Harmful algal blooms and eutrophication: Examining linkages from selected coastal regions of the United States

Coastal waters of the United States (U.S.) are subject to many of the major harmful algal bloom (HAB) poisoning syndromes and impacts. These include paralytic shellfish poisoning (PSP), neurotoxic shellfish poisoning (NSP), amnesic shellfish poisoning (ASP), ciguatera fish poisoning (CFP) and various other HAB phenomena such as fish kills, loss of submerged vegetation, shellfish mortalities, and widespread marine mammal mortalities. Here, the occurrences of selected HABs in a selected set of regions are described in terms of their relationship to eutrophication, illustrating a range of responses. Evidence suggestive of changes in the frequency, extent or magnitude of HABs in these areas is explored in the context of the nutrient sources underlying those blooms, both natural and anthropogenic. In some regions of the U.S., the linkages between HABs and eutrophication are clear and well documented, whereas in others, information is limited, thereby highlighting important areas for further research.     

沿岸海域富营养化与赤潮发生的关系

综述了赤潮的发生与沿岸海域富营养化的关系。近几十年来,人类活动使得天然水体的富营养化进程大大加速。营养负荷的增加与高生物量水华的增多相联系。控制营养输入后,浮游植物生物量或有害藻类水华事件也相应减少。营养的组成与浮游植物的种类组成及水华的形成有密切联系。有机营养对有害藻类水华的促进作用受到关注。营养输入时机影响浮游植物种间竞争的结果,因而对浮游植物的群落演替具有深远影响。由于浮游植物存在生理差异,因而对营养加富的反应因种而异。营养在调控某些有毒藻类的毒素产量方面也发挥着重要作用。此外,营养输入与藻类水华之间存在复杂的间接联系。当然,营养状况并非浮游植物群落演替的唯一决定因素。研究结果提示,控制营养输入、减缓水域富营养化是减少有害藻类水华发生的有效途径,而深入研究典型有害藻类的营养生理对策则为防治并最终消除有害藻类水华提供了理论基础。     

赤潮的分类分级标准及预警色设置

为便于赤潮信息的发布、统计和管理,依据我国赤潮发生的特点初步制定了我国赤潮的分类分级及预警色划分的标准。根据形成赤潮的生物种类特性及其对人类健康和近岸水产养殖的影响,将我国赤潮分为有毒赤潮、鱼毒赤潮、有害赤潮和无害赤潮4种类型,考虑到我国沿海赤潮发生面积和持续时间相差巨大,将我国赤潮分为大型、中型和小型3个级别。由此,将我国赤潮分为12种,并依次用不同颜色和符号代表之,以利于在媒体上发布。在此基础上,制定了不同类型赤潮的预警机制和管理措施,为赤潮防灾减灾工作提供参考。     

Applied simulations and integrated modelling for the understanding of toxic and harmful algal blooms (ASIMUTH): Integrated HAB forecast systems for Europe's Atlantic Arc

Reasons for the emergent interest in HABs are abundant, including concerns associated with human health, adverse effects on biological resources, economic losses attributed to recreation, tourism and seafood related industries, and the cost of maintaining public advisory services and monitoring programs for shellfish toxins and water quality. The impact of HABs can potentially be mitigated by early warning of their development. In this regard the project ASIMUTH (Applied Simulations and Integrated Modelling for the Understanding of Toxic and Harmful algal blooms) was borne in order to develop short term HAB alert systems for Atlantic Europe. This was achieved using information on the most current marine conditions (weather, water characteristics, toxicity, harmful algal presence etc.) combined with high resolution local numerical predictions. This integrated, multidisciplinary, trans-boundary approach to the study of HABs developed during ASIMUTH led to a better understanding of the physical, chemical and ecological factors controlling these blooms, as well as their impact on human activities. The outcome was an appropriate alert system for an effective management of areas that are usually associated with HAB events and where these episodes may have a more significant negative impact on human activities. Specifically for the aquaculture industry, the information provided enabled farmers to adapt their working practices in time to prevent mortalities in finfish farms and/or manage their shellfish harvest more effectively. This paper summarises the modelling and alert developments generated by the ASIMUTH project.     

Red to red - the marine bacterium Hahella chejuensis and its product prodigiosin for mitigation of harmful algal blooms

Harmful algal blooms (HABs), commonly called red tides, are caused by some toxic phytoplanktons, and have made massive economic losses as well as marine environmental disturbances. As an effective and environment-friendly strategy to control HAB outbreaks, biological methods using marine bacteria capable of killing the harmful algae or algicidal extracellular compounds from them have been given attention. A new member of the gamma-Proteobacteria, Hahella chejuensis KCTC 2396, was originally isolated from the Korean seashore for its ability to secrete industrially useful polysaccharides, and was characterized to produce a red pigment. This pigment later was identified as an alkaloid compound, prodigiosin. During the past several decades, prodigiosin has been extensively studied for its medical potential as immunosuppressants and antitumor agents, owing to its antibiotic and cytotoxic activities. The lytic activity of this marvelous molecule against Cochlodinium polykrikoides cells at very low concentrations (1 ppb) was serendipitously detected, making H. chejuensis a strong candidate among the biological agents for HAB control. This review provides a brief overview of algicidal marine bacteria and their products, and describes in detail the algicidal characteristics, biosynthetic process, and genetic regulation of prodigiosin as a model among the compounds active against red-tide organisms from the biochemical and genetic viewpoints.     

Different terms used to describe "red tides"

An event characterized by sudden increase in phytoplankton population, in the sea or aqueous environment, is often designated by different Spanish terms that attempt to describe the nature, aspect, characteristics, and/or properties of such phenomena. In this communication, we discuss the convenience of reaching an agreement among the Spanish-speaking scientific community to use a simple Spanish term that could be much more informative and accurate when referring to Harmful Algal Blooms (HABs), in general. Summarizing the different Spanish terms historically employed to describe the proliferation of noxious phytoplankton in the sea, we propose "Proliferación Microalgal Nociva" (PMN = HAB) as a term that, on the basis of its etymological meaning could be considered correct. Its use could help to avoid the prevailing confusion in our language caused by different misleading terms now employed when referring to a Harmful Algal Bloom event.     

Meta‐analysis reveals enhanced growth of marine harmful algae from temperate regions with warming and elevated CO2 levels

Elevated pCO₂ and warming may promote algal growth and toxin production, and thereby possibly support the proliferation and toxicity of harmful algal blooms (HABs). Here, we tested whether empirical data support this hypothesis using a meta‐analytic approach and investigated the responses of growth rate and toxin content or toxicity of numerous marine and estuarine HAB species to elevated pCO₂ and warming. Most of the available data on HAB responses towards the two tested climate change variables concern dinoflagellates, as many members of this phytoplankton group are known to cause HAB outbreaks. Toxin content and toxicity did not reveal a consistent response towards both tested climate change variables, while growth rate increased consistently with elevated pCO₂. Warming also led to higher growth rates, but only for species isolated at higher latitudes. The observed gradient in temperature growth responses shows the potential for enhanced development of HABs at higher latitudes. Increases in growth rates with more CO₂ may present an additional competitive advantage for HAB species, particularly as CO₂ was not shown to enhance growth rate of other non‐HAB phytoplankton species. However, this may also be related to the difference in representation of dinoflagellate and diatom species in the respective HAB and non‐HAB phytoplankton groups. Since the proliferation of HAB species may strongly depend on their growth rates, our results warn for a greater potential of dinoflagellate HAB development in future coastal waters, particularly in temperate regions.     

Development of an oligonucleotide microarray for the detection and monitoring of marine dinoflagellates

Harmful Algal Blooms (HABs), mainly caused by dinoflagellates and diatoms, have great economic and sanitary implications. An important contribution for the comprehension of HAB phenomena and for the identification of risks related to toxic algal species is given by the monitoring programs. In the microscopy-based monitoring methods, harmful species are distinguished through their morphological characteristics. This can be time consuming and requires great taxonomic expertise due to the existence of morphologically close-related species. The high throughput, automation possibility and specificity of microarray-based detection assay, makes this technology very promising for qualitative detection of HAB species. In this study, an oligonucleotide microarray targeted to the ITS1-5.8S-ITS2 rDNA region of nine toxic dinoflagellate species/clades was designed and evaluated. Two probes (45-47 nucleotides in length) were designed for each species/clade to reduce the potential for false positives. The specificity and sensitivity of the probes were evaluated with ITS1-5.8S-ITS2 PCR amplicons obtained from 20 dinoflagellates cultured strains. Cross hybridization experiments confirmed the probe specificity; moreover, the assay showed a good sensitivity, allowing the detection of up to 2 ng of labeled PCR product. The applicability of the assay with field samples was demonstrated using net concentrated seawater samples, un-spiked or spiked with known amounts of cultured cells. Despite the general application of microarray technology for harmful algae detection is not new, a peculiar group of target species/clades has been included in this new-format assay. Moreover, novelties regarding mainly the probes and the target rDNA region have allowed sensitivity improvements in comparison to previously published studies.     

Occurrences of harmful algal blooms (HABs) associated with ocean environments in the South China Sea

Harmful algal blooms (HABs) occur frequently in the South China Sea (SCS), causing enormous economic losses in aquaculture. We analyzed historical HAB records during the period from 1980 to 2003 in SCS. We found that HABs-affected areas have expanded and the frequency of HABs varied during this period. The seasonal and annual variations, as well as causative algal species of HABs are different among the four regions. Areas with frequent HABs include the Pearl River Estuary (China), the Manila Bay (the Philippines), the Masinloc Bay (the Philippines), and the western coast of Sabah (Malaysia). HABs occurred frequently during March–May in the northern region of SCS, May–July in the eastern region, July in the western region, and year-round in the southern region. Among the species that cause HABs, Noctiluca scintillans dominated in the northern region, and Pyrodinium bahamense in the southern and eastern regions. Causative species also varied in different years for the entire SCS. Both P. bahamense and N. scintillans were the dominant species during 1980–2003. Some species not previously recorded formed blooms during 1991–2003, including Phaeocystis globosa, Scrippsiella trochoidea, Heterosigma akashiwo, and Mesodinium rubrum. Variations in HABs are related to various regional conditions, such as a reversed monsoon wind in the entire SCS, river discharges in the northern area, upwelling in Vietnam coastal waters during southwest winds and near Malaysia coastal waters during northeast winds, and eutrophication from coastal aquaculture in the Pearl River estuary, Manila Bay, and Masinloc Bay. Handling editor: D. Hamilton     

High-resolution spatio-temporal distribution of a coastal phytoplankton bloom using laser in situ scattering and transmissometry (LISST)

Development of optical observation technologies provides new insights into harmful algal bloom (HAB) detection and assessment of HAB species dynamics. Based on preliminary laboratory tests, a laser in situ scattering and transmissometry instrument (LISST-100X) was used to monitor a high-biomass phytoplankton proliferation in the field. Short-term spatial and temporal changes in particle size distribution were measured during a recurrent Alexandrium taylori outbreak. Since the bloom was not monospecific, a size-fraction method to discriminate particular species from LISST-100X measurements was proposed. The results were validated to simultaneous microscopic counts of phytoplankton, and the significantly positive correlation obtained between the two methodologies confirmed the instrument's ability to discriminate phytoplankton at the group and species level. The LISST-100X obtains high-resolution in situ data, and is therefore a better alternative than the traditional microscope for assessing temporal and spatial evolution of HABs. Field observations showed high variability over a short time scale associated with diel vertical migration of A. taylori and the whole phytoplankton population (nanoplankton and microplankton). A numerical circulation model was used to investigate the influence of beach hydrodynamics in the observed horizontal variability. Simulations of the model suggested an important role of daily coastal circulation in determining the distribution of A. taylori in coastal environments.     

Spatial, seasonal and species variations of harmful algal blooms in the South Yellow Sea and East China Sea

The occurrences of harmful algal blooms (HABs), in terms of frequency and area in the Chinese coastal waters, have been increasing since 1980s and caused considerable economic losses. In the present study, we have analyzed spatial and seasonal characteristics of HAB events in the southern Yellow Sea and East China Sea along Chinese coast from 1933 to 2004. With a total 435 HAB records, the most frequent HAB occurrence area (FHA) is off the Yangtze River mouth and another two FHA areas are located south of the Yangtze River estuary along about isobaths of 30–60 m coastal water in the East China Sea. The time of HAB occurrence shifted during our study period: from autumn (August–October) before 1980s to July–August in 1980s, during May–July in 1990s, and May–June for the period of 2000–2004. Causative species were found to be different: Noctiluca scintillans and Skeletonema costatum were dominant causative species prior to 2000; and Prorocentrum donghaiense Lu was dominant from 2000 to 2004 and also caused large blooms in May. Trichodesmium sp. caused many HABs in autumn (August–October) prior to 1980s with only one HAB between 1980 and 2004. The changes of the dominant HAB species may have affected the timings of HAB occurrence, as well as the increasing HAB-affected areas in recent years.     

Fiber-optic microarray for simultaneous detection of multiple harmful algal bloom species

Harmful algal blooms (HABs) are a serious threat to coastal resources, causing a variety of impacts on public health, regional economies, and ecosystems. Plankton analysis is a valuable component of many HAB monitoring and research programs, but the diversity of plankton poses a problem in discriminating toxic from nontoxic species using conventional detection methods. Here we describe a sensitive and specific sandwich hybridization assay that combines fiber-optic microarrays with oligonucleotide probes to detect and enumerate the HAB species Alexandrium fundyense, Alexandrium ostenfeldii, and Pseudo-nitzschia australis. Microarrays were prepared by loading oligonucleotide probe-coupled microspheres (diameter, 3 mum) onto the distal ends of chemically etched imaging fiber bundles. Hybridization of target rRNA from HAB cells to immobilized probes on the microspheres was visualized using Cy3-labeled secondary probes in a sandwich-type assay format. We applied these microarrays to the detection and enumeration of HAB cells in both cultured and field samples. Our study demonstrated a detection limit of approximately 5 cells for all three target organisms within 45 min, without a separate amplification step, in both sample types. We also developed a multiplexed microarray to detect the three HAB species simultaneously, which successfully detected the target organisms, alone and in combination, without cross-reactivity. Our study suggests that fiber-optic microarrays can be used for rapid and sensitive detection and potential enumeration of HAB species in the environment.     

Physical transport processes affect the origins of harmful algal blooms in estuaries

The effects of physical transport processes on the initiation of harmful algal blooms (HABs) in estuaries were investigated through both mathematical model analysis and numerical model experiments. This study highlights the influence of the flushing effect due to physical transport processes on the location of bloom initiation, which is comparable to or even more important than local processes. The theoretical analysis suggests that the differential flushing effect at different waterbodies due to complex geometry is one of the dominant factors causing inhomogeneous distribution of algal density during HAB initiation. The ratio of residence time to volume is one of the key variables that determine the differential timing of HAB occurrence in estuary-subestuary systems with multiple interconnected waterbodies. As a result, a HAB tends to be observed first in those locations with relatively long residence time and small waterbodies, such as tributaries or areas with large eddies. Multiple unconnected originating locations can co-exist within an estuary.Two three-dimensional model experiments with realistic forcings were conducted to demonstrate the flushing effect on annual Cochlodinium polykrikoides bloom in the lower James River. The results show that while the environmental conditions that affect local processes, such as salinity and temperature, are important in determining the originating locations of HABs, the differential flushing effect is the dominant factor driving the spatial difference in the density of C. polykrikoides in this region during the bloom initiation. This explains why the occurrence of the first bloom in this region is frequently observed in the Lafayette River, a relatively small waterbody with long residence time. Because of the relatively low growth rate of C. polykrikoides and because of the high water-exchange between the mainstem and tributaries of the James River, initial cyst distribution is suggested to have a relatively small impact on originating locations of the bloom compared to flushing effect and salinity, and the HAB originating locations do not have to be in the waterbody with abundant cysts.     

Satellite discrimination of Karenia mikimotoi and Phaeocystis harmful algal blooms in European coastal waters: Merged classification of ocean colour data

The detection of dense harmful algal blooms (HABs) by satellite remote sensing is usually based on analysis of chlorophyll-a as a proxy. However, this approach does not provide information about the potential harm of bloom, nor can it identify the dominant species. The developed HAB risk classification method employs a fully automatic data-driven approach to identify key characteristics of water leaving radiances and derived quantities, and to classify pixels into “harmful”, “non-harmful” and “no bloom” categories using Linear Discriminant Analysis (LDA). Discrimination accuracy is increased through the use of spectral ratios of water leaving radiances, absorption and backscattering. To reduce the false alarm rate the data that cannot be reliably classified are automatically labelled as “unknown”. This method can be trained on different HAB species or extended to new sensors and then applied to generate independent HAB risk maps; these can be fused with other sensors to fill gaps or improve spatial or temporal resolution. The HAB discrimination technique has obtained accurate results on MODIS and MERIS data, correctly identifying 89% of Phaeocystis globosa HABs in the southern North Sea and 88% of Karenia mikimotoi blooms in the Western English Channel. A linear transformation of the ocean colour discriminants is used to estimate harmful cell counts, demonstrating greater accuracy than if based on chlorophyll-a; this will facilitate its integration into a HAB early warning system operating in the southern North Sea.     

Eutrophication and harmful algal blooms: A scientific consensus

In January 2003, the US Environmental Protection Agency sponsored a “roundtable discussion” to develop a consensus on the relationship between eutrophication and harmful algal blooms (HABs), specifically targeting those relationships for which management actions may be appropriate. Academic, federal, and state agency representatives were in attendance. The following seven statements were unanimously adopted by attendees based on review and analysis of current as well as pertinent previous data:

• (1)Degraded water quality from increased nutrient pollution promotes the development and persistence of many HABs and is one of the reasons for their expansion in the U.S. and other nations;
• (2)The composition–not just the total quantity–of the nutrient pool impacts HABs;
• (3)High-biomass blooms must have exogenous nutrients to be sustained;
• (4)Both chronic and episodic nutrient delivery promote HAB development;
• (5)Recently developed tools and techniques are already improving the detection of some HABs, and emerging technologies are rapidly advancing toward operational status for the prediction of HABs and their toxins;
• (6)Experimental studies are critical to further the understanding about the role of nutrients in HABs expression, and will strengthen prediction and mitigation of HABs; and
• (7)Management of nutrient inputs to the watershed can lead to significant reduction in HABs.

Supporting evidence and pertinent examples for each consensus statement are provided herein.     

Fiber-Optic Microarray for Simultaneous Detection of Multiple Harmful Algal Bloom Species

Harmful algal blooms (HABs) are a serious threat to coastal resources, causing a variety of impacts on public health, regional economies, and ecosystems. Plankton analysis is a valuable component of many HAB monitoring and research programs, but the diversity of plankton poses a problem in discriminating toxic from nontoxic species using conventional detection methods. Here we describe a sensitive and specific sandwich hybridization assay that combines fiber-optic microarrays with oligonucleotide probes to detect and enumerate the HAB species Alexandrium fundyense, Alexandrium ostenfeldii, and Pseudo-nitzschia australis. Microarrays were prepared by loading oligonucleotide probe-coupled microspheres (diameter, 3 μm) onto the distal ends of chemically etched imaging fiber bundles. Hybridization of target rRNA from HAB cells to immobilized probes on the microspheres was visualized using Cy3-labeled secondary probes in a sandwich-type assay format. We applied these microarrays to the detection and enumeration of HAB cells in both cultured and field samples. Our study demonstrated a detection limit of approximately 5 cells for all three target organisms within 45 min, without a separate amplification step, in both sample types. We also developed a multiplexed microarray to detect the three HAB species simultaneously, which successfully detected the target organisms, alone and in combination, without cross-reactivity. Our study suggests that fiber-optic microarrays can be used for rapid and sensitive detection and potential enumeration of HAB species in the environment.     

Differences in serotonergic neurotransmission between rats displaying high or low anxiety/depression-like behaviour: effects of chronic paroxetine treatment

Disturbances in serotonergic neurotransmission have been suggested to be closely interlinked with hyperactivity of the hypothalamic-pituitary-adrenocortical (HPA) system, and are likely to be involved in the pathophysiology of anxiety disorders and major depression. We therefore investigated markers of serotonergic transmission and their modulation by chronic paroxetine in rats selectively bred for high (HAB) or low (LAB) anxiety-related behaviour, both under basal conditions and in response to emotional stress. Hippocampal serotonin 1 A (5-HT1A) receptor mRNA expression was reduced in HAB rats, whereas 5-HT concentrations in hippocampal microdialysates did not differ between HAB and LAB rats under basal conditions. In the hippocampus, overall expression of serotonin transporter binding sites was increased in HAB compared with LAB rats. Exposure to emotional stress failed to increase intrahippocampal 5-HT release in HAB rats whereas LAB rats displayed a physiological, albeit small rise. Chronic paroxetine treatment markedly increased the stress-induced rise in hippocampal 5-HT in HAB, but not LAB rats. This effect may be (at least in part) related to a greater down-regulation of hippocampal serotonin transporter binding sites by paroxetine in HABs compared with LABs, while 5-HT1A receptor expression remained unaffected in this brain area. The findings indicate reduced hippocampal serotonergic transmission in HAB rats as compared with LAB rats, which is evident both at the presynaptic (5-HT release) and the postsynaptic (5-HT1A receptor) level. Chronic paroxetine enhanced the presynaptic responsivity in HAB rats, but not LAB rats, pointing to a preferential efficacy of paroxetine in rats with enhanced anxiety/depression-related behaviour.     

The Diversity of Harmful Algal Bloom-Triggering Mechanisms and the Complexity of Bloom Initiation

Mechanisms influencing initiation of harmful algal blooms (HABs) are diverse, and are not likely to be mutually exclusive. Rather, initiation of HABs is a result of interactions between processes, which result in biological, physical, and chemical conditions optimal for a bloom. Due to the complexity of some bloom initiation processes, bloom-preventative management may be possible. Results from a modeling exercise and a laboratory experiment indicated that a phytoplankton bloom could be circumvented through manipulation of the nutrient-loading mode, i.e., pulsed vs. continuous loading. These findings, should they prove consistent in more robust field experiments, may provide insights for the development of new management approaches for some HABs. Optimal bloom conditions, however, vary between HAB species. Consequently, it is unlikely that a single management solution will exist. Preventative management efforts will require early warning of HAB initiation, perhaps even before the appearance of an HAB species. An indicator based on the dynamic nature of phytoplankton succession events and phytoplankton species diversity may prove useful for this purpose. Applying this index to an existing plankton data set showed that Microcystis blooms might have been predicted months before the start of the bloom.     

东海春季水华期浮游植物生长与微型浮游动物摄食

2005年4～6月在东海有害水华频发区14个站位采样,通过现场稀释法实验对春季东海水域浮游植物比生长率和微型浮游动物比摄食率进行了研究.结果表明东海有害水华频发区浮游植物群落以甲藻为优势.浮游植物比生长率在水华爆发前相对较低,平均为1.18 d~(-1);进入水华期后比生长率明显升高,但在水华站位随现存量增加而降低;非水华区比生长率近岸高、远岸低.微型浮游动物主要以急游虫和桡足类幼体为主,而种类上以砂壳纤毛虫居多.微型浮游动物比摄食率在水华爆发前波动较大,介于0.53～1.73 d~(-1),平均为0.90 d~(-1);在水华区比摄食率较为稳定,浮游植物比生长率的降低导致群落净生长率持续下降;在非水华区,比摄食率整体较高,近岸低而远岸高.微型浮游动物的摄食对浮游植物群落的生长有一定的控制作用,但在水华爆发后这种控制作用将减弱.     

The value of harmful algal bloom predictions to the nearshore commercial shellfish fishery in the Gulf of Maine

In this study, we develop a framework for measuring the value of harmful algal bloom (HAB) predictions. The framework captures the effects of both private and public responses to HABs. Using data from the New England nearshore commercial shellfish fishery and impact estimates for a large-scale HAB event in 2005, we illustrate how the potential value of HAB forecasts may be estimated. The results of our study suggest that the long-term value of a HAB prediction and tracking system for the Gulf of Maine is sensitive to the frequency of HAB events, the accuracy of predictions, the choice of HAB impact measures, and the effectiveness of public and private responses.