Roger P. Harris

Genetic and physiological influences on the alkenone/alkenoate versus growth temperature relationship in Emiliania huxleyi and Gephyrocapsa oceanica

Selected warm and cold water strains of the coccolithophorid Emiliania huxleyi and the closely related species Gephyrocapsa oceanica were cultured under controlled temperature conditions to assess genetic and physiological variability in the alkenone/alkenoate vs. temperature relationship. Differences in the strains’ growth rates over the 6–30°C experimental temperature range were small but consistent with their cold or warm water origins. E. huxleyi and G. oceanica had similar alkenone/alkenoate biochemistry, justifying the extension of alkenone stratigraphy to sediments predating the appearance of E. huxleyi. These species could not be distinguished by C38/C37 alkenone or alkenoate/alkenone ratios as previously suggested (Volkman et al. 1995; Sawada et al. 1996) but given samples from a range of temperatures may be distinguished by a plot of the C38 ethyl vs. C38 methyl unsaturation ratios (U38EtK and U38MeK, respectively). Biochemical responses to temperature and the C37 alkenone-based (U37K′) temperature calibrations differed significantly among the strains. The U37K′ temperature calibration was nonlinear for five of the six strains examined. A reduction in slope of the calibration at temperatures 21°C suggests the cell’s alkenone-based adaptation to temperature is limited at the extremes of its growth temperature range. The unsaturation ratios of the C38 methyl and ethyl alkenones (U38MeK and U38EtK) varied similarly with temperature and were strongly intercorrelated. The experiments also documented an influence of cell physiological state on both alkenone and alkenoate composition and on alkenone unsaturation. Cells in late logarithmic and stationary growth had significantly increased abundance of alkenoates and C38 ethyl alkenones relative to C38 methyl alkenone abundance. In some strains the unsaturation ratios of both C37 and C38 alkenones also significantly decreased when cells entered the late log phase. Comparison of culture results with field data indicates that the average physiological state of alkenone-synthesizers in the open ocean differs from cultured cells growing under exponential growth and appears to be more similar to cells in late log or stationary growth phases. Differences in alkenone/alkenoate ratios between cultured cells and sediments underlying waters of a similar temperature most probably reflect a difference in cell physiology between cultured cells and oceanic populations and not greater diagenetic losses of alkenones relative to alkenoates, as previously suggested (Prahl et al. 1995). Our experiments confirm that biogeographical variations observed in the alkenone vs. temperature relationship in natural waters reflect, at least in part, differences in genetic makeup and physiological status of the local alkenone-synthesizing populations. Hence, alkenone-based paleo sea surface temperature estimates are subject to errors, albeit small, which arise from genetic differences between modern-day and paleo-populations. The reduction in slope of the U37K′ temperature calibration for most strains at T >24°C indicate that linear U37K′ temperature calibrations (e.g., Prahl et al. 1988) which are currently used to estimate paleo SST, and which are poorly constrained at higher temperatures, probably underestimate the magnitude of SST change for tropical and subtropical regions.

Regime shifts in marine ecosystems: detection, prediction and management

Regime shifts are abrupt changes between contrasting, persistent states of any complex system. The potential for their prediction in the ocean and possible management depends upon the characteristics of the regime shifts: their drivers (from anthropogenic to natural), scale (from the local to the basin) and potential for management action (from adaptation to mitigation). We present a conceptual framework that will enhance our ability to detect, predict and manage regime shifts in the ocean, illustrating our approach with three well-documented examples: the North Pacific, the North Sea and Caribbean coral reefs. We conclude that the ability to adapt to, or manage, regime shifts depends upon their uniqueness, our understanding of their causes and linkages among ecosystem components and our observational capabilities.

Global biodiversity patterns of marine phytoplankton and zooplankton

Although the oceans cover 70% of the Earths surface, our knowledge of biodiversity patterns in marine phytoplankton and zooplankton is very limited compared to that of the biodiversity of plants and herbivores in the terrestrial world. Here, we present biodiversity data for marine plankton assemblages from different areas of the world ocean. Similar to terrestrial vegetation, marine phytoplankton diversity is a unimodal function of phytoplankton biomass, with maximum diversity at intermediate levels of phytoplankton biomass and minimum diversity during massive blooms. Contrary to expectation, we did not find a relation between phytoplankton diversity and zooplankton diversity. Zooplankton diversity is a unimodal function of zooplankton biomass. Most strikingly, these marine biodiversity patterns show a worldwide consistency, despite obvious differences in environmental conditions of the various oceanographic regions. These findings may serve as a new benchmark in the search for global biodiversity patterns of plants and herbivores.

Copepod hatching success in marine ecosystems with high diatom concentrations

Diatoms dominate spring bloom phytoplankton assemblages in temperate waters and coastal upwelling regions of the global ocean. Copepods usually dominate the zooplankton in these regions and are the prey of many larval fish species. Recent laboratory studies suggest that diatoms may have a deleterious effect on the success of copepod egg hatching. These findings challenge the classical view of marine food-web energy flow from diatoms to fish by means of copepods. Egg mortality is an important factor in copepod population dynamics, thus, if diatoms have a deleterious in situ effect, paradoxically, high diatom abundance could limit secondary production. Therefore, the current understanding of energy transfer from primary production to fisheries in some of the most productive and economically important marine ecosystems may be seriously flawed. Here we present in situ estimates of copepod egg hatching success from twelve globally distributed areas, where diatoms dominate the phytoplankton assemblage. We did not observe a negative relationship between copepod egg hatching success and either diatom biomass or dominance in the microplankton in any of these regions. The classical model for diatom-dominated system remains valid.

The role of nutricline depth in regulating the ocean carbon cycle

Carbon uptake by marine phytoplankton, and its export as organic matter to the ocean interior (i.e., the “biological pump”), lowers the partial pressure of carbon dioxide (pCO2) in the upper ocean and facilitates the diffusive drawdown of atmospheric CO2. Conversely, precipitation of calcium carbonate by marine planktonic calcifiers such as coccolithophorids increases pCO2 and promotes its outgassing (i.e., the “alkalinity pump”). Over the past ≈100 million years, these two carbon fluxes have been modulated by the relative abundance of diatoms and coccolithophores, resulting in biological feedback on atmospheric CO2 and Earths climate; yet, the processes determining the relative distribution of these two phytoplankton taxa remain poorly understood. We analyzed phytoplankton community composition in the Atlantic Ocean and show that the distribution of diatoms and coccolithophorids is correlated with the nutricline depth, a proxy of nutrient supply to the upper mixed layer of the ocean. Using this analysis in conjunction with a coupled atmosphere–ocean intermediate complexity model, we predict a dramatic reduction in the nutrient supply to the euphotic layer in the coming century as a result of increased thermal stratification. Our findings indicate that, by altering phytoplankton community composition, this causal relationship may lead to a decreased efficiency of the biological pump in sequestering atmospheric CO2, implying a positive feedback in the climate system. These results provide a mechanistic basis for understanding the connection between upper ocean dynamics, the calcium carbonate-to-organic C production ratio and atmospheric pCO2 variations on time scales ranging from seasonal cycles to geological transitions.

Zooplankton grazing on the coccolithophore Emiliania huxleyi and its role in inorganic carbon flux

Grazing and faecal pellet production by the copepods Calanus helgolandicus and Pseudocalanus elongatus, feeding on the coccolithophore Emiliania huxleyi, were measured under defined laboratory conditions, together with the chemical characteristics and sinking rates of the faecal pellets produced. Ingestion rates of both copepods were equivalent at comparable cell concentrations, the relationship between ingestion rate (I, cells copepod-1 h-1) and food concentration (C, cells ml-1), being I=0.558C for both species. P. elongatus produced a larger number of smaller faecal pellets than C. helgolandicus, but egested a larger volume of material per individual. Only between 27 and 50% of the ingested coccolith calcite was egested in the faecal pellets, and it is possible that acid digestion in the copepod gut is responsible for these considerable losses. Average sinking rates of faecal pellets containing E. huxleyi coccoliths, produced by both species, were >100 m d-1. The implications of the quantitative laboratory estimates for the vertical flux of inorganic carbon are considered using recently studied shelf-break and oceanic E. huxleyi blooms in the N. E. Atlantic as examples.

The Atlantic Meridional Transect: overview and synthesis of data

The Atlantic Meridional Transect programme uses the twice-annual passage of the RRS James Clark Ross between the UK and the Falkland Islands, before and after the Antarctic research programme in the Austral Summer (see Aiken, J., & Bale, A. J. (2000). An introduction to the Atlantic Meridional Transect (AMT) Programme. Progress in Oceanography, this issue). This paper examines the scientific rationale for a spatially-extensive time and space series programme and reviews the relevant physical and biological oceanography of the Atlantic Ocean. The main scientific observations from the research programme are reported. These are set in the context of historical and contemporary observations pertinent to the principal objectives of the cruise, notably the satellite remotely sensed observations of ocean properties. The extent to which the programme goals have been realised by the research to date is assessed and discussed. New bio-optical signatures, which can be related to productivity parameters, have been derived. These can be used to interpret remotely sensed observations of ocean colour in terms of productivity and production processes such as the air/sea exchange of biogenic gases, which relate to the issues of climate change and the sustainability of marine ecosystems.

STERYL CHLORIN ESTERS ARE FORMED BY ZOOPLANKTON HERBIVORY

Steryl chlorin esters (SCEs) were formed in laboratory feeding experiments when starved females of the copepod Calanus helgolandicus were allowed to graze on a culture of the diatom Thalassiosira weissflogii. They were found when the zooplankton had grazed for 48 hours and were also identified in fecal pellets subsequently left in seawater in the dark. The distribution contained the diatom sterols in approximately the same relative abundance as the free sterols in the substrate, as well as the most abundant copepod sterol, all esterified to the chlorophyll a degradation product, pyropheophorbide a. Hence, in studies aimed at using sedimentary SCE sterol distributions as indicators of phytoplankton community structure, cholesterol should not be considered since the cholesteryl ester of pyropheophorbide a was a significant component in the fecal pellet SCEs. The findings represent a step forward in unravelling the transformations undergone by chlorophyll a in aquatic environments, since the abundance and wide occurrence of sedimentary SCEs indicate that they are a significant preservational sink for the chlorophyll a biosynthesised in the photic zone.

The Physical And Chemical Environment And Changes In Community Structure Associated With Bloom Evolution - The Joint Global Flux Study North-Atlantic Bloom Experiment

Abstract The physical and chemical structure of the upper 100 m of the water column and biological parameters were measured during spring bloom development along a 20°W transect rom 60 to 47°N in June 1989. At 60°N, the situation was that of a late bloom: weak and intermittent stratification, high nutrient concentrations, and high and variable phytoplankton biomass and production. At 47°N, a post-bloom situation was observed: seasonal stratification in the upper 50 m, surface nutrient depletion, a subsurface chlorophyll maximum and reduced levels of primary production. At all stations, detrital material accounted for more than two-thirds of the > 0.8 μm particulate organic carbon within the upper 100 m. Phytoplankton biomass showed no pronounced latitudinal trends, but there was a shift from > 5 μm diatoms and prymnesiophytes at 60°N to dinoflagellates and 1–5 μm prymnesiophytes at 47°N. Nanophytoplankton comprised The data suggest a shift in the balance between production and consumption at different stages of the bloom. At 60°N, a late bloom situation, primary production exceeded consumption, while at 47°N, under post-bloom conditions, the situation was reversed. Lipid biomarkers indicate that the concentration of labile detrital carbon was significantly higher at the northernmost station, and that this was associated with mesozooplankton grazing. This suggests the efficiency of bloom utilization was low, which together with deeper mixing and the larger size structure of the plankton community, would result in a potential for substantial export flux during the late bloom phase.

The Lipid Composition of the Coccolithophore Emiliania Huxleyi and Its Possible Ecophysiological Significance

The lipid class and fatty acid composition of eight geographically disperse isolates of Emiliania huxleyi , grown under 12 h L:D cycles and harvested during logarithmic and stationary growth phases, were examined. Cell size and chlorophyll content tended to decrease from logarithmic to stationary growth phase, Methyl and ethyl ketones were the dominant lipid classes, although proportions exhibited no clear pattern either between strains or growth phases. Neutral lipid hardly accumulated over the course of the growth experiments, and triacylglycerol was either absent or only present at low levels. In all strains with the exception of a South African isolate, levels of total fatty acid per cell decreased markedly between logarithmic and stationary phases, primarily attributable to reductions in the levels of saturated and monounsaturated fatty acids. Major fatty acids in all strains during both growth phases were 14:0,16:0,18:1 (n-9), 18:4 (n-3), 18:5 (n-3) and 22:6 (n-3). Although all strains were rich in polyunsaturated fatty acids (47–72% of total fatty acids) stationary phase cultures consistently contained the highest proportions. The polyunsaturated fatty acid docosahexanoic acid (22:6, n-3) was the most abundant fatty acid in all strains, comprising a maximum of 38·4% of total fatty acids in strain M 181 during stationary phase. Multivariate analysis (PCA) allowed logarithmic and stationary phase cultures to be distinguished although no obvious intra-isolate variability was apparent. The results are discussed in terms of the importance of lipids for the ecophysiology of E. huxleyi and the role of this dominant coccolithophore in the marine food chain.