Paul J. Harrison

Comparison of factors controlling phytoplankton productivity in the NE and NW subarctic Pacific gyres

The subarctic North Pacific is one of the three major high nitrate low chlorophyll (HNLC) regions of the world. The two gyres, the NE and the NW subarctic Pacific gyres dominate this region; the NE subarctic Pacific gyre is also known as the Alaska Gyre. The NE subarctic Pacific has one of the longest time series of any open ocean station, primarily as a result of the biological sampling that began in 1956 on the weathership stationed at Stn P (50°N, 145°W; also known as Ocean Station Papa (OSP)). Sampling along Line P, a transect from the coast (south end of Vancouver Island) out to Stn P has provided valuable information on how various parameters change along this coastal to open ocean gradient. The NW subarctic Pacific gyre has been less well studied than the NE gyre. This review focuses mainly on the NE gyre because of the large and long term data set available, but makes a brief comparison with the NW gyre. The NE gyre has saturating NO3 concentrations all year (winter = about 16 μM and summer = about 8 μM), constantly very low chlorophyll (chl) (usually <0.5 mg m−3) which is dominated by small cells (<5 μm). Primary productivity is low (about 300–600 mg C m−2 d−1 and varies little (2 times) seasonally. Annual primary productivity is 3 to 4 times higher than earlier estimates ranging from 140 to 215 g C m−2 y−1. Iron limits the utilization of nitrate and hence the primary productivity of large cells (especially diatoms) except in the winter when iron and light may be co-limiting. There are observations of episodic increases in chl above 1 mg m−3, suggesting episodic iron inputs, most likely from Asian dust in the spring/early summer, but possibly from horizontal advection from the Alaskan Gyre in summer/early fall. The small cells normally dominate the phytoplankton biomass and productivity, and utilize the ammonium produced by the micrograzers. They do not appear to be Fe-limited, but are controlled by microzooplankton grazers. The NW Subarctic Gyre has higher nutrient concentrations and a shallower summer mixed depth and photic zone than Stn P in the NE gyre. Chl concentrations tend to be higher (0.5 to 1.5 μg L−1) than Stn P, but primary productivity in the summer is similar to Stn P (∼600 mg C m−2 d−1). There are no seasonal data from this gyre. Iron enrichment experiments in October, resulted in an increase in chl (mainly the centric diatom Thalassiosira sp.) and a draw down of nitrate, suggesting that large phytoplankton are Fe-limited, similar to Stn P.

Effects of nutrient limitation on toxin production and composition in the marine dinoflagellate Protogonyaulax tamarensis

Toxin production was measured by high pressure liquid chromatography (HPLC) when the marine dinoflagellate Protogonyaulax tamarensis (NEPCC 255) was grown under nitrogen or phosphorus limitation. The major toxins found in P. tamarensis (255) consisted of (N21-SO3-)STX (11%), (N21-SO3-)NeoSTX (44%), and [(N21-SO3-)GTX2 plus (N21-SO3-)GTX3] (20%). Total toxin content on a per cell basis was high for cultures in log phase (30 to 40 fmol cell-1) and then decreased to ca 20 fmol cell-1 as the cultures entered stationary phase. There was a gradual decrease in the toxin content per cell during nitrogen-limited stationary phase to ca 3 fmol cell-1 or less. Phosphorus-limited cultures showed a markedly different response than nitrogen-limited cultures. Toxin content in P-limited cells dramatically increased at the start of stationary phase, reaching levels 3 to 4 times that observed in control and nitrogen-limited cultures. These results cannot be explained by changes in the average cell volume. Eventhough dramatic effects on the total toxin concentration were observed in response to nutrient limitation (N or P), the toxin composition (on a percent basis) remained constant. This suggests that the individual toxin composition of a given isolate is a fixed genetic trait and not a transient response to changing environmental factors.

Temporal and spatial variations in nutrient stoichiometry and regulation of phytoplankton biomass in Hong Kong waters: Influence of the Pearl River outflow and sewage inputs

In 2001, the Hong Kong government implemented the Harbor Area Treatment Scheme (HATS) under which 70% of the sewage that had been formerly discharged into Victoria Harbor is now collected and sent to Stonecutters Island Sewage Works where it receives chemically enhanced primary treatment (CEPT), and is then discharged into waters west of the Harbor. The relocation of the sewage discharge will possibly change the nutrient dynamics and phytoplankton biomass in this area. Therefore, there is a need to examine the factors that regulate phytoplankton growth in Hong Kong waters in order to understand future impacts. Based on a historic nutrient data set (1986-2001), a comparison of ambient nutrient ratios with the Redfield ratio (N:P:Si=16:1:16) showed clear spatial variations in the factors that regulate phytoplankton biomass along a west (estuary) to east (coastal/oceanic) transect through Hong Kong waters. Algal biomass was constrained by a combination of low light conditions, a rapid change in salinity, and strong turbulent mixing in western waters throughout the year. Potential stoichiometric Si limitation (up to 94% of the cases in winter) occurred in Victoria Harbor due to the contribution of sewage effluent with high N and P enrichment all year, except for summer when the frequency of stoichiometric Si limitation (48%) was the same as P, owing to the influence of the high Si in the Pearl River discharge. In the eastern waters, potential N limitation and N and P co-limitation occurred in autumn and winter respectively, because of the dominance of coastal/oceanic water with low nutrients and low N:P ratios. In contrast, potential Si limitation occurred in spring and a switch to potential N, P and Si limitation occurred in eastern waters in summer. In southern waters, there was a shift from P limitation (80%) in summer due to the influence of the N-rich Pearl River discharge, to N limitation (68%) in autumn, and to N and P co-limitation in winter due to the dominance of N-poor oceanic water from the oligotrophic South China Sea. Our results show clear temporal and spatial variations in the nutrient stoichiometry which indicates potential regulation of phytoplankton biomass in HK waters due to the combination of the seasonal exchange of the Pearl River discharge and oceanic water, sewage effluent inputs, and strong hydrodynamic mixing from SW monsoon winds in summer and the NE monsoon winds in winter.

Seasonal and spatial dynamics of nutrients and phytoplankton biomass in Victoria Harbour and its vicinity before and after sewage abatement

This study investigated the seasonal and spatial dynamics of nutrients and phytoplankton biomass at 12 stations in Hong Kong (HK) waters during a three year period from 2004 to 2006 after upgraded sewage treatment and compared these results to observations before sewage treatment. Pearl River estuary (PRE) discharge significantly increased NO(3) and SiO(4) concentrations, particularly in western and southern waters when rainfall and river discharge was maximal in summer. Continuous year round discharge of sewage effluent resulted in high NH(4) and PO(4) in Victoria Harbour (VH) and its vicinity. In winter, spring and fall, the water column at all stations was moderately mixed by winds and tidal currents, and phytoplankton biomass was relatively low compared to summer. In summer, the mean surface phytoplankton chl biomass was generally > 9 microL(-1) in most areas as a result of thermohaline stratification, and high nutrients, light, and water temperature. In summer, the potential limiting nutrient is PO(4) in the most productive southern waters and it seldom decreased to limiting levels ( approximately 0.1 microM), suggesting that phytoplankton growth may be only episodically limiting. The mean bottom dissolved oxygen (DO) remained > 3.5 mg L(-1) at most stations, indicating that the eutrophication impact in HK waters was not as severe as expected for such a eutrophic area. After the implementation of chemically enhanced primary sewage treatment in 2001, water quality in VH improved as indicated by a significant decrease in NH(4) and PO(4) and an increase in bottom DO. In contrast, there were an increase in chl a and NO(3), and a significant decrease in bottom DO in southern waters in summer, suggesting that hypoxic events are most likely to occur in this region if phytoplankton biomass and oxygen consumption keep increasing and exceed the buffering capacity of HK waters maintained by monsoon winds, tidal mixing and zooplankton grazing. Therefore, future studies on the long-term changes in nutrient loading from PRE and HK sewage discharge will be crucial for developing future strategies of sewage management in HK waters.

Environmental response to sewage treatment strategies: Hong Kong's experience in long term water quality monitoring

In many coastal cities around the world, marine outfalls are used for disposal of partially treated wastewater effluent. The combined use of land-based treatment and marine discharge can be a cost-effective and environmentally acceptable sewage strategy. Before 2001, screened sewage was discharged into Victoria Harbour through many small outfalls. After 2001, the Hong Kong Harbour Area Treatment Scheme (HATS) was implemented to improve the water quality in Victoria Harbour and surrounding waters. Stage I of HATS involved the construction of a 24 km long deep tunnel sewerage system to collect sewage from the densely populated urban areas of Hong Kong to a centralized sewage treatment plant at Stonecutters Island. A sewage flow of 1.4 million m3 d(-1) receives Chemically Enhanced Primary Treatment (CEPT) followed by discharge via a 1.2 km long outfall 2 km west of the harbor. The ecosystem recovery in Victoria Harbour and the environmental response to sewage abatement after the implementation of HATS was studied using a 21-year data set from long term monthly water quality monitoring. Overall, the pollution control scheme has achieved the intended objectives. The sewage abatement has resulted in improved water quality in terms of a significant reduction in nutrients and an increase in bottom DO levels. Furthermore, due to the efficient tidal mixing and flushing, the impact of the HATS discharge on water quality in the vicinity of the outfall location is relatively limited. However, Chl a concentrations have not been reduced in Victoria Harbour where algal growth is limited by hydrodynamic mixing and water clarity rather than nutrient concentrations. Phosphorus removal in the summer is suggested to reduce the risk of algal blooms in the more weakly-flushed and stratified southern waters, while nutrient removal is less important in other seasons due to the pronounced role played by hydrodynamic mixing. The need for disinfection of the effluent to reduce bacterial (E. coli) concentrations to acceptable levels is also confirmed and has recently been implemented.

Effects of temperature and irradiance on growth of strains belonging to seven Skeletonema species isolated from Dokai Bay, southern Japan

The effect of temperature on the growth of Skeletonema ardens, S. costatum sensu stricto, the S. marinoi–dohrnii complex, S. japonicum, S. menzelii, S. pseudocostatum and S. tropicum isolated from Dokai Bay in southern Japan were examined under five to seven different temperatures and an irradiance of 150u2009µmolu2009m−2u2009s−1. The effect of irradiance on the growth of the seven Skeletonema species was also examined under a wide range of irradiances ranging from 7–700u2009µmolu2009m−2u2009s−1 at 20°C. All Skeletonema species were able to grow at temperatures ranging from 15 to 25°C. Intra-species differences in specific growth rates of four strains for S. menzelii, and five strains for S. ardens, the S. marinoi–dohrnii complex, S. japonicum and S. tropicum were not significant (Kruskal–Wallis test, Pu2009>u20090.05). Significant inter-species differences in specific growth rates were observed at 10, 15, 25 and 30°C (Kruskal–Wallis test, Pu2009<u20090.01; Steel–Dwass test, Pu2009<u20090.01). The S. marinoi–dohrnii complex and S. japonicum grew faster than other species at the lower temperatures of 10 and 15°C, and S. ardens and S. menzelii grew at the highest temperature of 35°C. The maximum specific growth rates (μ max) from growth–irradiance curves ranged from 1.50 to 3.44u2009d−1. Threshold values of irradiance (I 0) and saturation irradiance (S) for growth ranged from 3.9 to 7.6u2009µmolu2009m−2u2009s−1, and from 250 to 740u2009µmolu2009m−2u2009s−1, respectively. In Dokai Bay, our results suggested that the occurrence of Skeletonema species should be affected mainly by temperature and less by irradiance. In particular, only two species, the S. marinoi–dohrnii complex and S. japonicum could maintain their populations in the surface water during the cold season, whereas during other periods, all seven species could maintain their population under the strong influence of estuarine circulation, which rapidly flushed the surface water out of Dokai Bay. Temperature and irradiance dependent growth values were in good agreement with their geographical distributions. The S. marinoi–dohrnii complex and S. japonicum were capable of growing in cold regions, but our results suggested that S. ardens and S. menzelii will tend to prefer tropical regions.

Modeling analysis of the effect of iron enrichment on dimethyl sulfide dynamics in the NE Pacific (SERIES experiment)

The large-scale iron enrichment conducted in the NE Pacific during the Subarctic Ecosystem Response to Iron Enrichment Study (SERIES) triggered a phytoplankton bloom dominated successively by nanophytoplankton and large diatoms. During the first 14 days, surface dimethyl sulfide (DMS) levels increased both inside (up to 22 nmol L-1) and outside (up to 19 nmol L-1) the patch, with no consistent Fe effect. Later, DMS concentrations became sixfold lower inside the patch than outside. In this study, we used a DMS budget module embedded in a one-dimensional ocean turbulence model to investigate the contribution of the interacting physical, photochemical, and biological processes to this particular DMS response. Temporal variations in biological net DMS production were reconstructed using an inverse modeling approach. Our results show that short-term (days) variations in both the physical processes (i.e., turbulent mixing and ventilation) and the biological cycling of DMS are needed to explain the time evolution of DMS concentrations both outside and inside the Fe-enriched patch. The biological net DMS production was generally high (up to 0.35 nmol L-1 h-1) and comparable outside and inside the patch during the first 10 days, corresponding to the observed accumulation of DMS inside and outside the patch. Later, it became negative (net DMS biological consumption) inside the patch, suggesting a change in dimethylsulfoniopropionate bacterial metabolism. This study stresses the importance of short-term variations in biological processes and their sensitivity to the physical environment in shaping the DMS response to iron enrichment.

Inorganic and Organic Nitrogen Uptake by Phytoplankton and Bacteria in Hong Kong Waters

Measurements of uptake rates of inorganic (NO3− and NH4+) and organic (urea, glycine, and glutamic acid) N, and indirect estimates of total N uptake by bacteria, were made in four contrasting environments in sub-tropical Hong Kong waters in summer of 2008. In addition, the effects of several days of rain on N uptake rates were studied in eastern waters. Although ambient NO3− was the dominant form of N in Hong Kong waters, the dominant N form taken up by phytoplankton was usually NH4+ and organic N, including urea and amino acids, rather than NO3−. Hence, because of the low NO3− uptake, there was a long turnover time for NO3− (100xa0days), and most of the NO3− was apparently transported offshore into deeper shelf waters. In eastern waters where NH4+ was undetectable, NO3− uptake rates were positively correlated with phytoplankton cell size. In contrast, potential rates of glutamic acid uptake were negatively correlated with phytoplankton size. N uptake rates in the smaller size fraction (0.7–2.8xa0μm) were less affected by the rain event, and smaller phytoplankton appeared to outcompete larger cells after several days of rain. The surface (PN)-specific N uptake rates in the >8-μm fraction decreased from 0.02 to 0.0001xa0h−1, while the smaller fraction only exhibited a one- to threefold decrease after the rainfall. In contrast, bacterial production and N uptake were not affected by the rain event, and bacteria N uptake accounted for 10–60% of the total N uptake by phytoplankton.

Nitrogen Sources and Rates of Phytoplankton Uptake in Different Regions of Hong Kong Waters in Summer

Phytoplankton uptake rates of ammonium (NH4+), nitrate (NO3−), and urea were measured at various depths (light levels) in Hong Kong waters during the summer of 2008 using 15N tracer techniques in order to determine which form of nitrogen (N) supported algal growth. Four regions were sampled, two differentially impacted by Pearl River discharge, one impacted by Hong Kong sewage discharge, and a site beyond these influences. Spatial differences in nutrient concentrations, ratios, and phytoplankton biomass were large. Dissolved nutrient ratios suggested phosphorus (P) limitation throughout the region, largely driven by high N loading from the Pearl River in summer. NH4+ and urea made up generally ≥50% of the total N taken up and the f ratio averaged 0.26. Even at the river-impacted site where concentrations of NO3− were >20xa0μM N, NH4+ comprised >60% of the total N uptake. Inhibition experiments demonstrated that NO3− uptake rates were reduced by 40% when NH4+ was >5xa0μM N. The relationship between the total specific uptake rates of N (sum of all measured substrates, V, per hour) and the chlorophyll a-specific rates (micromolars of N per microgram of Chl a per hour) varied spatially with phytoplankton biomass. Highest uptake rates and biomass were observed in southern waters, suggesting that P limitation and other factors (i.e., flushing rate) controlled production inshore and that the unincorporated N (mainly NO3−) was transported offshore. These results suggest that, at the beginning of summer, inshore algal blooms are fueled primarily by NH4+ and urea, rather than NO3−, from the Pearl River discharge. When NH4+ and urea are depleted, then NO3− is taken up and can increase the magnitude of the bloom.

Regulation of bacterial metabolic activity by dissolved organic carbon and viruses

The regulation of bacterial metabolic activity by viruses and dissolved organic carbon (DOC) was examined using natural microbial communities in three treatments (active viruses, inactive viruses, and virus free) at two contrasting coastal sites (pristine vs. eutrophic) with substantial differences in environmental conditions during the wet and dry seasons. Our results showed that net growth rates and production of bacterioplankton were reduced primarily by viruses via repressing metabolically active bacteria with high nucleic acid (HNA) content which had a high capacity for incorporating carbon, while bacterial respiration was primarily regulated by DOC lability. The quality of organic matter played a more important role in regulating bacterial growth efficiency (BGE) than the supply of organic matter in eutrophic coastal waters. The lack of HMW-DOC and high carbon demand in the virus-free treatment resulted in a significant increase in cell-specific bacterial respiration, which was responsible for the lowest bacterial growth efficiency among the three treatments. The presence of viruses did not necessarily lower bacterial growth efficiency since virus-induced mortality alleviated bacterial carbon demand and enhanced carbon cycling. Virus-induced mortality was greater in relatively pristine waters than eutrophic waters, likely since the high supply of substrates alleviated the pressure of viral infection, through extracellular proteases produced by bacteria, which might result in the hydrolytic destruction or modification of viral capsids. An important implication of our results was that the input of riverine DOC and nutrients improved bacterial metabolic activity by alleviating virus-induced mortality of bacteria in estuarine and coastal waters.