Science Backgrounder: Marine Disease and Climate Change

Marine ecosystems are ecologically, economically, and socially essential. While humans derive obvious benefits from marine ecosystems like food from fisheries and income from tourism, all living organisms benefit from a diverse array of marine ecosystem services that are less obvious. For example, many species of shellfish naturally filter and clean seawater (zu Ermgassen et al. 2013), and seagrasses stabilize terrain and offer protection against storms (Guannel et al. 2016). During Hurricane Sandy in the northeast U.S., wetlands prevented an estimated $625 million worth of flooding damage in New Jersey alone (Narayan et al. 2017).

While marine ecosystems offer robust benefits to humans, human impacts and environmental stressors can swiftly disrupt the complex web of life within ecosystems. One stressor of increasing concern amidst a changing climate is disease outbreak (Burge et al. 2014).

Disease outbreaks often occur as a result of a shift in dynamics between a host, a pathogen, and the environment, resulting in a “perfect storm.” For example, a pathogen may become more abundant due to rising temperatures, making a host become more susceptible to disease from increased exposure to the pathogen and/or increased temperature stress. The interconnectedness of these elements is understood in many terrestrial systems (Anderson et al. 2004), but studies regarding disease outbreak dynamics in the ocean are only now gaining momentum. In general, there is less research in marine systems than in land-based systems, and dynamic physical and biological processes in the ocean can make studying disease ecology challenging.

DiseaseVennDiagram (1)

Hosts and pathogens interact with their environment to cause disease outbreaks, as illustrated in this venn diagram. Image: Melissa Hoffman.

 

HOT RESEARCH QUESTIONS

(Adapted from Burge et al. 2014)

1. How do the environment, host, and pathogen evolve together? Who are the winners and losers in the face of climate change?
2. How can we better identify causative agents of diseases and how they are transmitted?
3. How can diagnostics be improved and included in adaptive management plans?
4. How can scientists model/predict future disease outbreaks to better prepare for them?

 

HOW CLIMATE CHANGE DETERMINES WINNERS AND LOSERS AMONG OCEAN ORGANISMS

In recent decades, there has been emerging concern for increased disease outbreak associated with climate change (Harvell et al. 2002; Altizer et al. 2013). There is no doubt that climate change is affecting our oceans, and researchers are beginning to gain a better understanding of how the many stressors tied to climate change are influencing host-pathogen interactions (Burge et al. 2014).

 

Rising Ocean Temperature
Rising levels of greenhouse gases in the atmosphere are causing increased global atmospheric and ocean temperatures. Increased temperatures have a number of impacts on oceanic systems, such as rising sea level, loss of sea ice, and altered ocean circulation. Warmer temperatures can negatively affect organisms’ physiology, affecting vital life functions such as growth, reproduction, and immune response. Prolonged periods of warm temperatures can lead to mass mortalities in certain organisms and have been linked to disease outbreak (Harvell et al. 2002).

Ocean Acidification
Increased emissions of carbon dioxide due to human activity are causing the oceans to become more acidic. Ocean acidity is expected to increase 150% by the end of the century relative to the pre- industrial era (Feely et al. 2009), creating conditions unparalleled in the past 300 million years. Ocean acidification changes the chemical composition of seawater and can make life difficult for many organisms with calcium carbonate in their bodies or shells (Kroeker et al. 2013). If ocean acidification disrupts an organism’s ability to produce calcium carbonate, their survival may be at stake.

Rainfall and Storms
Stronger and more frequent extreme weather events are linked to human-caused climate change. Increased duration and frequency of rainfall leads to more stormwater runoff, subjecting marine organisms to higher concentrations of pollutants and nutrients (Shapiro et al. 2010; Haapkylä et al. 2011). Stronger storms, like hurricanes, can cause physical harm to organisms and disturb entire ecosystems. These combined effects can increase stress in host organisms and create opportunities for pathogenic agents to invade new locations.

So What? Climate change can affect marine hosts and pathogens in complex, sometimes unpredictable, ways. These stressors have the potential to significantly alter interactions between hosts and pathogens, sometimes favoring disease outbreak in an ecosystem.

Burge Fig 1

Image: Burge et al., 2014. Reproduced with permission of Annual Review of Marine Science, Volume 6 by Annual Reviews, http://www.annualreviews.org

 

MARINE DISEASES AND CLIMATE CHANGE: CASE STUDIES

Below are examples of diseases in marine ecosystems that have caused significant impacts on the surrounding ecosystem, socio-economic conditions, or human health. While the exact etiology of some of these disease outbreaks may be difficult to tease out, climate-related stressors are likely involved. This is by no means an exhaustive list, and more examples of how disease outbreak ecology can impact ecosystems can be found here (Lafferty and Harvell 2014).

 

Caribbean Coral Reefs

Molasses11.jpg

Acropora palmate with white pox disease in the Florida Keys, March 2008. Image: Jim Stuby. Public Domain license.

 

Coral reefs provide crucial habitat to many organisms, which makes reef damage an ecosystem-wide problem. Coral reef ecosystems in Caribbean waters are facing some of the most widespread and intense deterioration in the world. Significant warming of the Caribbean basin in the past few decades has caused coral bleaching and rapid emergence of new virulent pathogens. One disease of concern is “white patch” or “white pox” disease, which is characterized by white patches on the corals’ skeleton, indicating that the zooxanthellae have been expelled or killed. Outbreaks have been linked to human fecal bacteria, Serrata marcescans, and sewage from the Florida Keys. Read more about coral diseases.

 

 

 

 

Epizootic Shell Disease in American Lobsters

LobstershelldiseaseAmerican lobster is one of the most valuable fisheries in the U.S., with an annual value of over $600 million (National Marine Fisheries Service). In recent decades, southern New England lobster populations have fallen victim to Epizootic Shell Disease, an infection characterized by unsightly lesions on the lobster’s shell that can significantly reduce its market value. While the etiology of the disease is not known, it is hypothesized that a suite of environmental stressors, pollutants, and bacteria are likely involved. There is also a major concern that the disease will become more prevalent in Maine, where the most robust and valuable stock currently resides. Read more about Epizootic Shell Disease.

 

 

Ichthyophonus Disease in Chinook Salmon

Image: Teruhiko Awakura

The mobility and migrations of fish make it uniquely difficult to study their diseases. One disease of significant economic and ecological concern is ichthyophoniasis, which occurs in both freshwater and marine species of fish. The disease is caused by a protistan parasite, presenting as nodules in internal organs or, in severe cases lesions on external tissue. On the Yukon River in Alaska, as many as 40% of Chinook salmon are estimated to be infected at certain times of year, threatening the livelihood of subsistence fishers. While the relationship of this infection and climate change is not  completely clear, there is likely a strong linkage between  chthyophoniasis and warming water temperatures (Kocan et al. 2009). Read more about ichthyophonus in salmon.

 

Vibriosis in Humans

Vibro vulnificus under the microscope

Image: Safeoysters.org

Noncholera Vibrio infections are especially concerning due to the direct threat to human health. Vibrio bacteria are common in the ocean, and more often than not, non-pathogenic to humans. However, humans can be affected by two species of Vibrio (Vibrio vulnificus and Vibrio parahaemolyticus), either by eating contaminated undercooked seafood, or through swimming in the ocean with open wounds. Most cases reported in the U.S. resulted from eating raw oysters. For those infected specifically with Vibrio vulficicus, vibriosis can be extremely serious, and about 1 in 4 patients die from this infection. Vibrio outbreaks are very closely coupled with climate change, as these bacteria thrive in warmer temperatures (Baker-Austin et al. 2010). Additionally, storms and extreme climatic events can introduce Vibrio species to new geographic areas through storm surges. Read more about vibriosis.

 

Diseases in Farmed Aquatic Animals

Disease in aquaculture facilities presents a significant problem for farmers and results in huge economic losses. Disease can ravage a farm and kill entire stocks in as little as 24 hours. As mentioned in the vibriosis section, some commonly farmed shellfish, such as oysters, can also pose a concern for human health. Most disease outbreaks in aquaculture settings occur when pathogens are introduced from the wild–through water intake, feed, or other infected organisms (Lafferty et al. 2015). See more examples of aquaculture diseases in the U.S. and the U.K.

 

MONITORING AND DIAGNOSING MARINE DISEASES

Detection is one of the most important factors in controlling disease in the marine environment, and it can also be one of the most challenging factors. Detection includes surveillance of organisms and habitats over time and the use of diagnostic tools to identify the disease. Surveillance and diagnosis of disease outbreaks over time is important for understanding patterns in the ecosystem and determining what is “normal.” Monitoring disease outbreaks can vary in difficulty depending on the ecosystem or organism being examined. Corals, for example, are sedentary and signs of disease are usually obvious, making detection and diagnosis relatively easy. Diagnosing disease in migratory fish, on the other hand, can be very challenging. The infographic below outlines different systems of organization considered for monitoring and diagnosing disease in marine organisms. It is important to note that many diseases require a combination of approaches to effectively diagnose and characterize an outbreak.

DiseaseProcesses_Infograph

 

HOW DO WE KNOW IF AN OUTBREAK IS AN EMERGENCY?

It is important to note that not all disease outbreaks are emergencies. Diseases occur naturally and can sometimes be beneficial to an ecosystem, so how do we know when a disease outbreak is or will be especially troublesome? While evaluating marine diseases is an evolving practice, scientists can characterize a disease outbreak as an emergency by  examining three important indicators (Groner et al. 2016):

Ecological Impact → Is there a significant disruption in the way the ecosystem normally functions? Does the disease outbreak result in the loss of a keystone species? Are important ecosystem services degraded?

Economic Impact → Is there significant economic loss for marine-based industries as a result of disease? Is there economic loss associated with reduced tourism following disease outbreaks?

Social Impact → Does the disease outbreak disrupt public safety, threaten human health, or diminish resilience of local communities?

If any one or combination of these impacts is present and severe enough to warrant a response, natural resource managers need to form management plans for addressing disease outbreaks.

 

ADAPTIVE DISEASE MANAGEMENT

stakeholdersIdeally, disease outbreaks should be prevented by early detection rather than mitigated after the fact. However, this can be a difficult feat due to the absence of baseline data on what is “normal” for an ecosystem, relevant diagnostic tools, or funding for research and surveillance programs. Nevertheless, interdisciplinary teams of scientists, managers, and various stakeholders have been working to formulate adaptive management plans for disease outbreaks.

Two key components of managing marine diseases involve surveillance of the “at-risk” ecosystem or species, and responsive tasks when disease is detected (Groner et al. 2016). Even when there is no disease emergency, researchers and managers must work to close knowledge gaps through ongoing research and communicate with stakeholders to develop management strategies. Below is a theoretical framework for responding to marine disease outbreak emergencies.

MitigationChart

 

PLANNING FOR THE FUTURE

While research has come a long way for diseases in the marine environment in recent decades, many knowledge gaps still remain. The complexity of marine ecosystems and unpredictable etiology of diseases make them uniquely difficult to study. In order to effectively manage these diseases and minimize ecological, economic, and social losses, researchers need to have a foundational understanding of the host and pathogen biology as well as environmental stressors. Amidst climate change, these dynamics are constantly shifting and evolving. While not all species are at risk for disease, more and more organisms are showing vulnerabilities.

One promising approach for mitigating marine disease is the use of mathematical models that aim to forecast disease outbreaks. In 2012, Wang and colleagues demonstrated how modeling ocean circulation and temperature patterns in Delaware Bay can help predict lethal MSX (the common name for infection by the pathogen Haplosporidium nelsoni) outbreaks in oysters (Wang et al. 2012). Using models in tandem with adaptive management plans can help stakeholders prepare for emergencies and have the potential to slow or stop outbreaks before they start (Lafferty and Hofmann 2016). That being said, accurate models can only be developed with sufficient baseline data and understanding of the host and pathogen ecology. These are areas of research that need further exploration in many systems.

Moving forward, researchers will need to pay particular attention to specific climatic and other environmental stressors that trigger disease and identify ways to reduce them. Incorporating disease mitigation strategies into existing management practices will be key (Burge et al. 2014), and there have already been some examples where this approach is successful (Miller et al. 2014). While frameworks for management exist, there are few successful examples in practice, so open communication between stakeholders will be necessary for sharing best practices. Enhancing the understanding of diseases in the marine environment will be vital for sustaining our valuable oceanic resources.

 

This backgrounder was written by Melissa Hoffman, a master’s student in the University of Rhode Island Biological and Environmental Systems program, as part of a Metcalf Institute graduate student internship for SciWrite@URI. She can be contacted at melissahoffman@uri.edu.

For More Information:

Sources:

Colleen Burge – University of Maryland, Baltimore
Disease ecology and climate change; improving communication about ocean health
and diseases for public audiences. Specific topics: seagrass wasting disease, coral health, mass mortalities in Pacific oyster caused by the Ostreid herpesvirus 1

Marta Gomez-Chiarri – University of Rhode Island
Pathology of host species, specifically including diseases in aquacultured organisms
and mitigation tools. Specific topics: use of probiotics to mitigate disease outbreaks, mechanisms of disease resistance in oysters

Maya Groner – Virginia Insitute of Marine Science
Ecology and evolution of aquatic diseases. Specific topics: wasting disease in seagrass beds, epizootic shell disease in lobsters

Drew Harvell – Cornell University
Disease ecology of many different ecosystems, climate change impacts on disease,
management strategies. Primary investigator for Ecology of Infectious Marine Diseases Research Coordination Network. Specific topics: disease ecology and climate change, coral reef and seagrass health

Paul Hershberger – U.S Geological Survey, Western Fisheries Research Center, Washington
Forecasting and mitigating the impacts of infectious and parasitic diseases on
populations of wild marine and anadromous fishes. Specific topics: Ichthyophonus infections in fish in Washington

Eileen Hofmann – Old Dominion University
Mathematical modeling for forecasting disease outbreaks to help management. Primary investigator for Ecology of Infectious Marine Diseases Research Coordination
Network. Specific topics: physical-biological models, climate controls on diseases of shellfish

Pieter Johnson – University of Colorado, Boulder
Disease emergence coupled with species invasions. Specific topics: interactions between loss of biodiversity and disease, role of pathogens in food webs

Gorka Bidegain – University of Southern Mississippi
Modeling ecology of marine diseases and transmission of waterborne pathogens. Specific topics: modelling disease in oysters, transmission of pathogens via filter feeding

Susan Kutz – University of Calgary
The role of climate change and animal health; conservation of subsistence resources;
disease ecology. Specific topics: community-based disease surveillance projects, parasitology

Kevin Lafferty, University of California – Santa Barbara, U.S Geological Survey
Ecology of marine infectious disease and how ecosystem dynamics impact disease. A principle investigator for Parasite Ecology Group at USCB. Specific topics: management strategies for disease, using parasites as ecosystem health indicators

Bette Willis – James Cook University, Australia
Environmental and human-caused drivers of disease outbreak in corals. Specific topics: ecology of disease in coral reef ecosystems, impact of climate change on hosts and pathogens, mitigating disease impacts

 

Additional Resources:

National Ocean Economics Program

Philosophical Transactions of the Royal Society B: Special Issue about marine disease

Altizer S, Ostfeld RS, Johnson PTJ, et al (2013) Climate Change and Infectious Diseases: From Evidence to a Predictive Framework. Science (80- ) 341:514–519. doi: 10.1126/science.1239401

Anderson PK, Cunningham AA, Patel NG, et al (2004) Emerging infectious diseases of plants : pathogen pollution , climate change and agrotechnology drivers. doi: 10.1016/j.tree.2004.07.021

Burge CA, Friedman CS, Getchell R, et al (2016) Complementary approaches to diagnosing marine diseases: a union of the modern and the classic. Philos Trans R Soc Lond B Biol Sci 371:1–11. doi: 10.1098/rstb.2015.0207

Burge CA, Mark Eakin C, Friedman CS, et al (2014) Climate Change Influences on Marine Infectious Diseases: Implications for Management and Society. Ann Rev Mar Sci 6:249–277. doi: 10.1146/annurev-marine- 010213-135029

Feely RA, Doney SC, Cooley SR (2009) Ocean Acidification. Oceanography 22:36–47.

Groner ML, Maynard J, Breyta R, et al (2016) Managing marine disease emergencies in an era of rapid change. Philos Trans R Soc Lond B Biol Sci. doi: http://dx.doi.org/10.1098/rstb.2015.0364

Guannel G, Arkema K, Ruggiero P, Verutes G (2016) The Power of Three : Coral Reefs , Seagrasses and Mangroves Protect Coastal Regions and Increase Their Resilience. PLoS One, 1–22. doi: 10.1371/journal.pone.0158094

Haapkylä J, Unsworth RKF, Flavell M, et al (2011) Seasonal rainfall and runoff promote coral disease on an inshore reef. PLoS One 6:1–10. doi: 10.1371/journal.pone.0016893

Harvell CD, Mitchell CE, Ward JR, et al (2002) Climate Warming and Disease Risks for Terrestrial and Marine Biota. Science 296(5576):2158–2163.

Kocan R, Hershberger P, Sanders G, Winton J (2009) Effects of temperature on disease progression and swimming stamina in Ichthyophonus-infected rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 32:835–843. doi: 10.1111/j.1365-2761.2009.01059.x

Kroeker KJ, Kordas RL, Crim R, et al (2013) Impacts of ocean acidification on marine organisms: Quantifying sensitivities and interaction with warming. Glob Chang Biol 19:1884–1896. doi: 10.1111/gcb.12179

Lafferty KD, Harvell CD (2014) The role of infectious diseases in marine communities. In: Marine Community Ecology and Conservation. p Ch. 5, 85-108

Lafferty KD, Harvell CD, Conrad JM, et al (2015) Infectious diseases affect marine fisheries and aquaculture economics. Ann Rev Mar Sci 7:471–496. doi: 10.1146/annurev-marine- 010814- 015646

Lafferty KD, Hofmann EE (2016) Marine disease impacts, diagnosis, forecasting, management and policy. Philos Trans R Soc B Biol Sci 371:20150200. doi: 10.1098/rstb.2015.0200

Miller MW, Lohr KE, Cameron CM, et al (2014) Disease dynamics and potential mitigation among restored and wild staghorn coral, Acropora cervicornis. PeerJ 2:e541. doi: 10.7717/peerj.541

Narayan S, Beck MW, Wilson P, et al (2017) The Value of Coastal Wetlands for Flood Damage Reduction in the Northeastern USA. Sci Rep 7:9463. doi: 10.1038/s41598-017- 09269-z

Shapiro K, Conrad PA, Mazet JAK, et al (2010) Effect of estuarine wetland degradation on transport of toxoplasma gondii surrogates from land to sea. Appl Environ Microbiol 76:6821–6828. doi: 10.1128/AEM.01435-10

Wang Z, Haidvogel DB, Bushek D, et al (2012) Circulation and water properties and their relationship to the oyster disease MSX in Delaware Bay. J Mar Res 70:279–308. doi: 10.1357/002224012802851931

zu Ermgassen PS, Spalding MD, Grizzle RE, Brumbaugh RD (2013) Quantifying the Loss of a Marine Ecosystem Service : Filtration by the Eastern Oyster in US Estuaries. Estuaries and Coasts 36:36–43. doi: 10.1007/s12237-012- 9559-y

 

 

 

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