Grantee Research Project Results
2005 Progress Report: Dynamics, Variability and Patterns of Harmful and Red Tide Bloom-Species in Narragansett Bay: Ecological Analysis of a 38-Year Time Series
EPA Grant Number: R829368Title: Dynamics, Variability and Patterns of Harmful and Red Tide Bloom-Species in Narragansett Bay: Ecological Analysis of a 38-Year Time Series
Investigators: Smayda, Theodore J. , Borkman, David G.
Institution: University of Rhode Island
EPA Project Officer: Packard, Benjamin H
Project Period: September 28, 2001 through January 27, 2006 (Extended to September 30, 2006)
Project Period Covered by this Report: September 28, 2004 through January 27, 2005
Project Amount: $348,912
RFA: Ecology and Oceanography of Harmful Algal Blooms (2001) RFA Text | Recipients Lists
Research Category: Water Quality , Water , Aquatic Ecosystems
Objective:
This project is directed towards filling fundamental knowledge gaps in the ecology of harmful algal blooms (HABs) and red tides. The biological data of the 18 species to be evaluated and accompanying physical and chemical data in the 38-year Narragansett Bay Time Series (NBTS) to be used in this project will be made Web site accessible. The goals of the project are to: (1) elucidate the mechanisms underlying the selection and bloom cycles of 18 indigenous, cosmopolitan, and representative HABs and benign red tide taxa in Narragansett Bay (NBay); (2) describe the long-term patterns, trends, and variability in their blooms; (3) quantify the effects and interactions of meteorological, climatic, physical, chemical, and biological parameters in this variability; (4) apply and evaluate the “open niche” hypothesis as a general HAB paradigm; (5) develop a Web site and dedicated server making the time series data electronically available to the scientific community as well as local and state agencies.
Progress Summary:
Our efforts to quantify the long-term variability in the bloom frequency, magnitude, duration, and occurrence patterns of the harmful bloom species found in NBay have followed the traditional approach of selecting a given species, and then interrogating the data for causal links between its observed bloom behavior and habitat conditions. Through this species-by-species procedure, the aim is to reconstruct the overall harmful algal bloom behavior in a representative ecosystem for general extrapolation. This approach focuses on internal ecosystem variables, such as prevailing physical, chemical, and biological conditions, supplemented by consideration of external drivers associated with meteorological and climatological conditions, such as the North Atlantic Oscillation Index. This latter effort tends to be subjective because it is difficult to quantify which feature of the meteorological or climatological event is significant to the process being evaluated. As a result, these regional scale drivers have greater utility as proxies, rather than as specific variables having the same value as direct measurements of nutrient or grazer abundance.
During the present period of activity on this project being reported, it became evident that significant whole-system, long-term events, trends, and thresholds that are ordinarily neglected in investigations of this type are very relevant to the analyses, even though at first glance they appear to be of peripheral value. The need to consider diatom blooms was one of these unanticipated realizations. It became evident that the major shifts in the long-term bloom behavior of the diatom Skeletonema costatum sensu lato, numerically the most important species in NBay, and the progressive displacement of the classical, annual winter-spring diatom bloom to a summer maximum impacted niche properties affecting observed HAB dynamics. Thus, we initiated detailed analyses of the multidecadal bloom behavior of S. costatum and its regulation from the perspective of its impacts on accompanying HAB behavior. We have been particularly interested in its summer bloom behavior because this is recognized as the “open niche” period in NBay, during which both harmful and benign flagellate species bloom, but the species selected and the duration and magnitude of its bloom are highly unpredictable. With regard to the “open niche” period, which follows the winter-spring diatom bloom, we have identified temperature as an unexpected factor in the general restriction of harmful flagellate species to that period. It appears that a 15°C “temperature barrier” that functions as a bloom threshold must be exceeded for the successional appearance of most harmful bloom species. This is evident based on a review of experimental results on the temperature-dependence of cellular growth rate and motility for ca. 25 HAB species representative of different toxicity types and habitats. The corollary of this is that the classical view that HABs require stratified watermasses to develop may be a default condition of this temperature requirement. This is contradictory to dogma which states that HAB formation has an absolute requirement for watermass stratification, and introduces a number of questions regarding the unresolved issues of the mechanisms of nutrient supply during watermass quiescence and adaptive strategies allowing bloom success at low nutrient levels.
Another realization that altered our conceptual and analytical approaches was the unanticipated ecosystem impact of the novel, prolonged (5-month), and very harmful “brown tide” bloom of the pelagophyte Aureococcus anophagefferens that occurred in 1985. Initially, interrogation of the data suggested that this anomalous bloom, which has not recurred in NBay, had no lasting effect; that “normal” bloom behavior, plankton dynamics, and community composition quickly recovered the following year, that is, there was no hysteresis effect. However, it became evident that significant and sustained changes in bloom species behavior in the years since the 1985 “brown tide” have occurred. Some examples of this altered behavior are presented below. Accordingly, during the period of this report, we launched a more detailed analysis of the “brown tide” year from the perspective of previous and subsequent bloom species behavior, incorporating into our analyses the nutrient and plankton behavior found along the salinity-nutrient gradient in NBay. The results suggest that the 1985 “brown tide” did not, per se and directly, influence subsequent bloom dynamics; rather, it represents a “hinge event” signaling that an important change in NBay ecology then occurred, transitioning this ecosystem into two different “systems” that must be considered in analyzing the long-term patterns in HABs. A conspicuous aspect of this two-system characterization is that three major species in NBay—S. costatum, Heterosigma akashiwo, and Prorocentrum minimum—(see below) all declined in abundance following the 1985 “brown tide” bloom, as did a number of minor bloom species.
The third and particularly significant realization was that HAB behavior in NBay is embedded within long-term patterns that become evident only if the time series is of sufficient duration. The momentum and long-term trajectory in HAB behavior generally, and among individual bloom species, associated with incorporation into long-term rhythms confound efforts to relate HAB behavior to instantaneous measurement of controlling variables. This realization became evident from the long-term cyclical shifts in functional groups (diatoms vs. flagellates) found associated with long-term shifts in nutrient ratios. This relationship and its significance are discussed in greater detail below.
The data analyses resulting from the non-traditional approaches inspired by the three unanticipated realizations cited above—the importance of diatoms to HAB dynamics, the 1985 “hinge event”, and the occurrence of long-term, rhythmic behavior—in combination with the more traditional analytical approaches applied suggest a major hypothesis: that a long-term regime change has occurred in NBay, and in its present phase, HABs have become selected against. The NBay time series is amenable to the required interrogation of whether this is the case and, if so, what primary factors have driven this regime change. The need to confirm whether a regime change has indeed occurred is important because the long-term variability found in HAB dynamics in NBay has many elements in common with HAB behavior generally. The current tendency of HAB scientists to seek explanations for the ongoing global increase in HABs by focusing on ballast water vectoring, shellfish transplantation, eutrophication, or climate change may be misguided. Complex, broad-based ecosystem changes, which are locally or regionally unique, may be the root cause driving some HAB behavior, rather than specific triggering events which may be the proxies for the ecosystem change.
Some Specific Results
Ichthyotoxic H. akashiwo, based on numerical abundance, was the fourth most abundant species in NBay during the period from 1959 to 1980. Since the late 1980s, it has dramatically decreased in abundance. The cause(s) of this decline is (are) obscure: statistical correlations were not found for H. akashiwo abundance when regressed against temperature, irradiance, or nutrients. Grazer regulation as a factor has also been eliminated because H. akashiwo is strongly allelopathic against grazers ranging from microzooplankton to copepods to planktivorous fish. There is tight allelochemic competition between the diatom S. costatum, the major species in NBay, and H. akashiwo, which outcompetes Skeletonema. There is a nearly perfect long-term, inverse annual cycle in the abundance of these two species. The decline in H. akashiwo does not appear to reflect a loss of its experimentally established allelochemical capacity against Skeletonema. The decrease in the annual abundance of H. akashiwo has accompanied the long-term decrease found in chlorophyll, suggesting that its decline is linked to a general ecosystem change that appears to be occurring in NBay that commenced in 1985 when a prodigous, novel, 5-month “brown tide” bloom of the pelagophyte A. anophagefferens occurred. Until this bloom, the annual abundance from 1959 - 1984 was more or less constant. Following the “brown tide,” its abundance began its progressive decline.
Our analyses point to nutrients as being a factor in the post-1985 ecosystem changes found in bloom species selection and their dynamics in NBay. Nutrient measurements begun in 1973, and detrended, exhibit the following long-term patterns: mean annual phosphorus concentrations decreased and silicate concentrations increased, while inorganic nitrogen (NH4 and NO3) concentrations were cyclical. These trends were accompanied by changes in the N:P, Si:N, and Si:P nutrient ratios, and in the ratio of the numerical abundance of functional groups. The ratio of the mean annual diatom-to-flagellate abundance, based on weekly sampling between 1960 and 1996, exhibited a pronounced multidecadal, recurrent oscillation. The diatom : flagellate functional group ratio progressively decreased five-fold, from ca. 5:1 to 1:1, then progressively recovered to ca. 5:1, followed thereafter by a pattern of similar decrease and recovery. Two distinct cycles exhibiting this pattern occurred during the 38-year time series. The trends in the mean annual diatom: flagellate ratio and the ratios of Si:N (range ca. 4.5 to 0.45) and Si:P (range ca. 20 to < 10:1) were strongly and positively correlated. The Spearman r (non parametric) correlation coefficients between the trends in the diatom : flagellate ratio and the Si:P and Si:N ratios were +0.79, and +0.71, respectively, both statistically significant. This demonstration of the importance of the ratio of Si to P or N in regulating functional group occurrences and, specifically, the selection of harmful bloom species, was the first field demonstration in support of the nutrient ratio hypothesis proposed by Smayda in 1989 that changes in the Si:N and Si:P ratios are selection factors in harmful blooms.
Chemostat experiments conducted by us suggest that the nutrient ratio theory, however, is more applicable to the issue of flagellate group selection (i.e., dinoflagellate, raphidophyte, haptophyte, etc.), rather than to individual species’ selections within a phylogenetic group, which remain unpredictable. For example, our analyses suggest that once the raphidophyte H. akashiwo is selected for, blooms exceeding 100 cells m L-1 displayed a linear dependence on pre-bloom inorganic P concentrations (dissolved inorganic P [DIP]). This species has a relatively high P requirement and NBay strains are unable to synthesize alkaline phosphatase which would allow their assimilation of dissolved organic P. Large blooms did not occur if pre-bloom DIP concentrations were < 0.5 μM, while blooms > 1,000 cells mL-1 occurred only at pre-bloom DIP concentrations >1.0 μM. This suggests that the long-term decline in H. akashiwo in NBay, discussed above, may be partly linked to the long-term decline found in DIP.
The dinoflagellate P. minimum also began to decline in abundance in NBay soon after the 1985 A . anophagefferens “brown tide.” There has also been a long-term decline in Prorocentrum triestinum since 1966, and Prorocentrum scutellum has become rare since 1983. P. minimum exhibited maximal abundance during 1972-1987. It was among the 24 most abundant species between 1959 and 1980, but has since fallen to 39th in abundance rank. The decline in its abundance and blooms in NBay is contrary to the progressive increase in its bloom frequency and abundance being found in many coastal regions, and which some investigators attribute to elevated nitrogen concentrations. Correlation analyses indicate nitrogen availability is also a factor in NBay since P. minimum tends to bloom during wet years accompanied by increased NO3 and riverine dissolved organic nitrogen concentrations, but low NH4 concentrations. However, grazing by copepods appears also to be a factor.
Although there is considerable debate over the extent to which HABs are nutrient-regulated, the statistical linkages found between nutrients and their ratios and bloom species behavior is a persistent feature of the NBay time series. This finding does not support the eutrophication theory of HAB formation, but does suggest that the tendency in HAB research to neglect nutrients or to focus only on a given nutrient is not prudent.
Web Site Development
Migration of the multidecadal NBay data bank on HAB species into electronic form was initiated towards development of an Internet-based data access Web site tentatively identifiable as t he Narragansett Bay Plankton Page (NBPP). The University of Rhode Island Environmental Data Center (EDC) will continue to assist in developing this site to reside within the existing Narragansett Bay Web Portal (http://www.narrbay.org Exit ). This portal is designed as the Internet entry point for people who are looking for information about NBay and coastal Rhode Island; it is accessible 24 hours a day, 7 days a week. Once developed, the plankton time series Web Site will be maintained by the EDC and have the capacity to receive new data. The NBPP Web Site will be available for use by the scientific community, State of RI agencies, and other NBay stakeholders. Funds expected from the Rhode Island Sea Grant will help in the development of this Web site.
Other Relevant Activities
- Smayda TJ. Member, U.S. Environmental Protection Agency (EPA) Nutrient Criteria for Estuaries Workgroup. (2005 - ).
- Smayda TJ. Member, Committee on Coastal Indicator for Harmful Algal Blooms, State of the Nation’s Ecosystems Project, H. John Heinz III Center for Science, Economics and the Environment Workshop. (2005).
- Smayda TJ. Invited Participant, H. John Heinz III Center for Science, Economics and the Environment Workshop on the Coastal Indicator for Harmful Algal Blooms, Washington, DC. (May, 2005).
- Smayda TJ. Invited Participant, Workshop on Harmful Algal Research and Response: A National Environmental Science Strategy 2005-2015 (HARNESS). Charleston, SC. (2004).
Future Activities:
Use of the residual funds available on this grant, and requested, will be used primarily for personnel services to help in the processing of data needed for completion of, and assistance in preparing final drafts and revisions of the numerous manuscripts presently in various draft stages that have resulted from this project. These include manuscripts on the long-term bloom dynamics of A. anophagefferens, H. akashiwo, P. minimum and S. costatum sensu lato, and the influence of the Si:P and Si:N ratios on the in situ selection of functional groups and harmful bloom species.
Dr. Smayda will also prepare a manuscript during this period that incorporates the NBay results obtained on this project, to be titled “The Relationship Between Anthropogenic Disturbances and the Global Increase in Harmful Algal Blooms.” He has been invited to present this plenary lecture at the 15th Annual Meeting of the North Pacific Marine Science Organization(PISCES), Yokohama, Japan (13-21 October 2006). In addition, he will complete a manuscript on the 15°C “temperature barrier” for presentation at the XI International Conference on Harmful Algae to be convened in Copenhagen (September, 2006). This manuscript will refine the presentation that he made at the Paris GEOHAB Workshop in December 2005 on Stratification and HABs (see Presentations). I have had to decline the formal presentation of an invited paper on harmful blooms of Cochlodinium polykrikoides in NBay at a workshop to be convened in South Korea in May, 2006, but will prepare a manuscript co-authored with Dr. Carmelo Tomas for publication in the Cochlodinium Workshop proceedings. This will also be undertaken during the requested period of project extension.
Journal Articles:
No journal articles submitted with this report: View all 35 publications for this projectSupplemental Keywords:
coastal ecosystems, harmful algal blooms, HAB ecology, red tide blooms, aquatic ecosystems and estuarine research, Narragansett Bay, East Coast (RI), ECOHAB, Narragansett Bay Time Series (NBTS), ecosystem protection, ecosystem exposure/risk, ecosystem/assessment/indicators, oceanography,, RFA, Scientific Discipline, Air, Geographic Area, Water, Ecosystem Protection/Environmental Exposure & Risk, Ecology, Aquatic Ecosystems & Estuarine Research, estuarine research, Ecosystem/Assessment/Indicators, Ecosystem Protection, Oceanography, climate change, Air Pollution Effects, Ecological Effects - Environmental Exposure & Risk, Aquatic Ecosystem, algal blooms, computing technology, Biology, Atmosphere, East Coast, ecological exposure, environmental monitoring, red tides, Narragansett Bay Time Series (NBTS), harmful algal blooms, marine biology, HAB ecology, coastal environments, data management, ECOHAB, World Wide Web, red tide bloom, Narragansett BayProgress and Final Reports:
Original AbstractThe perspectives, information and conclusions conveyed in research project abstracts, progress reports, final reports, journal abstracts and journal publications convey the viewpoints of the principal investigator and may not represent the views and policies of ORD and EPA. Conclusions drawn by the principal investigators have not been reviewed by the Agency.