Resilience of Coral-Associated Bacterial Communities Exposed to Fish Farm Effluent

10.1371/journal.pone.0007319PLoS ONE410

Cellular Responses in Sea Fan Corals: Granular Amoebocytes React to Pathogen and Climate Stressors

BACKGROUND: Climate warming is causing environmental change making both marine and terrestrial organisms, and even humans, more susceptible to emerging diseases. Coral reefs are among the most impacted ecosystems by climate stress, and immunity of corals, the most ancient of metazoans, is poorly known. Although coral mortality due to infectious diseases and temperature-related stress is on the rise, the immune effector mechanisms that contribute to the resistance of corals to such events remain elusive. In the Caribbean sea fan corals (Anthozoa, Alcyonacea: Gorgoniidae), the cell-based immune defenses are granular acidophilic amoebocytes, which are known to be involved in wound repair and histocompatibility. METHODOLOGY/PRINCIPAL FINDINGS: We demonstrate for the first time in corals that these cells are involved in the organismal response to pathogenic and temperature stress. In sea fans with both naturally occurring infections and experimental inoculations with the fungal pathogen Aspergillus sydowii, an inflammatory response, characterized by a massive increase of amoebocytes, was evident near infections. Melanosomes were detected in amoebocytes adjacent to protective melanin bands in infected sea fans; neither was present in uninfected fans. In naturally infected sea fans a concurrent increase in prophenoloxidase activity was detected in infected tissues with dense amoebocytes. Sea fans sampled in the field during the 2005 Caribbean Bleaching Event (a once-in-hundred-year climate event) responded to heat stress with a systemic increase in amoebocytes and amoebocyte densities were also increased by elevated temperature stress in lab experiments. CONCLUSIONS/SIGNIFICANCE: The observed amoebocyte responses indicate that sea fan corals use cellular defenses to combat fungal infection and temperature stress. The ability to mount an inflammatory response may be a contributing factor that allowed the survival of even infected sea fan corals during a stressful climate event

Impacts of aspergillosis on sea fan coral demography: modeling a moving target

Little is known about how epizootics in natural populations affect vital rates and population structure, or about the process of recovery after an outbreak subsides. We investigated the effects of aspergillosis, an infectious disease caused by the fungal pathogen Aspergillus sydowii, on the demography of a gorgonian coral, Gorgonia ventalina. Caribbean sea fans were affected by a seven-year epizootic, marked by an initial period in 1994 of high infection prevalence, high mortality rates, and almost complete reproductive failure of infected fans. Post epizootic, in 2005, host populations were relatively healthy, with low disease prevalence. Using longitudinal data from populations on coral reefs in the Florida Keys (USA) and the Yucatán Peninsula (Mexico), we documented changes in the epidemiology of sea fan aspergillosis over the course of the epizootic. We developed an "integral projection model" that scales disease impacts from individual to population levels using direct estimates of vital rates. Within-colony lesion growth rate and host mortality were higher during the peak of the epizootic. Effects on individuals and populations changed substantially post-epizootic; recruitment increased, mortality of infected adults decreased, and the size dependence of infection was reduced. Elasticity analysis indicated that population growth is more sensitive to changes in the growth and survival of established colonies than to recruitment, due to slow colony growth and the longevity and fecundity of large adults. Disease prevalence in our monitored populations decreased from ∼50% in 1997 to <10% by 2003 and <1% in 2007 and was accompanied by very high mortality during the early stages of the epizootic. The population model suggested that host evolution (due to selection for higher disease resistance through differential mortality) could proceed quickly enough to explain the observed changes in prevalence and in the size independence of infection risk. Our model indicates that the time required for population recovery following an outbreak is largely determined by the percentage of healthy tissue lost from the population. However, recovery following an especially severe outbreak (i.e., 80% or more tissue loss) is much faster if the affected population receives an external supply of recruits from unaffected areas

Growth anomalies on the coral genera Acropora and Porites are strongly associated with host density and human population size across the Indo-Pacific

Growth anomalies (GAs) are common, tumor-like diseases that can cause significant morbidity and decreased fecundity in the major Indo-Pacific reef-building coral genera, Acropora and Porites. GAs are unusually tractable for testing hypotheses about drivers of coral disease because of their pan-Pacific distributions, relatively high occurrence, and unambiguous ease of identification. We modeled multiple disease-environment associations that may underlie the prevalence of Acropora growth anomalies (AGA) (n = 304 surveys) and Porites growth anomalies (PGA) (n = 602 surveys) from across the Indo-Pacific. Nine predictor variables were modeled, including coral host abundance, human population size, and sea surface temperature and ultra-violet radiation anomalies. Prevalence of both AGAs and PGAs were strongly host density-dependent. PGAs additionally showed strong positive associations with human population size. Although this association has been widely posited, this is one of the first broad-scale studies unambiguously linking a coral disease with human population size. These results emphasize that individual coral diseases can show relatively distinct patterns of association with environmental predictors, even in similar diseases (growth anomalies) found on different host genera (Acropora vs. Porites). As human densities and environmental degradation increase globally, the prevalence of coral diseases like PGAs could increase accordingly, halted only perhaps by declines in host density below thresholds required for disease establishment

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

International audienceTo 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 128C. Our seasonal outlook for 2015 and long-term projections show bottom temperatures greater than or equal to 128C 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

Deciphering coral disease dynamics: integrating host, microbiome, and the changing environment

Diseases of tropical reef organisms is an intensive area of study, but despite significant advances in methodology and the global knowledge base, identifying the proximate causes of disease outbreaks remains difficult. The dynamics of infectious wildlife diseases are known to be influenced by shifting interactions among the host, pathogen, and other members of the microbiome, and a collective body of work clearly demonstrates that this is also the case for the main foundation species on reefs, corals. Yet, among wildlife, outbreaks of coral diseases stand out as being driven largely by a changing environment. These outbreaks contributed not only to significant losses of coral species but also to whole ecosystem regime shifts. Here we suggest that to better decipher the disease dynamics of corals, we must integrate more holistic and modern paradigms that consider multiple and variable interactions among the three major players in epizootics: the host, its associated microbiome, and the environment. In this perspective, we discuss how expanding the pathogen component of the classic host-pathogen-environment disease triad to incorporate shifts in the microbiome leading to dysbiosis provides a better model for understanding coral disease dynamics. We outline and discuss issues arising when evaluating each component of this trio and make suggestions for bridging gaps between them. We further suggest that to best tackle these challenges, researchers must adjust standard paradigms, like the classic one pathogen-one disease model, that, to date, have been ineffectual at uncovering many of the emergent properties of coral reef disease dynamics. Lastly, we make recommendations for ways forward in the fields of marine disease ecology and the future of coral reef conservation and restoration given these observations

Managing marine disease emergencies in an era of rapid change

Infectious marine diseases can decimate populations and are increasing among some taxa due to global change and our increasing reliance on marine environments. Marine diseases become emergencies when significant ecological, economic or social impacts occur. We can prepare for and manage these emergencies through improved surveillance, and the development and iterative refinement of approaches to mitigate disease and its impacts. Improving surveillance requires fast, accurate diagnoses, forecasting disease risk and real-time monitoring of disease-promoting environmental conditions. Diversifying impact mitigation involves increasing host resilience to disease, reducing pathogen abundance and managing environmental factors that facilitate disease. Disease surveillance and mitigation can be adaptive if informed by research advances and catalysed by communication among observers, researchers and decision-makers using information-sharing platforms. Recent increases in the awareness of the threats posed by marine diseases may lead to policy frameworks that facilitate the responses and management that marine disease emergencies require

Thermal Stress and Coral Cover as Drivers of Coral Disease Outbreaks

Very little is known about how environmental changes such as increasing temperature affect disease dynamics in the ocean, especially at large spatial scales. We asked whether the frequency of warm temperature anomalies is positively related to the frequency of coral disease across 1,500 km of Australia's Great Barrier Reef. We used a new high-resolution satellite dataset of ocean temperature and 6 y of coral disease and coral cover data from annual surveys of 48 reefs to answer this question. We found a highly significant relationship between the frequencies of warm temperature anomalies and of white syndrome, an emergent disease, or potentially, a group of diseases, of Pacific reef-building corals. The effect of temperature was highly dependent on coral cover because white syndrome outbreaks followed warm years, but only on high (>50%) cover reefs, suggesting an important role of host density as a threshold for outbreaks. Our results indicate that the frequency of temperature anomalies, which is predicted to increase in most tropical oceans, can increase the susceptibility of corals to disease, leading to outbreaks where corals are abundant

Low-Altitude UAV Imaging Accurately Quantifies Eelgrass Wasting Disease From Alaska to California

Declines in eelgrass, an important and widespread coastal habitat, are associated with wasting disease in recent outbreaks on the Pacific coast of North America. This study presents a novel method for mapping and predicting wasting disease using Unoccupied Aerial Vehicle (UAV) with low-altitude autonomous imaging of visible bands. We conducted UAV mapping and sampling in intertidal eelgrass beds across multiple sites in Alaska, British Columbia, and California. We designed and implemented a UAV low-altitude mapping protocol to detect disease prevalence and validated against in situ results. Our analysis revealed that green leaf area index derived from UAV imagery was a strong and significant (inverse) predictor of spatial distribution and severity of wasting disease measured on the ground, especially for regions with extensive disease infection. This study highlights a novel, efficient, and portable method to investigate seagrass disease at landscape scales across geographic regions and conditions