Patricia M. Glibert

Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences.

Although algal blooms, including those considered toxic or harmful, can be natural phenomena, the nature of the global problem of harmful algal blooms (HABs) has expanded both in extent and its public perception over the last several decades. Of concern, especially for resource managers, is the potential relationship between HABs and the accelerated eutrophication of coastal waters from human activities. We address current insights into the relationships between HABs and eutrophication, focusing on sources of nutrients, known effects of nutrient loading and reduction, new understanding of pathways of nutrient acquisition among HAB species, and relationships between nutrients and toxic algae. Through specific, regional, and global examples of these various relationships, we offer both an assessment of the state of understanding, and the uncertainties that require future research efforts. The sources of nutrients potentially stimulating algal blooms include sewage, atmospheric deposition, groundwater flow, as well as agricultural and aquaculture runoff and discharge. On a global basis, strong correlations have been demonstrated between total phosphorus inputs and phytoplankton production in freshwaters, and between total nitrogen input and phytoplankton production in estuarine and marine waters. There are also numerous examples in geographic regions ranging from the largest and second largest U.S. mainland estuaries (Chesapeake Bay and the Albemarle-Pamlico Estuarine System), to the Inland Sea of Japan, the Black Sea, and Chinese coastal waters, where increases in nutrient loading have been linked with the development of large biomass blooms, leading to anoxia and even toxic or harmful impacts on fisheries resources, ecosystems, and human health or recreation. Many of these regions have witnessed reductions in phytoplankton biomass (as chlorophylla) or HAB incidence when nutrient controls were put in place. Shifts in species composition have often been attributed to changes in nutrient supply ratios, primarily N∶P or N∶Si. Recently this concept has been extended to include organic forms of nutrients, and an elevation in the ratio of dissolved organic carbon to dissolved organic nitrogen (DOC∶DON) has been observed during several recent blooms. The physiological strategies by which different groups of species acquire their nutrients have become better understood, and alternate modes of nutrition such as heterotrophy and mixotrophy are now recognized as common among HAB species. Despite our increased understanding of the pathways by which nutrients are delivered to ecosystems and the pathways by which they are assimilated differentially by different groups of species, the relationships between nutrient delivery and the development of blooms and their potential toxicity or harmfulness remain poorly understood. Many factors such as algal species presence/abundance, degree of flushing or water exchange, weather conditions, and presence and abundance of grazers contribute to the success of a given species at a given point in time. Similar nutrient loads do not have the same impact in different environments or in the same environment at different points in time. Eutrophication is one of several mechanisms by which harmful algae appear to be increasing in extent and duration in many locations. Although important, it is not the only explanation for blooms or toxic outbreaks. Nutrient enrichment has been strongly linked to stimulation of some harmful species, but for others it has not been an apparent contributing factor. The overall effect of nutrient over-enrichment on harmful algal species is clearly species specific.

Nitrogen Uptake, Dissolved Organic Nitrogen Release, and New Production

In oceanic, coastal, and estuarine environments, an average of 25 to 41 percent of the dissolved inorganic nitrogen (NH4 + and NO3 –) taken up by phytoplankton is released as dissolved organic nitrogen (DON). Release rates for DON in oceanic systems range from 4 to 26 nanogram-atoms of nitrogen per liter per hour. Failure to account for the production of DON during nitrogen-15 uptake experiments results in an underestimate of gross nitrogen uptake rates and thus an underestimate of new and regenerated production. In these studies, traditional nitrogen-15 techniques were found to underestimate new and regenerated production by up to 74 and 50 percent, respectively. Total DON turnover times, estimated from DON release resulting from both NH4 + and NO3 – uptake, were 10 � 1, 18 � 14, and 4 days for oceanic, coastal, and estuarine sites, respectively.

Effect of irradiances up to 2000 μE m−2 s−1 on marine Synechococcus WH7803—I. Growth, pigmentation, and cell composition

Abstract We grew Synechococcus WH7803 at rates exceeding 1.4 d −1 at irradiances from 200 to 2000 μE m −2 s −1 under continuous light in nutrient replete media with no evidence of photoinhibition. Concentrations of the photosynthetic pigments phycoerythrin, phycocyanin, and chlorophyll a , were inversely related to growth irradiance. Phycoerythrin exhibited the greatest plasticity with the concentration in cells adapted to 30 μE m −2 s −1 being ca . 20 times greater than that in cells adapted to 700 μE m −2 s −1 . Changes in the phycoerythrin: phycocyanin ratio as well as their respective concentrations indicate that phycobilisomes underwent changes in size at irradiances which saturated or nearly saturated growth and underwent changes in number at irradiances which limited growth. Phycoerythrin in high light adapted cells contained 20% in light limited cells. Results support the notion that nutrient replete Synechococcus have the capacity to grow at maximal growth rates in brightly lit oceanic surface mixed layers.

COMPARISONS OF NITRATE UPTAKE, STORAGE, AND REDUCTION IN MARINE DIATOMS AND FLAGELLATES

Diatoms, but not flagellates, have been shown to increase rates of nitrogen release after a shift from a low growth irradiance to a much higher experimental irradiance. We compared NO3− uptake kinetics, internal inorganic nitrogen storage, and the temperature dependence of the NO3− reduction enzymes, nitrate (NR) and nitrite reductase (NiR), in nitrogen‐replete cultures of 3 diatoms (Chaetoceros sp., Skeletonema costatum, Thalassiosira weissflogii) and 3 flagellates (Dunaliella tertiolecta, Pavlova lutheri, Prorocentrum minimum) to provide insight into the differences in nitrogen release patterns observed between these species. At NO3− concentrations <40 μmol‐N·L−1, all the diatom species and the dinoflagellate P. minimum exhibited saturating kinetics, whereas the other flagellates, D. tertiolecta and P. lutheri, did not saturate, leading to very high estimated K  s values. Above ∼60 μmol‐N·L−1, NO3− uptake rates of all species tested continued to increase in a linear fashion. Rates of NO3− uptake at 40 μmol‐N·L−1, normalized to cellular nitrogen, carbon, cell number, and surface area, were generally greater for diatoms than flagellates. Diatoms stored significant amounts of NO3− internally, whereas the flagellate species stored significant amounts of NH4+. Half‐saturation concentrations for NR and NiR were similar between all species, but diatoms had significantly lower temperature optima for NR and NiR than did the flagellates tested in most cases. Relative to calculated biosynthetic demands, diatoms were found to have greater NO3− uptake and NO3− reduction rates than flagellates. This enhanced capacity for NO3− uptake and reduction along with the lower optimum temperature for enzyme activity could explain differences in nitrogen release patterns between diatoms and flagellates after an increase in irradiance.

Scales of Nutrient-Limited Phytoplankton Productivity in Chesapeake Bay

The scales on which phytoplankton biomass vary in response to variable nutrient inputs depend on the nutrient status of the plankton community and on the capacity of consumers to respond to increases in phytoplankton productivity. Overenrichment and associated declines in water quality occur when phytoplankton growth rate becomes nutrient-saturated, the production and consumption of phytoplankton biomass become uncoupled in time and space, and phytoplankton biomass becomes high and varies on scales longer than phytoplankton generation times. In Chesapeake Bay, phytoplankton growth rates appear to be limited by dissolved inorganic phosphorus (DIP) during spring when biomass reaches its annual maximum and by dissolved inorganic nitrogen (DIN) during summer when phytoplankton growth rates are highest. However, despite high inputs of DIN and dissolved silicate (DSi) relative to DIP (molar ratios of N∶P and Si∶P>100), seasonal accumulations of phytoplankton biomass within the salt-intruded-reach of the bay appear to be limited by riverine DIN supply while the magnitude of the spring diatom bloom is governed by DSi supply. Seasonal imbalances between biomass production and consumption lead to massive accumulations of phytoplankton biomass (often>1,000 mg Chl-a m−2) during spring, to spring-summer oxygen depletion (summer bottom water <20% saturation), and to exceptionally high levels of annual phytoplankton production (>400 g m−2 yr−1). Nitrogen-dependent seasonal accumulations of phytoplankton biomass and annual production occur as a consequence of differences in the rates and pathways of nitrogen and phosphorus cycling within the bay and underscore the importance of controlling nitrogen inputs to the mesohaline and lower reaches of the bay.

Harmful algal blooms in the Chesapeake and coastal bays of Maryland, USA: Comparison of 1997, 1998, and 1999 events

Harmful algal blooms in the Chesapeake Bay and coastal bays of Maryland, USA, are not a new phenomenon, but may be increasing in frequency and diversity. Outbreaks ofPfiesteria piscicida (Dinophyceae) were observed during 1997 in several Chesapeake Bay tributaries, while in 1998,Pfiesteria-related events were not found but massive blooms ofProrocentrum minimum (Dinophyceae) occurred. In 1999,Aureococcus anophagefferens (Pelagophyceae) developed in the coastal bays in early summer in sufficient densities to cause a brown tide. In 1997, toxicPfiesteria was responsible for fish kills at relatively low cell densities. In 1998 and 1999, the blooms ofP. minimum andA. anophagefferens were not toxic, but reached sufficiently high densities to have ecological consequences. These years differed in the amount and timing of rainfall events and resulting nutrient loading from the largely agricultural watershed. Nutrient loading to the eastern tributaries of Chesapeake Bay has been increasing over the past decade. Much of this nutrient delivery is in organic form. The sites of thePfiesteria outbreaks ranked among those with the highest organic loading of all sites monitored bay-wide. The availability of dissolved organic carbon and phosphorus were also higher at sites experiencingA. anophagefferens blooms than at those without blooms. The ability to supplement photosynthesis with grazing or organic substrates and to use a diversity of organic nutrients may play a role in the development and maintenance of these species. ForP. minimum andA. anophagefferens, urea is used preferentially over nitrate.Pfiesteria is a grazer, but also has the ability to take up nutrients directly. The timing of nutrient delivery may also be of critical importance in determining the success of certain species.

Total dissolved nitrogen analysis : comparisons between the persulfate, UV and high temperature oxidation methods

We compared the persulfate (PO), ultraviolet (UV), and high temperature oxidation (HTO) methods used to analyze total dissolved nitrogen (TDN) concentrations in aquatic samples to determine whether the three methods differed in terms of standard parameters (blanks, limits of detection and linearity, and precision) or in oxidation efficiency of standard compounds and field samples of varying salinity. The TDN concentrations of several N-containing standard compounds, as well as a humic mixture and a suite of field samples collected from the Sargasso Sea, Chesapeake Bay and an aquaculture pond were determined with the three methods. The PO method had the highest percent recoveries for the range of labile and refractory standard compounds tested (93±13). The HTO method yielded recoveries of 87±14; recoveries increased to 91±10 under optimized conditions. The standard UV method, with 30% H2O2 as the oxidant, was found to be highly variable, producing the lowest percent recoveries (71±21); the oxidation efficiency of the UV method increased substantially in subsequent trials (91±12), when the PO reagent was used in place of H2O2. In the field sample comparison, the PO, UV with PO reagent, and HTO method produced similar results (slopes of the Model II regression lines comparing them ranged from 1.00 to 1.05 with r2≥0.99). The standard UV method, however, produced concentrations 5% to 40% lower than the other methods. Analysis of the spectra emitted by the UV lamp used in this study suggests that variations in the UV spectra reaching the sample may have caused the reduced efficiencies. The poor recovery of some standard compounds with each of the methods suggests that concentrations of TDN, and subsequently DON, measured in the field with any of the methods will likely be underestimated to some degree depending on the composition of the TDN pool at that time. With careful attention to detail, however, the PO and HTO methods can provide reproducible results consistent with each other. The standard UV method, however, was found to be highly unpredictable in practice.

Utilization of ammonium and nitrate during austral summer in the Scotia Sea

Abstract The nitrogenous nutrition of the phytoplankton in the Scotia Sea was investigated with 15 N tracer techniques during the austral summer of 1979. On a regional scale, ambient NH 4 + concentrations in the upper hundred meters were variable (0.1 to 2.5 μg-at. 1 −1 ) and one or more orders of magnitude lower than ambient NO 3 − concentrations (17 to 31 μg-at. 1 −1 ). Despite the abundance of NO 3 − , late summer phytoplankton showed a consistent preference for NH 4 + utilization relative to NO 3 − . This was determined by use of a relative preference index and the patterns are similar to those of other marine, estuarine, and fresh waters to which it has been applied. The ratio of NO 3 − utilization to total nitrogen utilization indicated that when ambient NH 4 + concentrations were > 1.0 μg-at. 1 −1 , NO 3 − accounted for s40% of the total nitrogen utilized. Thus, even when NO 3 − is present in quantities that approach the upper limits for near-surface open-ocean waters, the processes that recycle NH 4 + locally can make a major contribution to the nutrition of the phytoplankton. Data for NO 3 − uptake from the 0.1% light level at several of the southernmost stations appeared anomalous. The observed values were higher than would have been expected solely from phytoplakton uptake.

Regional studies of daily, seasonal and size fraction variability in ammonium remineralization

Rates of ammonium remineralization were determined using a 15N isotope dilution technique for two oceanic regions, one coastal region, and one estuarine region, covering a wide range of ambient nutrient, light, and temperature conditions. Results showed that NH4+assimilative and regenerative fluxes were primarily in balance, even when the ambient nitrogenous pool was completely dominated by NO3-. Variations in uptake and remineralization rates relative to time of day and season were also determined. Size fraction studies at several of the sites showed that the smallest size fraction (<10 μm) was usually the most important in remineralizing NH4+, and the importance of the apparent bacterial fraction (<1 μm) may increase following blooms. The results support the concept that, over a wide variety of conditions, the fluxes of NH4+remineralization and uptake are tightly coupled; phytoplankton are able to utilize NH4+at the rate that it is produced by heterotrophic processes.

Linking environmental nutrient enrichment and disease emergence in humans and wildlife

Worldwide increases in human and wildlife diseases have challenged ecologists to understand how large-scale environmental changes affect host-parasite interactions. One of the most profound changes to Earths ecosystems is the alteration of global nutrient cycles, including those of phosphorus (P) and especially nitrogen (N). Along with the obvious direct benefits of nutrient application for food production, anthropogenic inputs of N and P can indirectly affect the abundance of infectious and noninfectious pathogens. The mechanisms underpinning observed correlations, however, and how such patterns vary with disease type, have long remained conjectural. Here, we highlight recent experimental advances to critically evaluate the relationship between environmental nutrient enrichment and disease. Given the interrelated nature of human and wildlife disease emergence, we include a broad range of human and wildlife examples from terrestrial, marine, and freshwater ecosystems. We examine the consequences of nutrient pollution on directly transmitted, vector-borne, complex life cycle, and noninfectious pathogens, including West Nile virus, malaria, harmful algal blooms, coral reef diseases, and amphibian malformations. Our synthetic examination suggests that the effects of environmental nutrient enrichment on disease are complex and multifaceted, varying with the type of pathogen, host species and condition, attributes of the ecosystem, and the degree of enrichment; some pathogens increase in abundance whereas others decline or disappear. Nevertheless, available evidence indicates that ecological changes associated with nutrient enrichment often exacerbate infection and disease caused by generalist parasites with direct or simple life cycles. Observed mechanisms include changes in host/vector density, host distribution, infection resistance, pathogen virulence or toxicity, and the direct supplementation of pathogens. Collectively, these pathogens may be particularly dangerous because they can continue to cause mortality even as their hosts decline, potentially leading to sustained epidemics or chronic pathology. We suggest that interactions between nutrient enrichment and disease will become increasingly important in tropical and subtropical regions, where forecasted increases in nutrient application will occur in an environment rich with infectious pathogens. We emphasize the importance of careful disease management in conjunction with continued intensification of global nutrient cycles.