Improving marine disease surveillance through sea temperature monitoring, outlooks and projections

To forecast marine disease outbreaks as oceans warm requires new environmental surveillance tools. We describe an iterative process for developing these tools that combines research, development and deployment for suitable systems. The first step is to identify candidate host–pathogen systems. The 24 candidate systems we identified include sponges, corals, oysters, crustaceans, sea stars, fishes and sea grasses (among others). To illustrate the other steps, we present a case study of epizootic shell disease (ESD) in the American lobster. Increasing prevalence of ESD is a contributing factor to lobster fishery collapse in southern New England (SNE), raising concerns that disease prevalence will increase in the northern Gulf of Maine under climate change. The lowest maximum bottom temperature associated with ESD prevalence in SNE is 12°C. Our seasonal outlook for 2015 and long-term projections show bottom temperatures greater than or equal to 12°C may occur in this and coming years in the coastal bays of Maine. The tools presented will allow managers to target efforts to monitor the effects of ESD on fishery sustainability and will be iteratively refined. The approach and case example highlight that temperature-based surveillance tools can inform research, monitoring and management of emerging and continuing marine disease threats.

[1]  T. Renault,et al.  Effects of temperature on herpes-like virus detection among hatchery-reared larval Pacific oyster Crassostrea gigas , 1996 .

[2]  Scott F. Heron,et al.  NOAA coral reef watch 50 km satellite sea surface temperature-based decision support system for coral bleaching management , 2013 .

[3]  F. Welch,et al.  Causes and Consequences , 2017, Nature.

[4]  T. Soniat.  Epizootiology of Perkinsus marinus disease of eastern oysters in the Gulf of Mexico , 1996 .

[5]  R. Carnegie,et al.  Declining impact of an introduced pathogen: ­Haplosporidium nelsoni in the oyster Crassostrea virginica in Chesapeake Bay , 2011 .

[6]  M. Maldonado,et al.  Recurrent disease outbreaks in corneous demosponges of the genus Ircinia: epidemic incidence and defense mechanisms , 2010 .

[7]  S. Planes,et al.  Temporary refugia for coral reefs in a warming world , 2013 .

[8]  P. Picco,et al.  A catastrophic mass‐mortality episode of gorgonians and other organisms in the Ligurian Sea (North‐western Mediterranean), summer 1999 , 2000 .

[9]  Kenneth R. N. Anthony,et al.  ReefTemp: An interactive monitoring system for coral bleaching using high‐resolution SST and improved stress predictors , 2008 .

[10]  L. E. Jones,et al.  Innate Immunity, Environmental Drivers, and Disease Ecology of Marine and Freshwater Invertebrates , 2006 .

[11]  K. Arrigo,et al.  Climate change influences on marine infectious diseases: implications for management and society. , 2014, Annual review of marine science.

[12]  E. Gaino,et al.  Mortality of commercial sponges: Incidence in two mediterranean areas , 1992 .

[13]  D. Porter,et al.  Nutritional Studies of Labyrinthula Sp. , 1973 .

[14]  C. Goggin,et al.  Perkinsus, a protistan parasite of abalone in Australia: A review , 1995 .

[15]  Tracy L. Pugh,et al.  EPIZOOTIC SHELL DISEASE IN AMERICAN LOBSTER (HOMARUS AMERICANUS) IN MASSACHUSETTS COASTAL WATERS: INTERACTIONS OF TEMPERATURE, MATURITY, AND INTERMOLT DURATION , 2006 .

[16]  B. Stevens.  Effects of epizootic shell disease in American lobster Homarus americanus determined using a quantitative disease index. , 2009, Diseases of aquatic organisms.

[17]  M. Iredell,et al.  The NCEP Climate Forecast System Version 2 , 2014 .

[18]  T. Schram,et al.  Egg production in the salmon louse [Lepeophtheirus salmonis (Kroyer)] in relation to origin and water temperature , 2000 .

[19]  J. Shields,et al.  Dysbiosis in Epizootic Shell Disease of the American Lobster (Homarus americanus) , 2012 .

[20]  R. Smolowitz,et al.  Bacterial Communities Associated with Lesions of Shell Disease in the American Lobster, Homarus americanus Milne-Edwards , 2012 .

[21]  Serge Planes,et al.  Opposite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs , 2014, Global change biology.

[22]  A. Dobson,et al.  Managing marine disease emergencies in an era of rapid change , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[23]  P. Howell.  The Status of the Southern New England Lobster Stock , 2012 .

[24]  Ming Chen,et al.  The Effect of Alkylphenols on Lobster Shell Hardening , 2012 .

[25]  L. A. Leblanc,et al.  Metal Concentrations in Tissues of American Lobsters (Homarus americanus, Milne-Edwards) with Epizootic Shell Disease , 2012 .

[26]  Scott F. Heron,et al.  Summer Hot Snaps and Winter Conditions: Modelling White Syndrome Outbreaks on Great Barrier Reef Corals , 2010, PloS one.

[27]  G. Yohe,et al.  Climate Change Impacts in the United States: The Third National Climate Assessment , 2014 .

[28]  J. Groot,et al.  The Wasting Disease and the Effect of Abiotic Factors (Light-Intensity, Temperature, Salinity) and Infection with Labyrinthula-Zosterae on the Phenolic Content of Zostera-Marina Shoots , 1995 .

[29]  R. Smolowitz,et al.  Exposures of Homarus americanus Shell to Three Bacteria Isolated from Naturally Occurring Epizootic Shell Disease Lesions , 2012 .

[30]  Joleah B. Lamb,et al.  Scuba diving damage and intensity of tourist activities increases coral disease prevalence , 2014 .

[31]  C. D. Harvell,et al.  Ochre star mortality during the 2014 wasting disease epizootic: role of population size structure and temperature , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[32]  Barbara A. Somers,et al.  Observations of Epizootic Shell Disease in American Lobsters, Homarus americanus, in Southern New England , 2012 .

[33]  S. Gorshkov,et al.  World ocean atlas , 1976 .

[34]  J. D. Stuart,et al.  Endocrine-Disrupting Alkylphenols are Widespread in the Blood of Lobsters from Southern New England and Adjacent Offshore Areas , 2012 .

[35]  B. Willis,et al.  A Framework for Responding to Coral Disease Outbreaks that Facilitates Adaptive Management , 2011, Environmental Management.

[36]  H. Laufer,et al.  Identification of Juvenile Hormone-Active Alkylphenols in the Lobster Homarus americanus and in Marine Sediments , 2004, The Biological Bulletin.

[37]  J. Shields,et al.  Overwintering of the parasitic dinoflagellate Hematodinium perezi in dredged blue crabs (Callinectes sapidus) from Wachapreague Creek, Virginia. , 2015, Journal of invertebrate pathology.

[38]  K. Kim,et al.  Characterization of Aspergillus sydowii (Thom et Church), a fungal pathogen of Caribbean sea fan corals , 2001, Hydrobiologia.

[39]  J. Shields,et al.  Epizootiology of the parasitic dinoflagellate Hematodinium sp. in the American blue crab Callinectes sapidus. , 2000, Diseases of aquatic organisms.

[40]  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.

[41]  L. Richardson,et al.  The roles of temperature and light in black band disease (BBD) progression on corals of the genus Diploria in Bermuda. , 2011, Journal of invertebrate pathology.

[42]  Epidemic Mortality of the Sponge Ircinia variabilis (Schmidt, 1862) Associated to Proliferation of a Vibrio Bacterium , 2012, Microbial Ecology.

[43]  N. Demir,et al.  RESPONSE OF THE AMERICAN LOBSTER TO THE STRESS OF SHELL DISEASE , 2009 .

[44]  H. Schuttenberg,et al.  A Strategic Framework for Responding to Coral Bleaching Events in a Changing Climate , 2009, Environmental management.

[45]  R. Noble,et al.  Dynamics and predictive modelling of Vibrio spp. in the Neuse River Estuary, North Carolina, USA. , 2007, Environmental microbiology.

[46]  Eugene M. Burreson,et al.  Epizootiology of Perkinsus marinus disease of oysters in Chesapeake Bay, with emphasis on data since 1985 , 1996 .

[47]  P. A. Heuch,et al.  Population dynamics of salmon lice Lepeophtheirus salmonis on Atlantic salmon and sea trout , 2005 .

[48]  H. Hummel,et al.  Epidemiology of Bonamia ostreae infecting European flat oysters Ostrea edulis from Lake Grevelingen, The Netherlands , 2010 .

[49]  H. Nauwynck,et al.  The effect of raising water temperature to 33 °C in Penaeus vannamei juveniles at different stages of infection with white spot syndrome virus (WSSV) , 2007 .

[50]  V. Savage,et al.  Systematic variation in the temperature dependence of physiological and ecological traits , 2011, Proceedings of the National Academy of Sciences.

[51]  D. E. Aiken.  Chapter 2 – Molting and Growth , 1980 .

[52]  S. Levitus,et al.  World ocean atlas 2013. Volume 1, Temperature , 2002 .

[53]  P. Banning.  Observations on bonamiasis in the stock of the European flat oyster, Ostrea edulis, in the Netherlands, with special reference to the recent developments in Lake Grevelingen , 1991 .

[54]  R. Ostfeld,et al.  Climate Change and Infectious Diseases: From Evidence to a Predictive Framework , 2013, Science.

[55]  B. Worm,et al.  Importance of genetic diversity in eelgrass Zostera marina for its resilience to global warming , 2008 .

[56]  Alan E. Strong,et al.  Remote sensing of sea surface temperatures during 2002 Barrier Reef coral bleaching , 2003 .

[57]  Scott F. Heron,et al.  Caribbean Corals in Crisis: Record Thermal Stress, Bleaching, and Mortality in 2005 , 2010, PloS one.

[58]  J. Lough,et al.  Climate Variability and Change: Monitoring Data and Evidence for Increased Coral Bleaching Stress , 2009 .

[59]  B. Poulos,et al.  Reduced replication of infectious hypodermal and hematopoietic necrosis virus (IHHNV) in Litopenaeus vannamei held in warm water , 2007 .

[60]  Kevin D Lafferty,et al.  The ecology of climate change and infectious diseases. , 2010, Ecology.

[61]  M. Butler,et al.  PaV1 infection in the Florida spiny lobster (Panulirus argus) fishery and its effects on trap function and disease transmission , 2012 .

[62]  R. Scheibling,et al.  Recurrent outbreaks of disease in sea urchins Strongylocentrotus droebachiensis in Nova Scotia: evidence for a link with large-scale meteorologic and oceanographic events , 1997 .

[63]  O. Hoegh‐Guldberg,et al.  Dynamics of a temperature-related coral disease outbreak , 2004 .

[64]  Göran Englund,et al.  Temperature dependence of the functional response. , 2011, Ecology letters.

[65]  A. Dobson,et al.  Emergency response for marine diseases. , 2015, Science.

[66]  Antoine Flahault,et al.  Climate change and infectious diseases , 2016, Public Health Reviews.

[67]  Joleah B. Lamb,et al.  Reserves as tools for alleviating impacts of marine disease , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[68]  H. Nauwynck,et al.  Effect of high water temperature (33 °C) on the clinical and virological outcome of experimental infections with white spot syndrome virus (WSSV) in specific pathogen-free (SPF) Litopenaeus vannamei , 2006 .

[69]  Sang‐Ki Lee,et al.  Downscaled projections of Caribbean coral bleaching that can inform conservation planning , 2015, Global change biology.

[70]  A. Simpson,et al.  Low temperature tolerance of a sea urchin pathogen: Implications for benthic community dynamics in a warming ocean , 2015 .

[71]  B. Brown,et al.  Coral bleaching: causes and consequences , 1997, Coral Reefs.

[72]  Joleah B. Lamb,et al.  Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence , 2015 .

[73]  M. Tourna,et al.  Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. , 2008, Environmental microbiology.

[74]  K. Garver,et al.  Estimation of Parameters Influencing Waterborne Transmission of Infectious Hematopoietic Necrosis Virus (IHNV) in Atlantic Salmon (Salmo salar) , 2013, PloS one.

[75]  K. Paaijmans,et al.  Optimal temperature for malaria transmission is dramatically lower than previously predicted. , 2013, Ecology letters.

[76]  M. Chen,et al.  Ghost of bleaching future : Seasonal Outlooks from NOAA ' s Operational Climate Forecast System , 2012 .

[77]  J. Miller,et al.  The Relationship Between Increasing Sea-surface Temperature and the Northward Spread of Perkinsus marinus (Dermo) Disease Epizootics in Oysters , 1998 .

[78]  Alfred D. Chandler,et al.  The National Marine Fisheries Service , 1988 .

[79]  J. Shields.  Complex etiologies of emerging diseases in lobsters (Homarus americanus) from Long Island Sound1 , 2013 .

[80]  E. Rosenberg,et al.  Microbial diseases of corals and global warming. , 2002, Environmental microbiology.

[81]  B. Willis,et al.  Predicting outbreaks of a climate-driven coral disease in the Great Barrier Reef , 2011, Coral Reefs.

[82]  M. Bally,et al.  Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change , 2007 .

[83]  M. Fogarty,et al.  Distinguishing disease impacts from larval supply effects in a lobster fishery collapse , 2009 .

[84]  P. Boudry,et al.  Temperature influence on pathogen transmission and subsequent mortalities in juvenile Pacific oysters Crassostrea gigas , 2013 .

[85]  C. Audemard,et al.  Infection dynamics of Marteilia refringens in flat oyster Ostrea edulis and copepod Paracartia grani in a claire pond of Marennes-Oléron Bay. , 2004, Diseases of aquatic organisms.

[86]  Peter Cornillon,et al.  The Past, Present, and Future of the AVHRR Pathfinder SST Program , 2010 .

[87]  Causes and consequences , 2021 .

[88]  Calvin S. Y. Chun,et al.  Withering syndrome of the black abalone, Haliotis cracherodii (leach): Water temperature, food availability, and parasites as possible causes , 1997 .

[89]  R. Ostfeld,et al.  Climate Warming and Disease Risks for Terrestrial and Marine Biota , 2002, Science.

[90]  G. Gettinby,et al.  Modelling the Impact of Temperature-Induced Life History Plasticity and Mate Limitation on the Epidemic Potential of a Marine Ectoparasite , 2014, PLoS ONE.

[91]  R. Tjeerdema,et al.  Health and survival of red abalone, Haliotis rufescens, under varying temperature, food supply, and exposure to the agent of withering syndrome. , 2005, Journal of invertebrate pathology.

[92]  B. Walther,et al.  Dietary transfer of enriched stable isotopes to mark otoliths, fin rays, and scales , 2013 .

[93]  Timothy F. R. Burgess,et al.  Reef-Scale Thermal Stress Monitoring of Coral Ecosystems: New 5-km Global Products from NOAA Coral Reef Watch , 2014, Remote. Sens..

[94]  M. Garnier,et al.  Evidence for the Involvement of Pathogenic Bacteria in Summer Mortalities of the Pacific Oyster Crassostrea gigas , 2007, Microbial Ecology.

[95]  M. Breitbart,et al.  Densovirus associated with sea-star wasting disease and mass mortality , 2014, Proceedings of the National Academy of Sciences.

[96]  M. Butler,et al.  Ecological and physiological effects of PaV1 infection on the Caribbean spiny lobster (Panulirus argus Latreille) , 2008 .

[97]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[98]  B. Willis,et al.  Coral disease, environmental drivers, and the balance between coral and microbial associates , 2007 .

[99]  William J. Skirving,et al.  A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions , 2004, Coral Reefs.