Seagrass meadows provide valuable ecosystem benefits but are at risk from disease. Eelgrass (Zost... more Seagrass meadows provide valuable ecosystem benefits but are at risk from disease. Eelgrass (Zostera marina) is a temperate species threatened by seagrass wasting disease (SWD), caused by the protist Labyrinthula zosterae. The pathogen is sensitive to warming ocean temperatures, prompting a need for greater understanding of the impacts on host health under climate change. Previous work demonstrates pathogen cultures grow faster under warmer laboratory conditions and documents positive correlations between warmer ocean temperatures and disease levels in nature. However, the consequences of disease outbreaks on eelgrass growth remain poorly understood. Here, we examined the effect of disease on eelgrass productivity in the field. We coupled in situ shoot marking with high-resolution imagery of eelgrass blades and used an artificial intelligence application to determine disease prevalence and severity from digital images. Comparisons of eelgrass growth and disease metrics showed that S...
Co-infection is the reality in natural populations, but few studies incorporate the players that ... more Co-infection is the reality in natural populations, but few studies incorporate the players that matter in the wild. We integrate the environment, host demography, two parasites, and host immunity in a study of co-infection to determine the drivers of parasite interactions. Here, we use an ecologically important Caribbean sea fan octocoral, Gorgonia ventalina, that is co-infected by a copepod and a labyrinthulid protist. We first expanded upon laboratory studies by showing that immune suppression is associated with the labyrinthulid in a natural setting. Histological analyses revealed that immune cells (amoebocytes) were significantly suppressed in both labyrinthulid infections and co-infections relative to healthy sea fans, but remained unchanged in copepod infections. However, surveys of natural coral populations demonstrated a critical role for the environment and host demography in this co-infection: the prevalence of copepod infections increased with sea fan size while labyrint...
Philosophical Transactions of the Royal Society B: Biological Sciences, 2016
Over 20 species of asteroids were devastated by a sea star wasting disease (SSWD) epizootic, link... more Over 20 species of asteroids were devastated by a sea star wasting disease (SSWD) epizootic, linked to a densovirus, from Mexico to Alaska in 2013 and 2014. ForPisaster ochraceusfrom the San Juan Islands, South Puget Sound and Washington outer coast, time-series monitoring showed rapid disease spread, high mortality rates in 2014, and continuing levels of wasting in the survivors in 2015. Peak prevalence of disease at 16 sites ranged to 100%, with an overall mean of 61%. Analysis of longitudinal data showed disease risk was correlated with both size and temperature and resulted in shifts in population size structure; adult populations fell to one quarter of pre-outbreak abundances. In laboratory experiments, time between development of disease signs and death was influenced by temperature in adults but not juveniles and adult mortality was 18% higher in the 19°C treatment compared to the lower temperature treatments. While larger ochre stars developed disease signs sooner than juven...
Philosophical transactions of the Royal Society of London. Series B, Biological sciences, Jan 5, 2016
To forecast marine disease outbreaks as oceans warm requires new environmental surveillance tools... more 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...
Sewage pollution threatens the health of coastal populations and ecosystems, including coral reef... more Sewage pollution threatens the health of coastal populations and ecosystems, including coral reefs. We investigated spatial patterns of sewage pollution in Puako, Hawaii using enterococci concentrations and δ(15)N Ulva fasciata macroalgal bioassays to assess relationships with the coral disease Porites lobata growth anomalies (PGAs). PGA severity and enterococci concentrations were high, spatially variable, and positively related. Bioassay algal δ(15)N showed low sewage pollution at the reef edge while high values of resident algae indicated sewage pollution nearshore. Neither δ(15)N metric predicted PGA measures, though bioassay δ(15)N was negatively related to coral cover. Furthermore, PGA prevalence was much higher than previously recorded in Hawaii and the greater Indo-Pacific, highlighting Puako as an area of concern. Although further work is needed to resolve the relationship between sewage pollution and coral cover and disease, these results implicate sewage pollution as a co...
Climate change is negatively affecting the stability of natural ecosystems, especially coral reef... more Climate change is negatively affecting the stability of natural ecosystems, especially coral reefs. The dissociation of the symbiosis between reef-building corals and their algal symbiont, or coral bleaching, has been linked to increased sea surface temperatures. Coral bleaching has significant impacts on corals, including an increase in disease outbreaks that can permanently change the entire reef ecosystem. Yet, little is known about the impacts of coral bleaching on the coral immune system. In this study, whole transcriptome analysis of the coral holobiont and each of the associate components (i.e. coral host, algal symbiont and other associated microorganisms) was used to determine changes in gene expression in corals affected by a natural bleaching event as well as during the recovery phase. The main findings include evidence that the coral holobiont and the coral host have different responses to bleaching, and the host immune system appears suppressed even a year after a bleac...
The response of corals to warm temperature anomalies includes changes in coral bacterial assembla... more The response of corals to warm temperature anomalies includes changes in coral bacterial assemblages. There are clear differences between the microbiota of bleached and healthy corals. However, few studies have tracked the microbiota of individual colonies throughout a warming event. We used 454 pyrosequencing and repeated measures to characterize bacterial assemblages in 15 Gorgonia ventalina colonies before, during, four months after, and one year after the 2010 Caribbean warm thermal anomaly. In the latter three sampling times, the G. ventalina microbiota differed significantly from the microbiota of Orbicella faveolata colonies, which were sampled only at these three times. O. faveolata microbiota did not exhibit coordinated shifts through time. Notably, the microbiota of the repeatedly sampled G. ventalina colonies shifted persistently from before to during, after, and long after the warming event. The same pattern emerges from the norm of reaction for the individual G. ventalina colonies. This is the first study to show persistent shifts in coral microbiota in association with a warm thermal anomaly. Whether shifting microbiota is adaptive or maladaptive, the lasting change in bacterial assemblages following this warming event identifies a new way that coral microbiota shape the response of coral colonies under thermal stress.
Infectious diseases are common in marine environments, but the effects of a changing climate on m... more Infectious diseases are common in marine environments, but the effects of a changing climate on marine pathogens are not well understood. Here we review current knowledge about how the climate drives host-pathogen interactions and infectious disease outbreaks. Climate-related impacts on marine diseases are being documented in corals, shellfish, finfish, and humans; these impacts are less clearly linked for other organisms. Oceans and people are inextricably linked, and marine diseases can both directly and indirectly affect human health, livelihoods, and well-being. We recommend an adaptive management approach to better increase the resilience of ocean systems vulnerable to marine diseases in a changing climate. Land-based management methods of quarantining, culling, and vaccinating are not successful in the ocean; therefore, forecasting conditions that lead to outbreaks and designing tools/approaches to influence these conditions may be the best way to manage marine disease.
Seafood is a growing part of the economy, but its economic value is diminished by marine diseases... more Seafood is a growing part of the economy, but its economic value is diminished by marine diseases. Infectious diseases are common in the ocean, and here we tabulate 67 examples that can reduce commercial species' growth and survivorship or decrease seafood quality. These impacts seem most problematic in the stressful and crowded conditions of aquaculture, which increasingly dominates seafood production as wild fishery production plateaus. For instance, marine diseases of farmed oysters, shrimp, abalone, and various fishes, particularly Atlantic salmon, cost billions of dollars each year. In comparison, it is often difficult to accurately estimate disease impacts on wild populations, especially those of pelagic and subtidal species. Farmed species often receive infectious diseases from wild species and can, in turn, export infectious agents to wild species. However, the impact of disease export on wild fisheries is controversial because there are few quantitative data demonstrati...
Proceedings of the National Academy of Sciences, 2014
Significance Sea stars inhabiting the Northeast Pacific Coast have recently experienced an extens... more Significance Sea stars inhabiting the Northeast Pacific Coast have recently experienced an extensive outbreak of wasting disease, leading to their degradation and disappearance from many coastal areas. In this paper, we present evidence that the cause of the disease is transmissible from disease-affected animals to apparently healthy individuals, that the disease-causing agent is a virus-sized microorganism, and that the best candidate viral taxon, the sea star-associated densovirus (SSaDV), is in greater abundance in diseased than in healthy sea stars.
Scientists have long predicted large-scale responses of infectious diseases to climate change, gi... more Scientists have long predicted large-scale responses of infectious diseases to climate change, giving rise to a polarizing debate, especially concerning human pathogens for which socioeconomic drivers and control measures can limit the detection of climate-mediated changes. Climate change has already increased the occurrence of diseases in some natural and agricultural systems, but in many cases, outcomes depend on the form of climate change and details of the host-pathogen system. In this review, we highlight research progress and gaps that have emerged during the past decade and develop a predictive framework that integrates knowledge from ecophysiology and community ecology with modeling approaches. Future work must continue to anticipate and monitor pathogen biodiversity and disease trends in natural ecosystems and identify opportunities to mitigate the impacts of climate-driven disease emergence.
Atmospheric carbon dioxide concentration is expected to exceed 500 parts per million and global t... more Atmospheric carbon dioxide concentration is expected to exceed 500 parts per million and global temperatures to rise by at least 2°C by 2050 to 2100, values that significantly exceed those of at least the past 420,000 years during which most extant marine organisms evolved. Under conditions expected in the 21st century, global warming and ocean acidification will compromise carbonate accretion, with corals becoming increasingly rare on reef systems. The result will be less diverse reef communities and carbonate reef structures that fail to be maintained. Climate change also exacerbates local stresses from declining water quality and overexploitation of key species, driving reefs increasingly toward the tipping point for functional collapse. This review presents future scenarios for coral reefs that predict increasingly serious consequences for reef-associated fisheries, tourism, coastal protection, and people. As the International Year of the Reef 2008 begins, scaled-up management i...
Seagrass meadows provide valuable ecosystem benefits but are at risk from disease. Eelgrass (Zost... more Seagrass meadows provide valuable ecosystem benefits but are at risk from disease. Eelgrass (Zostera marina) is a temperate species threatened by seagrass wasting disease (SWD), caused by the protist Labyrinthula zosterae. The pathogen is sensitive to warming ocean temperatures, prompting a need for greater understanding of the impacts on host health under climate change. Previous work demonstrates pathogen cultures grow faster under warmer laboratory conditions and documents positive correlations between warmer ocean temperatures and disease levels in nature. However, the consequences of disease outbreaks on eelgrass growth remain poorly understood. Here, we examined the effect of disease on eelgrass productivity in the field. We coupled in situ shoot marking with high-resolution imagery of eelgrass blades and used an artificial intelligence application to determine disease prevalence and severity from digital images. Comparisons of eelgrass growth and disease metrics showed that S...
Co-infection is the reality in natural populations, but few studies incorporate the players that ... more Co-infection is the reality in natural populations, but few studies incorporate the players that matter in the wild. We integrate the environment, host demography, two parasites, and host immunity in a study of co-infection to determine the drivers of parasite interactions. Here, we use an ecologically important Caribbean sea fan octocoral, Gorgonia ventalina, that is co-infected by a copepod and a labyrinthulid protist. We first expanded upon laboratory studies by showing that immune suppression is associated with the labyrinthulid in a natural setting. Histological analyses revealed that immune cells (amoebocytes) were significantly suppressed in both labyrinthulid infections and co-infections relative to healthy sea fans, but remained unchanged in copepod infections. However, surveys of natural coral populations demonstrated a critical role for the environment and host demography in this co-infection: the prevalence of copepod infections increased with sea fan size while labyrint...
Philosophical Transactions of the Royal Society B: Biological Sciences, 2016
Over 20 species of asteroids were devastated by a sea star wasting disease (SSWD) epizootic, link... more Over 20 species of asteroids were devastated by a sea star wasting disease (SSWD) epizootic, linked to a densovirus, from Mexico to Alaska in 2013 and 2014. ForPisaster ochraceusfrom the San Juan Islands, South Puget Sound and Washington outer coast, time-series monitoring showed rapid disease spread, high mortality rates in 2014, and continuing levels of wasting in the survivors in 2015. Peak prevalence of disease at 16 sites ranged to 100%, with an overall mean of 61%. Analysis of longitudinal data showed disease risk was correlated with both size and temperature and resulted in shifts in population size structure; adult populations fell to one quarter of pre-outbreak abundances. In laboratory experiments, time between development of disease signs and death was influenced by temperature in adults but not juveniles and adult mortality was 18% higher in the 19°C treatment compared to the lower temperature treatments. While larger ochre stars developed disease signs sooner than juven...
Philosophical transactions of the Royal Society of London. Series B, Biological sciences, Jan 5, 2016
To forecast marine disease outbreaks as oceans warm requires new environmental surveillance tools... more 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...
Sewage pollution threatens the health of coastal populations and ecosystems, including coral reef... more Sewage pollution threatens the health of coastal populations and ecosystems, including coral reefs. We investigated spatial patterns of sewage pollution in Puako, Hawaii using enterococci concentrations and δ(15)N Ulva fasciata macroalgal bioassays to assess relationships with the coral disease Porites lobata growth anomalies (PGAs). PGA severity and enterococci concentrations were high, spatially variable, and positively related. Bioassay algal δ(15)N showed low sewage pollution at the reef edge while high values of resident algae indicated sewage pollution nearshore. Neither δ(15)N metric predicted PGA measures, though bioassay δ(15)N was negatively related to coral cover. Furthermore, PGA prevalence was much higher than previously recorded in Hawaii and the greater Indo-Pacific, highlighting Puako as an area of concern. Although further work is needed to resolve the relationship between sewage pollution and coral cover and disease, these results implicate sewage pollution as a co...
Climate change is negatively affecting the stability of natural ecosystems, especially coral reef... more Climate change is negatively affecting the stability of natural ecosystems, especially coral reefs. The dissociation of the symbiosis between reef-building corals and their algal symbiont, or coral bleaching, has been linked to increased sea surface temperatures. Coral bleaching has significant impacts on corals, including an increase in disease outbreaks that can permanently change the entire reef ecosystem. Yet, little is known about the impacts of coral bleaching on the coral immune system. In this study, whole transcriptome analysis of the coral holobiont and each of the associate components (i.e. coral host, algal symbiont and other associated microorganisms) was used to determine changes in gene expression in corals affected by a natural bleaching event as well as during the recovery phase. The main findings include evidence that the coral holobiont and the coral host have different responses to bleaching, and the host immune system appears suppressed even a year after a bleac...
The response of corals to warm temperature anomalies includes changes in coral bacterial assembla... more The response of corals to warm temperature anomalies includes changes in coral bacterial assemblages. There are clear differences between the microbiota of bleached and healthy corals. However, few studies have tracked the microbiota of individual colonies throughout a warming event. We used 454 pyrosequencing and repeated measures to characterize bacterial assemblages in 15 Gorgonia ventalina colonies before, during, four months after, and one year after the 2010 Caribbean warm thermal anomaly. In the latter three sampling times, the G. ventalina microbiota differed significantly from the microbiota of Orbicella faveolata colonies, which were sampled only at these three times. O. faveolata microbiota did not exhibit coordinated shifts through time. Notably, the microbiota of the repeatedly sampled G. ventalina colonies shifted persistently from before to during, after, and long after the warming event. The same pattern emerges from the norm of reaction for the individual G. ventalina colonies. This is the first study to show persistent shifts in coral microbiota in association with a warm thermal anomaly. Whether shifting microbiota is adaptive or maladaptive, the lasting change in bacterial assemblages following this warming event identifies a new way that coral microbiota shape the response of coral colonies under thermal stress.
Infectious diseases are common in marine environments, but the effects of a changing climate on m... more Infectious diseases are common in marine environments, but the effects of a changing climate on marine pathogens are not well understood. Here we review current knowledge about how the climate drives host-pathogen interactions and infectious disease outbreaks. Climate-related impacts on marine diseases are being documented in corals, shellfish, finfish, and humans; these impacts are less clearly linked for other organisms. Oceans and people are inextricably linked, and marine diseases can both directly and indirectly affect human health, livelihoods, and well-being. We recommend an adaptive management approach to better increase the resilience of ocean systems vulnerable to marine diseases in a changing climate. Land-based management methods of quarantining, culling, and vaccinating are not successful in the ocean; therefore, forecasting conditions that lead to outbreaks and designing tools/approaches to influence these conditions may be the best way to manage marine disease.
Seafood is a growing part of the economy, but its economic value is diminished by marine diseases... more Seafood is a growing part of the economy, but its economic value is diminished by marine diseases. Infectious diseases are common in the ocean, and here we tabulate 67 examples that can reduce commercial species' growth and survivorship or decrease seafood quality. These impacts seem most problematic in the stressful and crowded conditions of aquaculture, which increasingly dominates seafood production as wild fishery production plateaus. For instance, marine diseases of farmed oysters, shrimp, abalone, and various fishes, particularly Atlantic salmon, cost billions of dollars each year. In comparison, it is often difficult to accurately estimate disease impacts on wild populations, especially those of pelagic and subtidal species. Farmed species often receive infectious diseases from wild species and can, in turn, export infectious agents to wild species. However, the impact of disease export on wild fisheries is controversial because there are few quantitative data demonstrati...
Proceedings of the National Academy of Sciences, 2014
Significance Sea stars inhabiting the Northeast Pacific Coast have recently experienced an extens... more Significance Sea stars inhabiting the Northeast Pacific Coast have recently experienced an extensive outbreak of wasting disease, leading to their degradation and disappearance from many coastal areas. In this paper, we present evidence that the cause of the disease is transmissible from disease-affected animals to apparently healthy individuals, that the disease-causing agent is a virus-sized microorganism, and that the best candidate viral taxon, the sea star-associated densovirus (SSaDV), is in greater abundance in diseased than in healthy sea stars.
Scientists have long predicted large-scale responses of infectious diseases to climate change, gi... more Scientists have long predicted large-scale responses of infectious diseases to climate change, giving rise to a polarizing debate, especially concerning human pathogens for which socioeconomic drivers and control measures can limit the detection of climate-mediated changes. Climate change has already increased the occurrence of diseases in some natural and agricultural systems, but in many cases, outcomes depend on the form of climate change and details of the host-pathogen system. In this review, we highlight research progress and gaps that have emerged during the past decade and develop a predictive framework that integrates knowledge from ecophysiology and community ecology with modeling approaches. Future work must continue to anticipate and monitor pathogen biodiversity and disease trends in natural ecosystems and identify opportunities to mitigate the impacts of climate-driven disease emergence.
Atmospheric carbon dioxide concentration is expected to exceed 500 parts per million and global t... more Atmospheric carbon dioxide concentration is expected to exceed 500 parts per million and global temperatures to rise by at least 2°C by 2050 to 2100, values that significantly exceed those of at least the past 420,000 years during which most extant marine organisms evolved. Under conditions expected in the 21st century, global warming and ocean acidification will compromise carbonate accretion, with corals becoming increasingly rare on reef systems. The result will be less diverse reef communities and carbonate reef structures that fail to be maintained. Climate change also exacerbates local stresses from declining water quality and overexploitation of key species, driving reefs increasingly toward the tipping point for functional collapse. This review presents future scenarios for coral reefs that predict increasingly serious consequences for reef-associated fisheries, tourism, coastal protection, and people. As the International Year of the Reef 2008 begins, scaled-up management i...
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