Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management

Abstract

The public health, tourism, fisheries, and ecosystem impacts from harmful algal blooms (HABs) have all increased over the past few decades. This has led to heightened scientific and regulatory attention, and the development of many new technologies and approaches for research and management. This, in turn, is leading to significant paradigm shifts with regard to, e.g., our interpretation of the phytoplankton species concept (strain variation), the dogma of their apparent cosmopolitanism, the role of bacteria and zooplankton grazing in HABs, and our approaches to investigating the ecological and genetic basis for the production of toxins and allelochemicals. Increasingly, eutrophication and climate change are viewed and managed as multifactorial environmental stressors that will further challenge managers of coastal resources and those responsible for protecting human health. Here we review HAB science with an eye toward new concepts and approaches, emphasizing, where possible, the unexpected yet promising new directions that research has taken in this diverse field.

Fig. 1

Noctiluca scintillans “red tide” at a pristine tourism resort off the east coast of Tasmania, SE Australia, believed to represent a recent climate-driven range extension from Sydney coastal waters (Source: Erin Watson, University of Tasmania).

Fig. 2

Distribution of events where PSP toxins were detected in shellfish or fish– 1970 versus 2009. (Source: US National Office for Harmful Algal Blooms).

Fig.3

Molecular biogeography of the dinoflagellate Alexandrium tamarense/catenella species complex based on large subunit ribosomal RNA sequences. Black arrows indicate natural dispersal, whereas clear arrows suggest human-assisted dispersal. After Scholin et al. 1995; Ruiz Sebastian et al. 2005. [Note, per correspondence between Gustaaf Hallegraeff and Fiona Martin – this figure to be redrawn to be similar to figure 2]

Fig. 4

Oligonucleotide microarray for studies of gene expression in the toxigenic dinoflagellate Alexandrium minutum (Source: I. Yang, Alfred Wegener Institute for Polar and Marine Research). The microarray was derived from the transcriptomic analysis of the corresponding cDNA and sequencing of >15,000 expressed sequence tags (ESTs) (Yang et al. 2010). Gene expression patterns can be determined from automated scanning of the color pattern generated via hybridization and fluorescence labelling.

Fig. 5

Vertical distribution of temperature (°C), particulate total volume (relative units), and fractional cell concentration of dinoflagellates (percentage) off the “pertuls d’Antioche,” France. In this example, the HAB species Dinophysis acuminata was a significant component of the dinoflagellate assemblage at the pycnocline, but was absent elsewhere in the water column. (Modified from Gentien et al. (1995).)

Fig. 6

The Environmental Sample Processor (ESP), a device developed for in situ automated detection of HAB species and toxins (Source: C. Scholin, Monterey Bay Aquarium Research Institute).

Fig. 7

Comparison of observed (a) and modeled (b) surface Alexandrium fundyense cell concentrations during a bloom in the Gulf of Maine (Li et al. 2009). Open circles denote stations sampled. The model slightly underestimates cell concentrations, but does capture the major features of the extensive coastal bloom.

Fig. 8

Locations for a hypothetical array of Environmental Sample Processors (ESPs) to provide an early warning of bloom delivery to coastal shellfish harvesting sites and provide cell abundance data for assimilation into the Alexandrium population dynamics model (modified from Anderson 2008).

Fig.9

Summary diagram of known feedback mechanisms between physicochemical climate variables and biological properties of marine phytoplankton systems. Left: Greenhouse warming raises surface temperatures and causes a shoaling of mixed-layer depths, but can also have broader impacts on global currents, upwelling, and even the deep-ocean conveyor belt. Selected phytoplankton such as coccolithophorids produce dimethylsulfoxide (DMS), acting as cloud condensation nuclei, thereby reducing solar irradiation Middle: Increased atmospheric CO₂ drives the biological pump, can alter phytoplankton species composition, and can alter ocean pH, influencing calcification of coccolithophorids but also nutrient availability. Right: Marine food- web structure, including top-down as well as bottom-up influences on phytoplankton species composition. Other anthropogenic influences in terms of eutrophication, shipping (ballast water introductions), and fishing are also indicated. Without exception, all perturbations will drive changes in phytoplankton (and HAB) species composition.