Taking the pulse of resilience in conserving seagrass meadows.

Foundational habitats such as seagrasses and coral reefs are at severe risk globally from climate warming. Infectious disease associated with warming events is both a cause of decline and an indicator of stress in both habitats. Since new approaches are needed to detect refugia and design climate-smart networks of marine protected areas, we test the hypothesis that the health of eelgrass (Zostera marina) in temperate ecosystems can serve as a proxy indicative of higher resilience and help pinpoint refugia. Eelgrass meadows worldwide are at-risk from environmental stressors, including climate warming and disease. Disease outbreaks of Labyrinthula zosterae are associated with recent, widespread declines in eelgrass meadows throughout the San Juan Islands, Washington, USA. Machine language learning, drone surveys, and molecular diagnostics reveal climate impacts on seagrass wasting disease prevalence (proportion of infected individuals) and severity (proportion infected leaf area) from San Diego, California to Alaska. Given that warmer temperatures favor many pathogens such as L. zosterae, we hypothesize that absent or low disease severity in meadows could indicate eelgrass resilience to climate and pathogenic stressors. Regional surveys showed the San Juan Islands as a hotspot for both high disease prevalence and severity, and surveys throughout the Northeast Pacific indicated higher prevalence and severity in intertidal, rather than subtidal, meadows. Further, among sites with eelgrass declines, losses were more pronounced at sites with shallower eelgrass meadows. We suggest deeper meadows with the lowest disease severity will be refuges from future warming and pathogenic stressors in the Northeast Pacific. Disease monitoring may be a useful conservation approach for marine foundation species, as low or absent disease severity can pinpoint resilient refugia that should be prioritized for future conservation efforts. Even in declining or at-risk habitats, disease surveys can help identify meadows that may contain especially resilient individuals for future restoration efforts. Our approach of using disease as a pulse-point for eelgrass resilience to multiple stressors could be applied to other habitats such as coral reefs to inform conservation and management decisions.

Predictable Changes in Eelgrass Microbiomes with Increasing Wasting Disease Prevalence across 23° Latitude in the Northeastern Pacific.

Predicting outcomes of marine disease outbreaks presents a challenge in the face of both global and local stressors. Host-associated microbiomes may play important roles in disease dynamics but remain understudied in marine ecosystems. Host-pathogen-microbiome interactions can vary across host ranges, gradients of disease, and temperature; studying these relationships may aid our ability to forecast disease dynamics. Eelgrass, Zostera marina, is impacted by outbreaks of wasting disease caused by the opportunistic pathogen Labyrinthula zosterae. We investigated how Z. marina phyllosphere microbial communities vary with rising wasting disease lesion prevalence and severity relative to plant and meadow characteristics like shoot density, longest leaf length, and temperature across 23° latitude in the Northeastern Pacific. We detected effects of geography (11%) and smaller, but distinct, effects of temperature (30-day max sea surface temperature, 4%) and disease (lesion prevalence, 3%) on microbiome composition. Declines in alpha diversity on asymptomatic tissue occurred with rising wasting disease prevalence within meadows. However, no change in microbiome variability (dispersion) was detected between asymptomatic and symptomatic tissues. Further, we identified members of Cellvibrionaceae, Colwelliaceae, and Granulosicoccaceae on asymptomatic tissue that are predictive of wasting disease prevalence across the geographic range (3,100 kilometers). Functional roles of Colwelliaceae and Granulosicoccaceae are not known. Cellvibrionaceae, degraders of plant cellulose, were also enriched in lesions and adjacent green tissue relative to nonlesioned leaves. Cellvibrionaceae may play important roles in disease progression by degrading host tissues or overwhelming plant immune responses. Thus, inclusion of microbiomes in wasting disease studies may improve our ability to understand variable rates of infection, disease progression, and plant survival. IMPORTANCE The roles of marine microbiomes in disease remain poorly understood due, in part, to the challenging nature of sampling at appropriate spatiotemporal scales and across natural gradients of disease throughout host ranges. This is especially true for marine vascular plants like eelgrass (Zostera marina) that are vital for ecosystem function and biodiversity but are susceptible to rapid decline and die-off from pathogens like eukaryotic slime-mold Labyrinthula zosterae (wasting disease). We link bacterial members of phyllosphere tissues to the prevalence of wasting disease across the broadest geographic range to date for a marine plant microbiome-disease study (3,100 km). We identify Cellvibrionaceae, plant cell wall degraders, enriched (up to 61% relative abundance) within lesion tissue, which suggests this group may be playing important roles in disease progression. These findings suggest inclusion of microbiomes in marine disease studies will improve our ability to predict ecological outcomes of infection across variable landscapes spanning thousands of kilometers.

Preparing Aquatic Research for an Extreme Future: Call for Improved Definitions and Responsive, Multidisciplinary Approaches.

Extreme events have increased in frequency globally, with a simultaneous surge in scientific interest about their ecological responses, particularly in sensitive freshwater, coastal, and marine ecosystems. We synthesized observational studies of extreme events in these aquatic ecosystems, finding that many studies do not use consistent definitions of extreme events. Furthermore, many studies do not capture ecological responses across the full spatial scale of the events. In contrast, sampling often extends across longer temporal scales than the event itself, highlighting the usefulness of long-term monitoring. Many ecological studies of extreme events measure biological responses but exclude chemical and physical responses, underscoring the need for integrative and multidisciplinary approaches. To advance extreme event research, we suggest prioritizing pre- and postevent data collection, including leveraging long-term monitoring; making intersite and cross-scale comparisons; adopting novel empirical and statistical approaches; and developing funding streams to support flexible and responsive data collection.

The Future Is Big-and Small: Remote Sensing Enables Cross-Scale Comparisons of Microbiome Dynamics and Ecological Consequences.

Coupling remote sensing with microbial omics-based approaches provides a promising new frontier for scientists to scale microbial interactions across space and time. These data-rich, interdisciplinary methods allow us to better understand interactions between microbial communities and their environments and, in turn, their impact on ecosystem structure and function. Here, we highlight current and novel examples of applying remote sensing, machine learning, spatial statistics, and omics data approaches to marine, aquatic, and terrestrial systems. We emphasize the importance of integrating biochemical and spatiotemporal environmental data to move toward a predictive framework of microbiome interactions and their ecosystem-level effects. Finally, we emphasize lessons learned from our collaborative research with recommendations to foster productive and interdisciplinary teamwork.

Plant species determine tidal wetland methane response to sea level rise.

Blue carbon (C) ecosystems are among the most effective C sinks of the biosphere, but methane (CH4) emissions can offset their climate cooling effect. Drivers of CH4 emissions from blue C ecosystems and effects of global change are poorly understood. Here we test for the effects of sea level rise (SLR) and its interactions with elevated atmospheric CO2, eutrophication, and plant community composition on CH4 emissions from an estuarine tidal wetland. Changes in CH4 emissions with SLR are primarily mediated by shifts in plant community composition and associated plant traits that determine both the direction and magnitude of SLR effects on CH4 emissions. We furthermore show strong stimulation of CH4 emissions by elevated atmospheric CO2, whereas effects of eutrophication are not significant. Overall, our findings demonstrate a high sensitivity of CH4 emissions to global change with important implications for modeling greenhouse-gas dynamics of blue C ecosystems.

The greenhouse gas offset potential from seagrass restoration.

Awarding CO2 offset credits may incentivize seagrass restoration projects and help reverse greenhouse gas (GHG) emissions from global seagrass loss. However, no study has quantified net GHG removal from the atmosphere from a seagrass restoration project, which would require coupled Corg stock and GHG flux enhancement measurements, or determined whether the creditable offset benefit can finance the restoration. We measured all of the necessary GHG accounting parameters in the 7-km2 Zostera marina (eelgrass) meadow in Virginia, U.S.A., part of the largest, most cost-effective meadow restoration to date, to provide the first seagrass offset finance test-of-concept. Restoring seagrass removed 9,600 tCO2 from the atmosphere over 15 years but also enhanced both CH4 and N2O production, releasing 950 tCO2e. Despite tripling the N2O flux to 0.06 g m-2 yr-1 and increasing CH4 8-fold to 0.8 g m-2 yr-1, the meadow now offsets 0.42 tCO2e ha-1 yr-1, which is roughly equivalent to the seagrass sequestration rate for GHG inventory accounting but lower than the rates for temperate and tropical forests. The financial benefit for this highly successful project, $87 K at $10 MtCO2e-1, defrays ~10% of the restoration cost. Managers should also consider seagrass co-benefits, which provide additional incentives for seagrass restoration.