysts as paleoenvironmental indicators in the Paleogene; a synopsis of concepts

The organic-walled, hypnozygotic cysts of dinoflagellates (“dinocysts”) provide a rich, albeit incomplete, history of this eukaryotic plankton group in ancient sediments. Building on pioneering studies of the late 1970s and 1980s, recent ocean drilling and more detailed, integrated studies of surface sections have provided a wealth of dino-cyst data spanning the entire Paleogene. Based on multidisciplinary approaches, these studies have been instrumental in refining existing and furnishing new concepts of Paleogene paleoenvironmental and paleoclimatic reconstructions by means of dinocysts. Since dinocysts typically exhibit high abundances in neritic settings, the dinoeyst-based environmental and paleoclimatic information is complementary to that derived from typically more offshore groups such as planktonic foraminifera, coccolithophorids, diatoms, and radiolaria. While in a recent paper we gave a broad overview of case studies from around the globe (Sluijs et al. 2005), here we focus on a summary of these analyses and present a synopsis of applied paleoecological concepts in Paleogene (65–24 ma) dinocyst studies. Representing Earth’s greenhouse-icehouse transition, this episode holds the key to the understanding of extreme transient climatic change. The present paper offers guidelines for the application of dinocyst palaeoecology to the reconstruction of Paleogene sea-surface productivity, temperature, salinity, stratification, and paleo-oxygenation as well as their application in sequence stratigraphy, oceanic circulation and general watermass reconstructions.      

Free sterol composition of species in the dinoflagellate genus Pyrocystis: a spectrum of sterol diversity

The dinoflagellate genus Pyrocystis includes a small number of marine species, which spend the majority of their life cycles as nonmotile cells within a carbohydrate sheath, and which are found ubiquitously throughout the world's oceans. The biochemistry of this model dinoflagellate genus has been widely studied due to its ability to bioluminesce. However, Pyrocystis has been comparatively understudied with respect to its lipid biochemistry, in particular that of sterols. To date, examination of the sterols of Pyrocystis has focused primarily upon Pyrocystis lunula, which produces cholesterol and 4,24-dimethyl-5α-cholestan-3β-ol as its predominant sterols, while it lacks the common dinoflagellate sterol, dinosterol. We have examined the sterol composition of the two other commercially available species of Pyrocystis, Pyrocystis fusiformis and Pyrocystis noctiluca. Pyrocystis noctiluca possesses dinosterol as its most abundant sterol, while P. fusiformis possesses dinosterol and 4,24-dimethyl-5α-cholestan-3β-ol as the predominant sterols, placing it at an intermediate position between P. lunula and P. noctiluca, as based on sterol composition. The potential limitations of the dinoflagellate sterol biomarker dinosterol are also explored in this study due to its notable absence in P. lunula.     

X-ray microanalysis of unfixed chromatin in dinoflagellate cells prepared by a monolayer cryotechnique

The fine structural appearance and elemental composition of unfixed chromatin is described for cells of the dinoflagellate Prorocentru micans prepared by a freeze-drying technique. This involves rapid freezing, cryo-dehydration and resin infiltration of a monolayer of cells dispersed over a resin base.The fine structure of the nucleus appears quite different from chemically fixed and dehydrated cells. In stained sections, the chromosomes are seen as pale areas containing diffuse chromatin, and are surrounded by electron-dense nucleoplasm which has a reticulate substructure.X-ray microanalysis reveals the presence of high levels of chromatin-associated Ca and transition metals Fe, Ni, Cu and Zn, in accordance with previous observations on chemically processed cells. Calculation of elemental mass fractions by on-line computer demonstrates an overall ratio of one divalent cation per two phosphorus groups (or per two nucleotides). This ratio is similar to that obtained previously for chemically fixed chromatin, and shows that the precise overall association of metals is not primarily determined by the process of fixation.     

Dinoflagellate cysts as indicators of water quality and productivity in British Columbia estuarine environments

Palynological analyses of 60 surface sediment samples from estuarine environments near Vancouver Island, including the Georgia Strait (GS), the Effingham (EFF) and the Seymour–Belize (SB) Inlets were performed in order to document the distribution of dinoflagellate cyst assemblages and their relationship to hydrographic conditions, productivity and nutrient concentrations. We tested transfer functions using the analogue method, and suggest that dinoflagellate cyst assemblages can be used to reconstruct primary productivity, temperature and salinity. The EFF and SB Inlets are characterized by a dominance of autotrophic taxa, particularly Operculodinium centrocarpum, whereas the Protoperidinioid and gymnodinial heterotrophic taxa such as Quinquecuspis concreta and Brigantedinium spp. dominate the assemblages of the GS. Multivariate analysis shows that this distribution is closely linked to primary productivity, sea-surface temperature (SST) and spring silica concentration. The abundance of autotrophic taxa in the EFF and SB Inlets is associated with high primary productivity and low summer SST, indicating summer upwelling of coastal British Columbia, whereas the heterotrophic taxa that characterizes the GS assemblages are related to low productivity, high summer SST and high silica concentration during spring. Multivariate analysis shows that the most important environmental parameters related to dinocyst distribution in the restricted embayment of the GS, are distance to the shore, distance to Vancouver Harbor, spring sea surface salinity (SSS), spring phosphate concentration and spring productivity. The autotrophic taxa are generally more common in coastal and shallow waters, but Spiniferites ramosus and Pentapharsodinium dalei show an opposite correlation to spring productivity and salinity. P. dalei is particularly abundant around Vancouver Harbor, near highly urbanized shores and within the Fraser River plume, where salinity is low and spring productivity and continental runoff are high. S. ramosus shows its highest abundance on the western coast of GS. Protoperidinioid and gymnodinial cysts characterize distal zones within the central and southern GS that are associated with a mixture of brackish waters coming from the Fraser River and deep upwelling waters entering the GS via Juan de Fuca Strait. The relationship between dinoflagellate cyst assemblages and primary productivity in these estuarine systems differs from that in oceanic and outer neritic zones, where the abundance of heterotrophic taxa is commonly associated with upwelling and high productivity.     

Calcareous dinoflagellate cyst distributions in surface sediments from upwelling areas off NW Africa, and their relationships with environmental parameters of the upper water column

Only very few studies have focussed on the spatial distribution and ecology of calcareous dinoflagellate cysts (dinocysts) in upwelling areas. Here, distributions of individual calcareous dinocyst species in surface sediment samples from the coastal upwelling zone off NW Africa and their relationships with known environmental parameters of the (sub-)surface waters have been analysed in order to enhance our knowledge on their modern distribution patterns and to determine the ecological significance and palaeoenvironmental reconstruction potential of each calcareous dinocyst species within this exemplary high-productivity region. In addition to calculating relative cyst abundances, well-constrained sedimentation rates have allowed the calculation of dinocyst accumulation rates (cysts cm^− 2 ka^− 1) for most of the surface sample positions, thus providing a much more accurate estimation of actual calcareous dinocyst production in the upper water column than could be warranted in similar studies so far. Distinct differences in the geographic distribution patterns of nine species were observed. In general, high accumulation rates of calcareous dinocysts were found around and south of 29°N and offshore the westernmost Canary Island La Palma, with slightly lower accumulation rates in the upwelling-influenced areas off Cape Yubi and in the upwelling filament area off Cape Ghir. Multivariate ordination techniques were applied in order to compare the cyst accumulation rates of individual species with physical parameters (temperature, salinity, density, mixed layer depth) and the trophic state (nitrate, phosphate and chlorophyll concentrations) of the overlying (sub-)surface waters. All species were found to relate significantly to one or more of the environmental parameters, partly confirming previous results on cyst ecology but also providing new information which will be useful for future palaeoenvironmental reconstructions within upwelling areas.     

Growth inhibition of dinoflagellate algae in shake flasks: Not due to shear this time!

Large scale algae cultures present interesting challenges in that they exhibit characteristics of typical bacterial and animal cell cultures. One current commercial food additive, docosahexaenoic acid (DHA), is produced using the dinoflagellate algae, Crypthecodinium cohnii. Like animal cell culture, the perceived sensitivity of algae culture to hydrodynamic forces has potentially limited the agitation and aeration applied to these systems. However, the high density cultivation of C. cohnii required for an economically feasible process inevitably results in high oxygen demand. In this study, we demonstrated what first appeared to be a problem with shear sensitivity in shake flasks is most probably a mass transfer limitation. We subsequently demonstrated the limit of chronic and rapid energy dissipation rate, EDR, that C. cohnii cells can experience. This limit was determined using a microfluidic device connected in a recirculation loop to a stirred tank bioreactor, which has been previously used to repeatedly expose animal cells to high levels of EDR. Inhibition of cell growth was observed when C. cohnii cells were subjected to an EDR of 5.9 × 10⁶ W/m³ with an average frequency of 0.2/min or more. This level of EDR is sufficiently high that C. cohnii can withstand typically encountered hydrodynamic forces in bioprocesses. This result suggests that at least one dinoflagellate algae, C. cohnii, is quite robust with respect to hydrodynamic forces and the scale‐up of process using this type of algae should be more concerned with providing sufficient gas transfer given the relatively high oxygen demand. © 2009 American Institute of Chemical Engineers Biotechnol. Prog., 2010     

Persufflation (or gaseous oxygen perfusion) as a method of organ preservation

Improved preservation techniques have the potential to improve transplant outcomes by better maintaining donor organ quality and by making more organs available for allotransplantation. Persufflation, (PSF, gaseous oxygen perfusion) is potentially one such technique that has been studied for over a century in a variety of tissues, but has yet to gain wide acceptance for a number of reasons. A principal barrier is the perception that ex vivo PSF will cause in vivo embolization post-transplant. This review summarizes the extensive published work on heart, liver, kidney, small intestine and pancreas PSF, discusses the differences between anterograde and retrograde PSF, and between PSF and other conventional methods of organ preservation (static cold storage, hypothermic machine perfusion). Prospective implications of PSF within the broader field of organ transplantation, and in the specific application with pancreatic islet isolation and transplant are also discussed. Finally, key issues that need to be addressed before PSF becomes a more widely utilized preservation strategy are summarized and discussed.     

Late Quaternary Protoperidinium cysts as indicators of paleoproductivity in the northern Arabian Sea

The reliability of organic-walled cysts of the heterotrophic dinoflagellate Protoperidinium as paleoproductivity indicators and the influence of bottom water oxygenation on cyst preservation is assessed by using Arabian Sea records of the past 125 kyr as a natural laboratory. Multidisciplinary geochemical, micropaleontological and palynological datasets are integrated to analyze the relationship between Protoperidinium cyst concentrations and other paleoproductivity proxies. Differential preservation potential is quantified in order to establish threshold oxidative degradation values for a possible application of quantitative Protoperidinium cyst records in paleoenvironmental reconstructions. Results indicate that variations in Protoperidinium cyst concentration closely correspond to other marine productivity and/or upwelling proxies. Although oxygenation will lead to significant cyst degradation, and thus decreased concentrations, down-core patterns in Protoperidinium cyst concentration still primarily reflect changes in sea surface productivity. In view of differential preservation among dinoflagellate cysts, down-core variations in relative abundance of Protoperidinium should be treated with caution.     

Shear-induced changes in membrane fluidity during culture of a fragile dinoflagellate microalga

The commonly used shear protective agent Pluronic F68 (PF68) was toxic to the marine dinoflagellate microalga Protoceratium reticulatum, but had a shear-protective effect on it at concentrations of ≤ 0.5 g L(-1) . Supplementation of P. reticulatum cultures with PF68 actually increased the fluidity of the cell membrane; therefore, the shear protective effect of PF68 could not be ascribed to reduced membrane fluidity, an explanation that has been commonly used in relation to its shear protective effect on animal cells. Data are reported on the membrane fluidity of P. reticulatum and its response to the presence of PF68 under sublethal and lethal turbulence regimens. The membrane fluidity was found to depend strongly on the level of lipoperoxides in the cells produced under lethal agitation.     

Nitrification rates in a saline medium at different dissolved oxygen concentrations

A kinetic study was carried out in a saline medium to assess the effect of O₂ on the two-step nitrification process: for the first nitritation step, 2–26 mg dissolved O₂ (DO) l^–1 was used and for the second nitratation step, 0.5–24 mg DO l^–1 was used. Nitritation rate was measured in the presence of sodium azide so as to inhibit nitratation. Ammonia-oxidizing (AOB) and nitrite-oxidizing (NOB) bacterial in the mixed culture were determined by 16 S rRNA hybridization. The affinity constants for oxygen O₂ of the AOB and the NOB were 1.66 mg O₂ l^–1 and 3 mg O₂ l^–1 respectively. The larger than the previously reported values of these constants might be due to the high salt content in the medium. High O₂ concentrations did inhibit the nitrification rate.     

The effects of different oxygen regimes on the feeding and vertical distribution of Nephelopsis obscura (Hirudinoidea)

The feeding rates and vertical distribution of the freshwater leech Nephelopsis obscura, fed on different densities of third instar Chironomus riparius, were determined in the laboratory at three different constant dissolved oxygen regimes (10%, 100%, 300% saturation) at 15 °C. The rate of feeding increased linearly with prey density up to maximal field prey densities, with no satiation response. Analysis of covariance showed that the rate (slope) at which prey were consumed was not significantly different among oxygen regimes but the amount eaten at any given prey density was higher in higher dissolved oxygen saturations. Analysis of the vertical distribution of N. obscura at different oxygen saturations and prey densities showed a higher proportion of N. obscura on or in the mud substrate compared to the water column at 100% and 300%. No correlation was found between prey density and the vertical distribution of N. obscura, but the numbers of prey eaten were correlated with the proportion of N. obscura on the mud substrate. These results indicate that higher percentage dissolved oxygen regimes increase the feeding of N. obscura and are of potential importance in explaining the seasonal depth distribution and microdistribution patterns recorded for N. obscura.