Use of a real-time remote monitoring network (RTRM) and shipborne sampling to characterize a dinoflagellate bloom in the Neuse Estuary, North Carolina, USA

Abstract The spatial-temporal distribution of a dinoflagellate bloom dominated or co-dominated by Prorocentrum minimum was examined during autumn through early spring in a warm temperate, eutrophic estuary. The developing bloom was first detected from a web-based alert provided by a network of real-time remote monitoring (RTRM) platforms indicating elevated dissolved oxygen and pH levels in upper reaches of the estuary. RTRM data were used to augment shipboard sampling, allowing for an in-depth characterization of bloom initiation, development, movement, and dissipation. Prolonged drought conditions leading to elevated salinities, and relatively high nutrient concentrations from upstream inputs and other sources, likely pre-disposed the upper estuary for bloom development. Over a 7-month period (October 2001–April 2002), the bloom moved toward the northern shore of the mesohaline estuary, intensified under favorable conditions, and finally dissipated after a major storm. Bloom location and transport were influenced by prevailing wind structure and periods of elevated rainfall. Chlorophyll a within bloom areas averaged 106 ± 13 μg L −1 (mean ± 1 S.E.; maximum, 803 μg L −1 ), in comparison to 20 ± 1 μg L −1 outside the bloom. There were significant positive relationships between dinoflagellate abundance and TN and TP. Ammonium, NO 3 − , and SRP concentrations did not decrease within the main bloom, suggesting that upstream inputs and other sources provided nutrient-replete conditions. In addition, PAM fluorometric measurements (09:00–13:00 h) of maximal PSII quantum yield ( F v / F m ) were consistently 0.6–0.8 within the bloom until late March, providing little evidence of photo-physiological stress as would have been expected under nutrient-limiting conditions. Nitrogen uptake kinetics were estimated for P. minimum during the period when that species was dominant (October–December 2001), based on literature values for N uptake by an earlier P. minimum bloom (winter 1999) in the Neuse Estuary. The analysis suggests that NH 4 + was the major N species that supported the bloom. Considering the chlorophyll a concentrations during October and December and the estimated N uptake rates, phytoplankton biomass was estimated to have doubled once per day. Bloom displacement (January–February) coincided with higher diversity of heterotrophic dinoflagellate species as P. minimum abundance decreased. This research shows the value of RTRM in bloom detection and tracking, and advances understanding of dinoflagellate bloom dynamics in eutrophic estuaries.

[1]  Patricia M. Glibert,et al.  Characterization of the affinity for nitrogen, uptake kinetics, and environmental relationships for Prorocentrum minimum in natural blooms and laboratory cultures , 2003 .

[2]  J. Burkholder,et al.  Real-time remote monitoring of water quality: a review of current applications, and advancements in sensor, telemetry, and computing technologies , 2004 .

[3]  T. Blackburn,et al.  Nitrogen cycling in coastal marine environments , 1988 .

[4]  J. Fuhrman,et al.  Dependent coupling of inorganic and organic nitrogen uptake and regeneration in the plume of the Chesapeake Bay estuary and its regulation by large heterotrophs , 1991 .

[5]  A. E. Greenberg,et al.  Standard methods for the examination of water and wastewater : supplement to the sixteenth edition , 1988 .

[6]  G. Hansen Analysis of the thecal plate pattern in the dinoflagellate Heterocapsa rotundata (Lohmann) comb. nov. (=Katodinium rotundatum (Lohmann) Loeblich) , 1995 .

[7]  J. Burkholder,et al.  Water-column nitrate enrichment promotes decline of eelgrass Zostera manna: evidence from seasonal mesocosm experiments , 1992 .

[8]  G. Harris Phytoplankton Ecology: Structure, Function and Fluctuation , 1986 .

[9]  D. Osmond,et al.  Pollutant Export from Various Land Uses in the Upper Neuse River Basin , 2002, Water environment research : a research publication of the Water Environment Federation.

[10]  J. Cloern PHYTOPLANKTON BLOOM DYNAMICS IN COASTAL ECOSYSTEMS' A REVIEW WITH SOME GENERAL LESSONS FROM SUSTAINED INVESTIGATION OF SAN FRANCISCO , 1996 .

[11]  Viney P. Aneja,et al.  Agricultural ammonia emissions and ammonium concentrations associated with aerosols and precipitation in the southeast United States , 2003 .

[12]  G. McMahon,et al.  Water-quality in the Albemarle-Pamlico drainage basin , 1993 .

[13]  J. Lund,et al.  The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting , 1958, Hydrobiologia.

[14]  Hans W. Paerl,et al.  Environmental controls of phytoplankton bloom dynamics in the Neuse River Estuary, North Carolina, U.S.A. , 1997 .

[15]  R. Fiedler,et al.  The determination of nitrogen-15 by emission and mass spectrometry in biochemical analysis: a review , 1975 .

[16]  A. Jassby INTERANNUAL VARIABILITY AT THREE INLAND WATER SITES: IMPLICATIONS FOR SENTINEL ECOSYSTEMS , 1998 .

[17]  M. Furnas In situ growth rates of marine phytoplankton: approaches to measurement, community and species growth rates , 1990 .

[18]  H. Paerl,et al.  Seasonal and hydrological control of phytoplankton nutrient limitation in the lower Neuse River Estuary, North Carolina , 1991 .

[19]  Hans W. Paerl,et al.  Seasonal phytoplankton composition, productivity and biomass in the Neuse River estuary, North Carolina , 1991 .

[20]  G. Wikfors,et al.  Time-dependent changes in hemocytes of eastern oysters, Crassostrea virginica, and northern bay scallops, Argopecten irradians irradians, exposed to a cultured strain of Prorocentrum minimum , 2005 .

[21]  M. Mallin,et al.  Nitrogen and Phosphorus Imports to the Cape Fear and Neuse River Basins To Support Intensive Livestock Production , 1999 .

[22]  Ø. Moestrup,et al.  Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates , 2000 .

[23]  T. Smayda,et al.  Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea , 1997 .

[24]  P. Juneau,et al.  Evidence for the Rapid Phytotoxicity and Environmental Stress Evaluation Using the PAM Fluorometric Method: Importance and Future Application , 1999 .

[25]  J. Landsberg,et al.  The Effects of Harmful Algal Blooms on Aquatic Organisms , 2002 .

[26]  J. Burkholder,et al.  WATER QUALITY TRENDS AND MANAGEMENT IMPLICATIONS FROM A FIVE-YEAR STUDY OF A EUTROPHIC ESTUARY , 2000 .

[27]  H. Paerl,et al.  Regulation of estuarine primary production by watershed rainfall and river flow , 1993 .

[28]  L. Crowder,et al.  Hypoxia in the Neuse River Estuary: Responses of Blue Crabs and Crabbers , 2001 .

[29]  B. Berland,et al.  Evidence of a new toxin in the red-tide dinoflagellate Prorocentrum minimum , 1997 .

[30]  J. Goering,et al.  UPTAKE OF NEW AND REGENERATED FORMS OF NITROGEN IN PRIMARY PRODUCTIVITY1 , 1967 .

[31]  J. C. Goldman,et al.  Seasonal variations in the utilization of ammonium and nitrate by photoplankton in Vineyard Sound, Massachusetts, USA , 1982 .

[32]  E. G. Vrieling,et al.  Harmful Marine Algal Blooms , 1995 .

[33]  G. Wikfors,et al.  Experimental and Histological Studies of Four Life-History Stages of the Eastern Oyster, Crassostrea virginica, Exposed to a Cultured Strain of the Dinoflagellate Prorocentrum minimum. , 1995, The Biological bulletin.

[34]  Erin R. Haramoto,et al.  Harmful algal blooms in the Chesapeake and Coastal Bays of Maryland, USA: Comparison of 1997, 1998, and 1999 events , 2001 .

[35]  T. Malone,et al.  Influences of river flow on the dynamics of phytoplankton production in a partially stratified estuary , 1988 .

[36]  R. Christian,et al.  Dynamics of NH4+ and NO3− uptake in the water column of the Neuse River Estuary, North Carolina , 1994 .

[37]  C. Gallegos,et al.  Event-scale response of phytoplankton to watershed inputs in a subestuary: Timing, magnitude and location of blooms , 1992 .

[38]  J. W. G. Lund,et al.  A Manual on Methods for Measuring Primary Production in Aquatic Environments. , 1970 .

[39]  Irina Olenina,et al.  Spreading and Establishment of the Potentially Toxic Dinoflagellate Prorocentrum minimum in the Baltic Sea , 2000 .

[40]  B. Berland,et al.  Toxicity of French strains of the dinoflagellate Prorocentrum minimum experimental and natural contaminations of mussels. , 1999, Toxicon : official journal of the International Society on Toxinology.

[41]  H. Paerl,et al.  Annual cycles of phytoplankton community-structure and bloom dynamics in the Neuse River Estuary, North Carolina , 1998 .

[42]  J. Bowen,et al.  Neuse River Estuary Modeling and Monitoring Project Stage 1: Predictions and Uncertainty Analysis of Response to Nutrient Loading Using a Mechanistic Eutrophication Model , 2000 .

[43]  J. McCarthy A UREASE METHOD FOR UREA IN SEAWATER1 , 1970 .

[44]  M. Mallin Phytoplankton ecology of North Carolina estuaries , 1994 .

[45]  J. Burkholder,et al.  Seasonal physical–chemical structure and acoustic Doppler current profiler flow patterns over multiple years in a shallow, stratified estuary, with implications for lateral variability , 2004 .

[46]  James D. Bowen,et al.  A CE-QUAL-W2 Model of Neuse Estuary for Total Maximum Daily Load Development , 2003 .

[47]  G. Wikfors,et al.  Effects of natural and field-simulated blooms of the dinoflagellate Prorocentrum minimum upon hemocytes of eastern oysters, Crassostrea virginica, from two different populations , 2005 .

[48]  T. Smayda,et al.  What is a bloom? A commentary , 1997 .

[49]  Viney P. Aneja,et al.  Trends in Ammonium Concentration in Precipitation and Atmospheric Ammonia Emissions at a Coastal Plain Site in North Carolina, U.S.A. , 2000 .

[50]  A. C. Redfield The biological control of chemical factors in the environment. , 1960, Science progress.

[51]  J. Burkholder,et al.  Type of suspended clay influences lake productivity and phytoplankton community response to phosphorus loading , 1990 .

[52]  J. Burkholder IMPLICATIONS OF HARMFUL MICROALGAE AND HETEROTROPHIC DINOFLAGELLATES IN MANAGEMENT OF SUSTAINABLE MARINE FISHERIES , 1998 .

[53]  Mark E. Borsuk,et al.  Seasonal and long-term nutrient trend decomposition along a spatial gradient in the Neuse river watershed , 2000 .

[54]  F. Colijn,et al.  Direct impact of silicate on the photosynthetic performance of the diatom Thalassiosira weissflogii assessed by on- and off-line PAM fluorescence measurements , 1999 .

[55]  Timothy R. Parsons,et al.  A manual of chemical and biological methods for seawater analysis , 1984 .

[56]  F. Tailor The biology of Dinoflagellates , 1987 .

[57]  Engel G. Vrieling,et al.  TOXIC PHYTOPLANKTON BLOOMS IN THE SEA , 1993 .