Perceived global increase in algal blooms is attributable to intensified monitoring and emerging bloom impacts

The global database

As of 10 December 2019 a total of 9503 HAEDAT events had been entered from across the globe, comprising 48% seafood biotoxin, 43% high phytoplankton counts and/or water discolorations causing a socio-economic impact, 7% mass animal or plant mortalities and 2% others (including foam and mucilage production). In a number of HAEDAT records, a single incident was categorised into multiple event types, such as both water discoloration and high phytoplankton count (11% were multiple event types). Among all events linked to seafood toxin syndromes, Paralytic Shellfish Toxins (PST) accounted for 35%, Diarrhetic Shellfish Toxins (DST) 30%, Ciguatera Poisoning (CP) and marine and brackish water cyanobacterial toxins each 9%, Amnesic Shellfish Toxins (AST) 7% and others 10% (including Neurotoxic Shellfish Toxins (NST), Azaspiracid Shellfish Toxins (AZA) and toxic aerosols).

Different OBIS regions (Fig. 1A) contained varying numbers of HAEDAT reports, with the largest number of records available for Europe, followed in order by North Asia, Mediterranean, the east and west coast of North America, the Caribbean, Pacific/Oceania, South East Asia and more limited data sets for South America, and Australia/New Zealand (Supplementary Table 1).

All geographic regions were impacted by multiple HAB types, but in varying proportions (Fig. 1B). High phytoplankton density problems comprised more than 50% of regional HAEDAT records in the Caribbean, Benguela, Mediterranean Sea, North and South East Asia, while seafood toxins and fish kill impacts dominated in all other regions. The productive Benguela upwelling system is prone to mass benthic mortalities linked to high algal biomass and low oxygen¹⁹. Among toxin-related impacts, those caused by PST prevailed in North America, the Caribbean, South America, South East Asia and North Asia, whereas DST were the most frequently recorded in Europe and the Mediterranean (Fig. 1C), and are an emerging threat in the USA. NST were confined to Florida (US), with a single outbreak also reported from New Zealand. Human poisonings from Ciguatera were prominent in the tropical Pacific, the Indian Ocean, Australia and the Caribbean. While HAEDAT records of PST, DST and AST mostly relate to the incidence of phycotoxins in seafood, causing closures of shellfish harvesting areas but rarely being associated with human poisonings, records for Ciguatera (CP) refer almost exclusively to human poisonings reported by medical practitioners. HAB events related to marine cyanotoxins were mainly reported from Australia/New Zealand (ANZ), the Indian Ocean (IND) and the Baltic Sea area in NW Europe (EUR).

Temporal trends in HAB events

The number of HAEDAT events reported for each region per year generally showed increases (Fig. 2A). Specifically, eight of the nine regions showed increases of which six were statistically significant (ECA, CCA, WCA, SEA, MED, EUR; Supplementary Table 1). The meta-analysis of the relationship between HAEDAT events and Year, plotted for each region with the significance level and the confidence intervals adjusted by the effective degrees of freedom (reduced because of autocorrelation) is shown in Fig. 2B. Most of the correlations for the individual regions overlapped zero (i.e. they were not significant), but the overall global total meta-analytic correlation was significant (r = 0.37, z = 2.97, p = 0.003) because it combined the information from each individual region and thus provided more statistical power. This suggests that the number of HAEDAT events is increasing over time. The meta-analysis of the relationship between number of geographic grids with one or more HAB events and Year had similar results but weaker statistical significance (r = 0.27, z = 2.16, p = 0.031, Fig. 2C).

While the number of geographic grids with HAB events is less prone to inconsistencies in what constitutes a HAB event and less affected by sampling effort, to try and adjust more specifically for sampling effort we used OBIS data on microalgae sampling. OBIS data generally showed an increase in sampling effort, although the SAM and NAS regions did not follow this trend (Fig. 3A). Once HAEDAT events were adjusted relative to OBIS observations, there were contrasting trends in standardised HAB events over time, with four regions (SAM, WCA, ANZ and NAS) changing direction compared to the unadjusted HAEDAT data (Fig. 3B vs. Fig. 3A). The meta-analysis of the standardised HAB events showed five of the nine regions with a substantially increasing trend (two flat, and two declining), but there was no statistically significant trend overall when all regions were combined (r = 0.35, z = 1.33, p = 0.18), (Fig. 3C). This implies there is insufficient evidence to conclude that HABs are increasing across all the regions analysed, but it is clear there are contrasting trends in individual regions.

In the period studied, aquaculture production increased 16-fold from a global total 11.35M tonnes in 1985 up to 178.5M tonnes in 2018, with the largest increases occurring SEA and SAM + CCA and with North America (ECA + WCA) and EUR stabilising (Fig. 4A). The number of HAEDAT events over time was significantly correlated with aquaculture production, with all regions with suitable data exhibiting more HAEDAT events as aquaculture expanded, with a strongly significant relationship overall (r = 0.43, z = 3.59, p = 0.0003; Fig. 4B bottom; Supplementary Table 2).

Selected HAB case studies

Further exploring the influence of monitoring efforts, Fig. 5 depicts a 4× fold increase of positive global records between 1985 and 2018 of the main causative organisms of Diarrhetic Shellfish Poisoning (DSP; 84,392 OBIS records of the dinoflagellate genus Dinophysis; Fig. 5A), a 7× fold increase of global observations of the main causative organisms of Amnesic Shellfish Poisoning (ASP; 128,282 records of the diatom genus Pseudo-nitzschia; Fig. 5B) and 6× fold increase of global observations of one of the causative organisms of Paralytic Shellfish Poisoning (PSP; 9887 records of the dinoflagellate genus Alexandrium; Fig. 5C). It should be noted that records for Dinophysis, Pseudo-nitzschia and Alexandrium may also include non-toxic species or strains. In all three cases the clear increase in the number of observations through time of causative organisms is paralleled by the increase of HAEDAT records of the associated toxin syndromes (Fig. 5D–F) which in the case of PSP are contributed also by other species, namely the tropical Pyrodinium bahamense and widespread Gymnodinium catenatum. The occurrence of the causative toxigenic HAB species is not always an accurate predictor for the incidence of human shellfish poisonings (indicated by the shellfish icons in Fig. 5G–I). This reflects the efficiency of the food safety risk management strategies implemented in many of the affected countries. Globally, some 11,000 cases of nonfatal events related to DSP were reported, mostly from Europe, South America and Japan (Fig. 5G). These events mainly include closures of shellfish harvesting areas due to observed levels of DST above regulatory limits to protect human health. It is noted that, despite the widespread distribution of Pseudo-nitzschia species (Fig. 5H), there have been no human fatalities from Amnesic Shellfish Poisoning since the original 1987 incident in Prince Edward Island, Canada (150 illnesses with 3 fatalities), even though associated mortalities of marine mammals of high conservation value are of increasing concern in western North America, including in the climate hotspot of Arctic Alaska³⁶. AST has also been associated with marine mammal calf mortalities in Argentina³⁷. Of the global total of 3800 human Paralytic Shellfish Poisonings during the 1985–2018 period (Fig. 5I), the largest number occurred in the Philippines, a country strongly dependent on aquaculture for human food protein, with 2555 poisonings recorded between 1983 and 2013 of which 165 were fatalities^23,38, predominantly caused by highly toxic Pyrodinium bahamense. Because of the increased use of molecular detection methods our knowledge on the global distribution of ciguatera- causing organisms, selected species of the benthic dinoflagellates Gambierdiscus and Fukuyoa, has increased considerably (Fig. 6A). The database on the presence of ciguatoxins in fish (Fig. 6B) is still limited because of the complexity of the chemical analysis used to confirm the presence of ciguatoxins. Exploring trends of human CP, in Hawaii poisonings have been decreasing, in French Polynesia and the Caribbean numbers remained stable, whereas CP is a new phenomenon in the Canary Islands (Fig. 6C). Globally CP affects 10,000–50,000 people annually but fatalities are rare²⁰.

Aquacultured finfish mortalities caused by the taxonomically unrelated microalgal genera Chattonella, Pseudochattonella, Heterosigma, Karenia, Karlodinium, Margalefidinium (Cochlodinium) and Prymnesium/ Chrysochromulina globally account for much greater economic damage than HABs contaminating seafood³⁹. While most shellfish toxins have now been well characterised and are effectively monitored and regulated, finfish held captive in intensive aquaculture operations continue to be vulnerable to HABs (USD71M loss in Japan in 1972, USD70M in Korea in 1995, USD290M in China in 2012, USD100M in Norway in 2019^{19,20,21,22,23,24,25,26,27,28,29,30,31,32}), even though the causative ichthyotoxins usually are of no human health significance. The 2016 Chilean salmon mortality that caused a record USD800M loss led to major social unrest⁴⁰. Again, the incidence of fish-killing HAB species is not an accurate predictor of economic losses. For example, Heterosigma blooms occur both on the west and east coast of North America, but fish mortalities are mostly confined to the west coast²⁹. In large part, this reflects locations where blooms occur relative to the location and size of the aquaculture operations. The dinoflagellate Karlodinium australe never caused any problems in its Australian lagoon type locality⁴¹ but in 2014 killed 50,000 caged fish in Malaysia and is now also known from Japan and the Philippines⁴². In the wild, finfish can swim away from bloom areas, hence aquaculture finfish mortality is largely a human-generated problem.

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