Ocean warming since 1982 has expanded the niche of toxic algal blooms in the North Atlantic and North Pacific oceans

Significance This study used high-resolution (daily, quarter-degree resolution) sea-surface temperature records to model trends in growth rates and bloom-season duration for two of the most toxic and widespread harmful algal bloom species indigenous to the North Atlantic and North Pacific oceans. Alexandrium fundyense synthesizes saxitoxin and Dinophysis acuminata synthesizes okadaic acid, which cause the human health syndromes paralytic and diarrhetic shellfish poisoning, respectively. The model provided hindcasts of harmful algal bloom (HAB) events that were consistent with in situ observations from long-term monitoring programs during the same time period. This study provides evidence that increasing ocean temperatures have already facilitated the intensification of these, and likely other, HABs and thus contribute to an expanding human health threat. Global ocean temperatures are rising, yet the impacts of such changes on harmful algal blooms (HABs) are not fully understood. Here we used high-resolution sea-surface temperature records (1982 to 2016) and temperature-dependent growth rates of two algae that produce potent biotoxins, Alexandrium fundyense and Dinophysis acuminata, to evaluate recent changes in these HABs. For both species, potential mean annual growth rates and duration of bloom seasons significantly increased within many coastal Atlantic regions between 40°N and 60°N, where incidents of these HABs have emerged and expanded in recent decades. Widespread trends were less evident across the North Pacific, although regions were identified across the Salish Sea and along the Alaskan coastline where blooms have recently emerged, and there have been significant increases in the potential growth rates and duration of these HAB events. We conclude that increasing ocean temperature is an important factor facilitating the intensification of these, and likely other, HABs and thus contributes to an expanding human health threat.

[1]  H. B. Mann Nonparametric Tests Against Trend , 1945 .

[2]  A. Cembella,et al.  Molecular phylogeny and toxin profiles of Alexandrium tamarense (Lebour) Balech (Dinophyceae) from the west coast of Greenland , 2012 .

[3]  Martin Edwards,et al.  � 2006, by the American Society of Limnology and Oceanography, Inc. Regional climate change and harmful algal blooms in the northeast Atlantic , 2022 .

[4]  N. Adams,et al.  Diarrhetic Shellfish Toxins and Other Lipophilic Toxins of Human Health Concern in Washington State , 2013, Marine drugs.

[5]  Elena Litchman,et al.  A Global Pattern of Thermal Adaptation in Marine Phytoplankton , 2012, Science.

[6]  G. Hays,et al.  Changes in marine dinoflagellate and diatom abundance under climate change , 2012 .

[7]  Stephanie K. Moore,et al.  Past trends and future scenarios for environmental conditions favoring the accumulation of paralytic shellfish toxins in Puget Sound shellfish , 2011 .

[8]  O. Doherty,et al.  Decadal Changes in the World's Coastal Latitudinal Temperature Gradients , 2013, PloS one.

[9]  D. Anderson,et al.  Regulation of growth in an estuarine clone of Gonyaulax tam arensis Lebour: Salinity-dependent temperature responses , 1982 .

[10]  F. V. Van Dolah,et al.  Marine Algal Toxins : Origins , Health Effects , and Their Increased Occurrence , 2006 .

[11]  O. Hoegh‐Guldberg,et al.  Ecological responses to recent climate change , 2002, Nature.

[12]  E. Chang,et al.  CMIP5 multimodel ensemble projection of storm track change under global warming , 2012 .

[13]  D. Anderson,et al.  Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. , 2012, Annual review of marine science.

[14]  Fei-xue Fu,et al.  Global change and the future of harmful algal blooms in the ocean , 2012 .

[15]  Qixing Zhou,et al.  Culture techniques and growth characteristics of Dinophysis acuminata and its prey , 2010 .

[16]  S. Levitus,et al.  Global ocean heat content 1955–2008 in light of recently revealed instrumentation problems , 2007 .

[17]  C. Gobler,et al.  Eutrophication and Harmful Algal Blooms: A Scientific Consensus. , 2008, Harmful algae.

[18]  Gustaaf M. Hallegraeff,et al.  OCEAN CLIMATE CHANGE, PHYTOPLANKTON COMMUNITY RESPONSES, AND HARMFUL ALGAL BLOOMS: A FORMIDABLE PREDICTIVE CHALLENGE 1 , 2010 .

[19]  Stephen Burrell,et al.  First detection of paralytic shellfish poisoning (PSP) toxins in Icelandic mussels (Mytilus edulis): Links to causative phytoplankton species , 2013 .

[20]  T. Smayda,et al.  Complexity in the eutrophication–harmful algal bloom relationship, with comment on the importance of grazing , 2008 .

[21]  P. Sen Estimates of the Regression Coefficient Based on Kendall's Tau , 1968 .

[22]  C. Roesler,et al.  Effects of temperature, irradiance, and salinity on photosynthesis, growth rates, total toxicity, and toxin composition for Alexandrium fundyense isolates from the Gulf of Maine and Bay of Fundy , 2005 .

[23]  James Harle,et al.  Vulnerability of coastal ecosystems to changes in harmful algal bloom distribution in response to climate change: projections based on model analysis , 2014, Global change biology.

[24]  C. Gobler,et al.  Harmful algal blooms and eutrophication: Examining linkages from selected coastal regions of the United States. , 2008, Harmful algae.

[25]  A. Timmermann,et al.  Increasing frequency of extreme El Niño events due to greenhouse warming , 2014 .

[26]  B. Reguera,et al.  Harmful Dinophysis species: A review , 2012 .

[27]  R. Kudela,et al.  An unprecedented coastwide toxic algal bloom linked to anomalous ocean conditions , 2016, Geophysical research letters.

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

[29]  D. Anderson,et al.  Temperature dependence of an estuarine harmful algal bloom: Resolving interannual variability in bloom dynamics using a degree‐day approach , 2014, Limnology and oceanography.

[30]  M. Edwards,et al.  Impact of climate change on marine pelagic phenology and trophic mismatch , 2004, Nature.

[31]  M. LeGresley,et al.  Thirty years – Alexandrium fundyense cyst, bloom dynamics and shellfish toxicity in the Bay of Fundy, eastern Canada , 2014 .

[32]  R. Seager,et al.  Forced and Internal Twentieth-Century SST Trends in the North Atlantic* , 2009 .

[33]  D. Anderson,et al.  EFFECTS OF TEMPERATURE CONDITIONING ON DEVELOPMENT AND GERMINATION OF GONYAULAX TAMARENSIS (DINOPHYCEAE) HYPNOZYGOTES 1 , 1980 .

[34]  T. Knutson,et al.  Multimodel Assessment of Regional Surface Temperature Trends: CMIP3 and CMIP5 Twentieth-Century Simulations , 2013 .

[35]  A. Contreras,et al.  Temperature as a factor regulating growth and toxin content in the dinoflagellate Alexandrium catenella , 2006 .

[36]  E. Bresnan,et al.  Shellfish toxicity in UK waters: a threat to human health? , 2009, Environmental health : a global access science source.

[37]  Clara Deser,et al.  Sea surface temperature variability: patterns and mechanisms. , 2010, Annual review of marine science.

[38]  Sarah C. Swan,et al.  Changing wind patterns linked to unusually high Dinophysis blooms around the Shetland Islands, Scotland , 2014 .

[39]  R. Sutton,et al.  A reversal of climatic trends in the North Atlantic since 2005 , 2016 .

[40]  A. Timmermann,et al.  Enhanced warming over the global subtropical western boundary currents , 2012 .

[41]  D. Anderson,et al.  Temperature and Residence Time Controls on an Estuarine Harmful Algal Bloom: Modeling Hydrodynamics and Alexandrium fundyense in Nauset Estuary , 2015, Estuaries and Coasts.

[42]  A. Timmermann,et al.  The impact of global warming on the tropical Pacific Ocean and El Niño , 2010 .

[43]  C. Gobler,et al.  The influence of anthropogenic nitrogen loading and meteorological conditions on the dynamics and toxicity of Alexandrium fundyense blooms in a New York (USA) estuary , 2010 .

[44]  David A. Siegel,et al.  Climate-driven trends in contemporary ocean productivity , 2006, Nature.

[45]  C. Reynolds,et al.  Community Assembly in Marine Phytoplankton: Application of Recent Models to Harmful Dinoflagellate Blooms , 2001 .

[46]  Lora E Fleming,et al.  Impacts of climate variability and future climate change on harmful algal blooms and human health , 2008, Environmental health : a global access science source.

[47]  D. Anderson,et al.  The effects of growth phase and light intensity on toxin production by Dinophysis acuminata from the northeastern United States , 2011 .

[48]  B. Reguera,et al.  PLANOZYGOTE DIVISION AND OTHER OBSERVATIONS ON THE SEXUAL CYCLE OF SEVERAL SPECIES OF DINOPHYSIS (DINOPHYCEAE, DINOPHYSIALES) 1 , 2008, Journal of phycology.

[49]  C. Gobler,et al.  The interactive roles of temperature, nutrients, and zooplankton grazing in controlling the winter–spring phytoplankton bloom in a temperate, coastal ecosystem, Long Island Sound , 2015 .

[50]  C. Jauzein,et al.  Comparing diatom and Alexandrium catenella/tamarense blooms in Thau lagoon: Importance of dissolved organic nitrogen in seasonally N-limited systems , 2014 .

[51]  D. Anderson,et al.  Effects of inorganic and organic nitrogen and phosphorus on the growth and toxicity of two Alexandrium species from Hong Kong , 2012 .

[52]  Stephanie K. Moore,et al.  An Alexandrium Spp. Cyst Record from Sequim Bay, Washington State, USA, and its Relation to Past Climate Variability 1 , 2012, Journal of phycology.

[53]  Van Dolah Fm Marine algal toxins: origins, health effects, and their increased occurrence. , 2000 .

[54]  H. Theil A Rank-Invariant Method of Linear and Polynomial Regression Analysis , 1992 .

[55]  D. Anderson,et al.  Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. , 2014, Protist.

[56]  M. Ritson,et al.  Outbreak of Diarrhetic Shellfish Poisoning Associated with Mussels, British Columbia, Canada , 2013, Marine drugs.

[57]  T. Barnett,et al.  Anthropogenic Warming of the Oceans: Observations and Model Results , 2006 .

[58]  M. Edwards,et al.  Ecological Status Report: results from the CPR survey 2009 , 2010 .

[59]  C. Gobler,et al.  The emergence of Dinophysis acuminata blooms and DSP toxins in shellfish in New York waters , 2013 .

[60]  R. Feely,et al.  Ocean acidification: the other CO2 problem. , 2009, Annual review of marine science.

[61]  P. C. Reid,et al.  Reorganization of North Atlantic Marine Copepod Biodiversity and Climate , 2002, Science.

[62]  Luis Pedro Coelho,et al.  Structure and function of the global ocean microbiome , 2015, Science.

[63]  M. Kendall Rank Correlation Methods , 1949 .

[64]  Raphael M Kudela,et al.  Harmful algal blooms and climate change: Learning from the past and present to forecast the future. , 2015, Harmful algae.

[65]  Stephanie K. Moore,et al.  Effects of ocean warming on growth and distribution of dinoflagellates associated with ciguatera fish poisoning in the Caribbean , 2015 .

[66]  D. Anderson,et al.  Community assembly and seasonal succession of marine dinoflagellates in a temperate estuary: The importance of life cycle events , 2006 .

[67]  Elena Litchman,et al.  Marine Phytoplankton Temperature versus Growth Responses from Polar to Tropical Waters – Outcome of a Scientific Community-Wide Study , 2013, PloS one.

[68]  Elizabeth C. Kent,et al.  Global analyses of sea surface temperature, sea ice, and night marine air temperature since the late nineteenth century , 2003 .

[69]  B. Reguera,et al.  Dinophysis Toxins: Causative Organisms, Distribution and Fate in Shellfish , 2014, Marine drugs.

[70]  Stephanie K. Moore,et al.  Present-day and future climate pathways affecting Alexandrium blooms in Puget Sound, WA, USA. , 2015, Harmful algae.

[71]  C. Gobler,et al.  Nitrogenous Nutrients Promote the Growth and Toxicity of Dinophysis acuminata during Estuarine Bloom Events , 2015, PloS one.