Marine harmful algal blooms (HABs) in the United States: History, current status and future trends

Abstract

Harmful algal blooms (HABs) are diverse phenomena involving multiple. species and classes of algae that occupy a broad range of habitats from lakes to oceans and produce a multiplicity of toxins or bioactive compounds that impact many different resources. Here, a review of the status of this complex array of marine HAB problems in the U.S. is presented, providing historical information and trends as well as future perspectives. The study relies on thirty years (1990-2019) of data in HAEDAT - the IOC-ICES-PICES Harmful Algal Event database, but also includes many other reports. At a qualitative level, the U.S. national HAB problem is far more extensive than was the case decades ago, with more toxic species and toxins to monitor, as well as a larger range of impacted resources and areas affected. Quantitatively, no significant trend is seen for paralytic shellfish toxin (PST) events over the study interval, though there is clear evidence of the expansion of the problem into new regions and the emergence of a species that produces PSTs in Florida - Pyrodinium bahamense. Amnesic shellfish toxin (AST) events have significantly increased in the U.S., with an overall pattern of frequent outbreaks on the West Coast, emerging, recurring outbreaks on the East Coast, and sporadic incidents in the Gulf of Mexico. Despite the long historical record of neurotoxic shellfish toxin (NST) events, no significant trend is observed over the past 30 years. The recent emergence of diarrhetic shellfish toxins (DSTs) in the U.S. began along the Gulf Coast in 2008 and expanded to the West and East Coasts, though no significant trend through time is seen since then. Ciguatoxin (CTX) events caused by Gambierdiscus dinoflagellates have long impacted tropical and subtropical locations in the U.S., but due to a lack of monitoring programs as well as under-reporting of illnesses, data on these events are not available for time series analysis. Geographic expansion of Gambierdiscus into temperate and non-endemic areas (e.g., northern Gulf of Mexico) is apparent, and fostered by ocean warming. HAB-related marine wildlife morbidity and mortality events appear to be increasing, with statistically significant increasing trends observed in marine mammal poisonings caused by ASTs along the coast of California and NSTs in Florida. Since their first occurrence in 1985 in New York, brown tides resulting from high-density blooms of Aureococcus have spread south to Delaware, Maryland, and Virginia, while those caused by Aureoumbra have spread from the Gulf Coast to the east coast of Florida. Blooms of Margalefidinium polykrikoides occurred in four locations in the U.S. from 1921-2001 but have appeared in more than 15 U.S. estuaries since then, with ocean warming implicated as a causative factor. Numerous blooms of toxic cyanobacteria have been documented in all 50 U.S. states and the transport of cyanotoxins from freshwater systems into marine coastal waters is a recently identified and potentially significant threat to public and ecosystem health. Taken together, there is a significant increasing trend in all HAB events in HAEDAT over the 30-year study interval. Part of this observed HAB expansion simply reflects a better realization of the true or historic scale of the problem, long obscured by inadequate monitoring. Other contributing factors include the dispersion of species to new areas, the discovery of new HAB poisoning syndromes or impacts, and the stimulatory effects of human activities like nutrient pollution, aquaculture expansion, and ocean warming, among others. One result of this multifaceted expansion is that many regions of the U.S. now face a daunting diversity of species and toxins, representing a significant and growing challenge to resource managers and public health officials in terms of toxins, regions, and time intervals to monitor, and necessitating new approaches to monitoring and management. Mobilization of funding and resources for research, monitoring and management of HABs requires accurate information on the scale and nature of the national problem. HAEDAT and other databases can be of great value in this regard but efforts are needed to expand and sustain the collection of data regionally and nationally.

Keywords: Eutrophication; HAB; HAEDAT; Harmful algal bloom; Red tide; Time series.

Fig. 1.

U.S. map showing HAEDAT zones. Some locations discussed in the text are also indicated.

Fig. 2.

The frequency of PST events (defined as at least one closure in a defined region or HAEDAT zone in a given year) in the U.S. derived from HAEDAT. Data include events linked to either A. catenella or P. bahamense. A-D, five-year frequencies, with the size of the circle denoting the number of events during that interval; E, PST frequencies (events per year) for the entire U.S. over the 30-year study interval (1990 – 2019); F, time series of observed (bars) and modeled (line) proportions of monitoring zones with at least one event. Also reported is the fitted linear logistic model and its non-significant p value (p>.05).

Fig. 3.

The HAB Index for western Maine. This metric combines multiple measures of PST toxicity to provide a single value that is indicative of overall severity for each year. Modified from Anderson et al., 2014.

Fig. 4.

The frequency of AST events in the U.S. derived from HAEDAT. A-D, five-year frequencies, with the size of the circle denoting the number of events during that interval; E, AST frequencies (events per year) for the entire U.S. (1991 – 2019); F, time series of observed (bars) and modeled (line) proportions of HAEDAT monitoring zones with at least one event. Also reported is the fitted linear logistic model and its significant p value (p<.05).

Fig. 5.

Time series of AST in Dungeness crab (red) and razor clams (blue) near Long Beach, WA. Monthly razor clam DA at Long Beach provides a 1–2 week early warning of Dungeness crab DA. The crab and clam regulatory limits are shown with red and blue horizontal lines respectively. Source: Washington State Department of Health.

Fig. 6.

Locations where algal toxins were detected in stranded (s) and harvested (h) marine mammals between 2004 and 2013. Red images represent species positive for domoic acid (DA) and purple images represent species positive for saxitoxin (STX). Many species contained both toxins confirming co-exposure. The 13 species that were sampled are listed on the side of the figure in gray (Source: Lefebvre et al., 2016).

Fig. 7.

Increasing trend in cases of California sea lions diagnosed with domoic acid poisoning as recorded at the Marine Mammal Center in Sausalito CA. Dotted line shows the significant regression (p < .05).

Fig. 8

The frequency of DST events in the U.S. derived from HAEDAT. A-D, five-year frequencies, with the size of the circle denoting the number of events during that interval; E, DST frequencies (events per year) for 2008 – 2019; F, time series of observed (bars) and modeled (line) proportions of HAEDAT monitoring zones with at least one event. Also reported is the fitted linear logistic model and its non-significant p value (p>.05).

Fig. 9.

The frequency of NST events in the US derived from HAEDAT. A-D, five-year frequencies, with the size of the circle denoting the number of events during that interval; E, DST frequencies (events per year) for the entire US over the 30 years study interval (1990–2019); F, time series of observed (bars) and modeled (line) proportions of HAEDAT monitoring zones with at least one event. Also reported is the fitted linear logistic model and its non-significant p value (p>.05)

Fig. 10.

NST-related mortality in manatees from 1990–2019. Dotted line shows the significant regression (p < .05). (Data from FWC, 2020)

Fig. 11.

Yearly maximum concentrations of Aureococcus anophagefferens in: A. Narrangansett Bay (Rhode Island, RI), B. Peconic Estuary (New York, NY) C. the south shore estuaries (New York, NY), D. Barnegat Bay (New Jersey, NJ), and E. Chincoteague Bay (Maryland, MD), and Aureoumbra lagunensis in F. eastern Florida estuaries (FL) and G. Baffin Bay (Texas, TX) from 1985 – 2018. ND indicates no detection of brown tide alga. ‗Data not available’ means no data was collected / no data exists. In cases where there is no bar and no ND or ‘data not available’, the densities were detectable but low. Data sources for: Rhode Island (Anderson et al., 1993; Sieburth et al., 1988), all New York estuaries (Suffolk County Department of Health Services, 1985–2018; C.J. Gobler, unpublished), New Jersey (Anderson et al., 1993; Bricelj et al., 2017; Mahoney et al., 2003; M.D. Gastrich, unpublished), Maryland (Maryland Department Nuzzi et al., 1996;of Natural Resources, 2009–2018; Trice et al., 2004), Florida (St. Johns River Management District, 2012–2018), and Texas (Buskey et al., 1997, 1999, 2001; Villareal et al., 2004; Wetz et al., 2017; M. Wetz, unpublished).

Fig. 12.

Change in the duration of the bloom season (days per year) from 1982 to 2016 for M. polykrikoides (American/Malaysian ribotype) along the US East Coast. Stippling (dots) indicates regions where trends were statistically significant (p<.05; Mann–Kendall test). Further analytical detail appears in Griffith et al., 2019b.

Fig. 13.

Time series of all HAEDAT-recorded marine HAB events in the U.S., including PSTs, ASTs, DSTs, NSTs, marine mammal mortalities, and others (defined above). A) Number of events; B) Observed (bars) and modeled (line) proportions of U.S. HAEDAT zones with at least one HAB event. Also reported is the fitted linear logistic model and its significant p value (p<.05).