A framework for examining climate-driven changes to the seasonality and geographical range of coastal pathogens and harmful algae

Abstract Climate change is expected to alter coastal ecosystems in ways which may have predictable consequences for the seasonality and geographical distribution of human pathogens and harmful algae. Here we demonstrate relatively simple approaches for evaluating the risk of occurrence of pathogenic bacteria in the genus Vibrio and outbreaks of toxin-producing harmful algae in the genus Alexandrium, with estimates of uncertainty, in U.S. coastal waters under future climate change scenarios through the end of the 21st century. One approach forces empirical models of growth, abundance and the probability of occurrence of the pathogens and algae at specific locations in the Chesapeake Bay and Puget Sound with ensembles of statistically downscaled climate model projections to produce first order assessments of changes in seasonality. In all of the case studies examined, the seasonal window of occurrence for Vibrio and Alexandrium broadened, indicating longer annual periods of time when there is increased risk for outbreaks. A second approach uses climate model projections coupled with GIS to identify the potential for geographic range shifts for Vibrio spp. in the coastal waters of Alaska. These two approaches could be applied to other coastal pathogens that have climate sensitive drivers to investigate potential changes to the risk of outbreaks in both time (seasonality) and space (geographical distribution) under future climate change scenarios.

[1]  R. Colwell,et al.  Influence of water temperature, salinity, and pH on survival and growth of toxigenic Vibrio cholerae serovar 01 associated with live copepods in laboratory microcosms , 1984, Applied and environmental microbiology.

[2]  E. Levin,et al.  The toxicology of climate change: environmental contaminants in a warming world. , 2009, Environment international.

[3]  R. Colwell,et al.  Temporal and Spatial Variability in the Distribution of Vibrio vulnificus in the Chesapeake Bay: A Hindcast Study , 2011, EcoHealth.

[4]  L. Hay,et al.  A COMPARISON OF DELTA CHANGE AND DOWNSCALED GCM SCENARIOS FOR THREE MOUNTAINOUS BASINS IN THE UNITED STATES 1 , 2000 .

[5]  D. Willard,et al.  Medieval Warm Period, Little Ice Age and 20th century temperature variability from Chesapeake Bay , 2003 .

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

[7]  P. Hunter Climate change and waterborne and vector‐borne disease , 2003, Journal of applied microbiology.

[8]  Angelo DePaola,et al.  Outbreak of Vibrio parahaemolyticus gastroenteritis associated with Alaskan oysters. , 2005, The New England journal of medicine.

[9]  K. Davies-Vollum,et al.  Spatial Distribution of Benthic Cysts of Alexandrium Catenella in Surface Sediments of Puget Sound, Washington, USA , 2011 .

[10]  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.

[11]  Michael H. Depledge,et al.  Data Mashups: Potential Contribution to Decision Support on Climate Change and Health , 2014, International journal of environmental research and public health.

[12]  M. Waldichuk Paralytic shellfish poisoning in British Columbia , 1980 .

[13]  C. Gugliandolo,et al.  Detection and differentiation of Vibrio vulnificus in seawater and plankton of a coastal zone of the Mediterranean Sea. , 2006, Research in microbiology.

[14]  R. Hill,et al.  Distribution of Vibrio vulnificus in the Chesapeake Bay , 1996, Applied and environmental microbiology.

[15]  E. Lipp,et al.  Plankton composition and environmental factors contribute to Vibrio seasonality , 2009, The ISME Journal.

[16]  A. DePaola,et al.  Vibrio vulnificus and Vibrio parahaemolyticus in U.S. retail shell oysters: a national survey from June 1998 to July 1999. , 2002, Journal of food protection.

[17]  J. Raven,et al.  Changes in pH at the exterior surface of plankton with ocean acidification , 2012 .

[18]  D. Vugia,et al.  Increasing rates of vibriosis in the United States, 1996-2010: review of surveillance data from 2 systems. , 2012, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[19]  C. Y. Kao CHAPTER 4 – Paralytic Shellfish Poisoning , 1993 .

[20]  Rita R. Colwell,et al.  Viewing Marine Bacteria, Their Activity and Response to Environmental Drivers from Orbit , 2013, Microbial Ecology.

[21]  W. Long,et al.  Modeling and forecasting the distribution of Vibrio vulnificus in Chesapeake Bay , 2014, Journal of applied microbiology.

[22]  G. Hallegraeff A review of harmful algal blooms and their apparent global increase , 1993 .

[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]  J. B. Kincer Our Changing Climate , 1939 .

[25]  L. Peperzak Future increase in harmful algal blooms in the North Sea due to climate change. , 2005, Water science and technology : a journal of the International Association on Water Pollution Research.

[26]  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 .

[27]  Vera L. Trainer,et al.  PARALYTIC SHELLFISH TOXINS IN PUGET SOUND, WASHINGTON STATE , 2003 .

[28]  N. Okabe,et al.  Vibrio vulnificus septicaemia in Japan: an estimated number of infections and physicians' knowledge of the syndrome , 2004, Epidemiology and Infection.

[29]  A. Wichels,et al.  Effect of elevated CO 2 on the dynamics of particle-attached and free-living bacterioplankton communities in an Arctic fjord , 2012 .

[30]  K. Koelle The impact of climate on the disease dynamics of cholera. , 2009, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[31]  K. Chew,et al.  Recent developments in pralytic shellfish poisoning research , 1984 .

[32]  Richard P. Stumpf,et al.  An expatriate red tide bloom: Transport, distribution, and persistence , 1991 .

[33]  D. Caron,et al.  Effects of changing pCO2 and phosphate availability on domoic acid production and physiology of the marine harmful bloom diatom Pseudo‐nitzschia multiseries , 2011 .

[34]  Robert J. Olson,et al.  FIRST HARMFUL DINOPHYSIS (DINOPHYCEAE, DINOPHYSIALES) BLOOM IN THE U.S. IS REVEALED BY AUTOMATED IMAGING FLOW CYTOMETRY 1 , 2010 .

[35]  Mercedes Pascual,et al.  Climate change and infectious diseases : Can we meet the needs for better prediction ? , 2013 .

[36]  Shinya Sato,et al.  Genetic Diversity and Distribution of the Ciguatera-Causing Dinoflagellate Gambierdiscus spp. (Dinophyceae) in Coastal Areas of Japan , 2013, PloS one.

[37]  K. Calvin,et al.  The RCP greenhouse gas concentrations and their extensions from 1765 to 2300 , 2011 .

[38]  Vera L. Trainer,et al.  Harmful algal blooms along the North American west coast region: History, trends, causes, and impacts , 2012 .

[39]  Lee-Ann Jaykus,et al.  Climate change and food safety: A review , 2010 .

[40]  Stephanie K. Moore,et al.  Recent trends in paralytic shellfish toxins in Puget Sound, relationships to climate, and capacity for prediction of toxic events , 2009 .

[41]  J. Triñanes,et al.  Emerging Vibrio risk at high latitudes in response to ocean warming , 2013 .

[42]  R. Colwell,et al.  Ocean Warming and Spread of Pathogenic Vibrios in the Aquatic Environment , 2013, Microbial Ecology.

[43]  D. Anderson,et al.  Approaches to monitoring, control and management of harmful algal blooms (HABs). , 2009, Ocean & coastal management.

[44]  Rita R. Colwell,et al.  Predicting the Distribution of Vibrio spp. in the Chesapeake Bay: A Vibrio cholerae Case Study , 2009, EcoHealth.

[45]  Wen Long,et al.  Ecological forecasting in Chesapeake Bay: Using a mechanistic-empirical modeling approach , 2013 .

[46]  S. Ladner,et al.  An evaluation of the use of remotely sensed parameters for prediction of incidence and risk associated with Vibrio parahaemolyticus in Gulf Coast oysters (Crassostrea virginica). , 2007, Journal of food protection.

[47]  J. Raven,et al.  Erratum: Changes in pH at the exterior surface of plankton with ocean acidification (Nature Climate Change (2012) 2 (510-513)) , 2012 .

[48]  C. Baker-Austin,et al.  Spread of Pacific Northwest Vibrio parahaemolyticus strain. , 2013, The New England journal of medicine.

[49]  R. Bidigare,et al.  Centers for Oceans and Human Health: a unified approach to the challenge of harmful algal blooms , 2008, Environmental health : a global access science source.

[50]  R. Colwell,et al.  Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios , 2011, The ISME Journal.

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

[52]  J. Hollibaugh,et al.  Occurrence and distribution of Vibrio vulnificus and Vibrio parahaemolyticus – potential roles for fish, oyster, sediment and water , 2014, Letters in applied microbiology.

[53]  R. Noble,et al.  Mechanistic and statistical models of total Vibrio abundance in the Neuse River Estuary. , 2013, Water research.

[54]  M. Widdowson,et al.  Foodborne Illness Acquired in the United States—Major Pathogens , 2011, Emerging infectious diseases.

[55]  Raymond G. Najjar,et al.  Climate simulations of major estuarine watersheds in the Mid-Atlantic region of the US , 2009 .

[56]  Nigel French,et al.  Climate Variability, Weather and Enteric Disease Incidence in New Zealand: Time Series Analysis , 2013, PloS one.

[57]  R. Najjar,et al.  The response of Chesapeake Bay salinity to climate‐induced changes in streamflow , 2000 .

[58]  C. Brown,et al.  Predicting the distribution of Vibrio vulnificus in Chesapeake Bay , 2010 .

[59]  Stephen H. Jones,et al.  Comparison of the Pathogenic Potentials of Environmental and Clinical Vibrio parahaemolyticus Strains Indicates a Role for Temperature Regulation in Virulence , 2010, Applied and Environmental Microbiology.

[60]  H. Paerl,et al.  Blooms Like It Hot , 2008, Science.

[61]  C. Johnson,et al.  Relationships between Environmental Factors and Pathogenic Vibrios in the Northern Gulf of Mexico , 2010, Applied and Environmental Microbiology.

[62]  B. Preston Observed Winter Warming of the Chesapeake Bay Estuary (1949–2002): Implications for Ecosystem Management , 2004, Environmental management.

[63]  A. DePaola,et al.  Densities of Vibrio vulnificus in the intestines of fish from the U.S. Gulf Coast , 1994, Applied and environmental microbiology.

[64]  N. González-Escalona,et al.  Vibrio parahaemolyticus Diarrhea, Chile, 1998 and 2004 , 2005, Emerging infectious diseases.

[65]  J. Hess,et al.  Ciguatera Fish Poisoning and Climate Change: Analysis of National Poison Center Data in the United States, 2001–2011 , 2014, Environmental health perspectives.

[66]  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.

[67]  J. Triñanes,et al.  Climate anomalies and the increasing risk of Vibrio parahaemolyticus and Vibrio vulnificus illnesses , 2010 .

[68]  R. Whitman,et al.  Efficacy of monitoring and empirical predictive modeling at improving public health protection at Chicago beaches. , 2011, Water research.

[69]  G. Higuera,et al.  Rise and fall of pandemic Vibrio parahaemolyticus serotype O3:K6 in southern Chile. , 2013, Environmental microbiology.

[70]  Scott P. Milroy,et al.  A three-dimensional biophysical model of Karenia brevis dynamics on the west Florida shelf: A look at physical transport and potential zooplankton grazing controls , 2008 .

[71]  M. Kemp,et al.  Potential climate-change impacts on the Chesapeake Bay , 2008 .

[72]  R. Kovats,et al.  Climate change and human health: impacts, vulnerability and public health. , 2006, Public health.

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

[74]  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.

[75]  E. Wood,et al.  Bias correction of monthly precipitation and temperature fields from Intergovernmental Panel on Climate Change AR4 models using equidistant quantile matching , 2010 .