Expanded Consumer Niche Widths May Signal an Early Response to Spatial Protection

Marine management interventions are increasingly being implemented with the explicit goal of rebuilding ocean ecosystems, but early responses may begin with alterations in ecological interactions preceding detectable changes in population-level characteristics. To establish a baseline from which to monitor the effects of spatial protection on reef fish trophic ecology and track future ecosystem-level changes, we quantified temperate reef fish densities, size, biomass, diets and isotopic signatures at nine sites nested within two fished and one five-year old marine protected area (MPA) on the northwest coast of Canada. We calculated rockfish (Sebastes spp.) community and species-specific niche breadth for fished and protected areas based on δ13C and δ15N values. We found that rockfish community niche width was greater inside the MPA relative to adjacent fished reefs due to an expanded nitrogen range, possibly reflecting early changes in trophic interactions following five years of spatial protection. Our data also demonstrated that the MPA had a positive effect on the δ15N signature of rockfish (i.e., trophic position), but the effect of rockfish length on its own was not well-supported. In addition, we found a positive interaction between rockfish length and δ15N signature, such that δ15N signatures of rockfish caught within the MPA increased more rapidly with body size than those caught in fished areas. Differences in rockfish size structure and biomass among fished and unfished areas were not clearly evident. Species of rockfish and lingcod varied in trophic and size responses, indicating that life-history traits play an important role in predicting MPA effects. These results may suggest early changes in trophic behavior of slow-growing rockfish due to predation risk by faster growing higher trophic level predators such as lingcod inside MPAs established on temperate reefs. Consequently, spatial protection may restore both the trophic and behavioral roles of previously fished consumers earlier and in measurable ways sooner than observable changes in abundance and size

North to south: ecosystem features determine seagrass community response to sea otter foraging

We compared sea otter recovery in California (CA) and British Columbia (BC) to determine how key ecosystem properties shape top-down effects in seagrass communities. Potential ecosystem drivers of sea otter foraging in CA and BC seagrass beds that we examined include the role of coastline complexity and environmental stress on sea otter effects. In BC, we found greater species richness across seagrass trophic assemblages. Furthermore, Cancer spp. crabs, an important link in the seagrass trophic cascade observed in CA, was less common. Additionally, the more recent reintroduction of sea otters, more complex coastline, and reduced environmental stress in BC seagrass habitats supported the hypothesis that sea otter foraging pressure is currently reduced in more northern latitudes. In order to manage the ecosystem features that lead to regional differences in top predator effects in seagrass communities, we review our findings, their spatial and temporal constraints, and present a social-ecological framework for future re- search

Deeper habitats and cooler temperatures moderate a climate-driven seagrass disease

Eelgrass creates critical coastal habitats worldwide and fulfills essential ecosystem functions as a foundation seagrass. Climate warming and disease threaten eelgrass, causing mass mortalities and cascading ecological impacts. Subtidal meadows are deeper than intertidal and may also provide refuge from the temperature-sensitive seagrass wasting disease. From cross-boundary surveys of 5761 eelgrass leaves from Alaska to Washington and assisted with a machine-language algorithm, we measured outbreak conditions. Across summers 2017 and 2018, disease prevalence was 16% lower for subtidal than intertidal leaves; in both tidal zones, disease risk was lower for plants in cooler conditions. Even in subtidal meadows, which are more environmentally stable and sheltered from temperature and other stressors common for intertidal eelgrass, we observed high disease levels, with half of the sites exceeding 50% prevalence. Models predicted reduced disease prevalence and severity under cooler conditions, confirming a strong interaction between disease and temperature. At both tidal zones, prevalence was lower in more dense eelgrass meadows, suggesting disease is suppressed in healthy, higher density meadows. These results underscore the value of subtidal eelgrass and meadows in cooler locations as refugia, indicate that cooling can suppress disease, and have implications for eelgrass conservation and management under future climate change scenarios

Disease surveillance by artificial intelligence links eelgrass wasting disease to ocean warming across latitudes

Ocean warming endangers coastal ecosystems through increased risk of infectious disease, yet detection, surveillance, and forecasting of marine diseases remain limited. Eelgrass (Zostera marina) meadows provide essential coastal habitat and are vulnerable to a temperature-sensitive wasting disease caused by the protist Labyrinthula zosterae. We assessed wasting disease sensitivity to warming temperatures across a 3500 km study range by combining long-term satellite remote sensing of ocean temperature with field surveys from 32 meadows along the Pacific coast of North America in 2019. Between 11% and 99% of plants were infected in individual meadows, with up to 35% of plant tissue damaged. Disease prevalence was 3× higher in locations with warm temperature anomalies in summer, indicating that the risk of wasting disease will increase with climate warming throughout the geographic range for eelgrass. Large-scale surveys were made possible for the first time by the Eelgrass Lesion Image Segmentation Application, an artificial intelligence (AI) system that quantifies eelgrass wasting disease 5000× faster and with comparable accuracy to a human expert. This study highlights the value of AI in marine biological observing specifically for detecting widespread climate-driven disease outbreaks.This work was supported by the National Science Foundation (awards OCE-1829921, OCE-1829922, OCE-1829992, OCE-1829890). This is contribution 104 from the Smithsonian's MarineGEO and Tennenbaum Marine Observatories Network.Peer reviewe

Data and code from: Deeper habitats and cooler temperatures moderate a climate-driven disease in an essential marine habitat

Please cite as: Olivia Graham, Tiffany Stephens, Brendan Rappazzo, Corinne Klohmann, Sukanya Dayal, Emily Adamczyk, Angeleen Olson, Margot Hessing-Lewis, Morgan Eisenlord, Bo Yang, Colleen Burge, Carla Gomes, Drew Harvell. (2022) Data and code from: Deeper habitats and cooler temperatures moderate a climate-driven disease in an essential marine habitat [dataset] Cornell University eCommons Repository. https://doi.org/10.7298/6ybh-w566These files contain data and R code supporting all results reported in Graham et al. "Deeper habitats and cooler temperatures moderate a climate-driven disease in an essential marine habitat." In Graham et al., we found: Eelgrass creates critical coastal habitats worldwide and fulfills essential ecosystem functions as a foundation seagrass. Warming and disease threaten eelgrass meadows with mass mortalities and cascading ecological impacts, even in pristine locations. Although deeper, subtidal meadows are valuable fish nursery grounds and may also provide refuge from the climate-fueled seagrass wasting disease, nothing is known about differences in disease levels across remote locations in northern latitudes and between tidal zones (intertidal and subtidal meadows). From cross-boundary surveys on 5,761 eelgrass leaves from Alaska to Washington assisted with a machine-language algorithm, we measured outbreak conditions with average disease prevalence over 66% in intertidal and 50% in subtidal. In field surveys, disease was consistently lower in subtidal compared to adjacent intertidal meadows; remotely-sensed temperatures revealed significant associations between spring temperature anomalies and disease. While new studies show links between warm temperature anomalies and increased disease, our work detects beneficial effects of cooling in colder water anomalies. Disease was reduced in all regions except Puget Sound in the cooler summer of 2017. Pooled across both years, predicted disease prevalence was nearly 40% lower for subtidal than intertidal leaves, but in both tidal zones, disease risk was lower for plants in cooler conditions. Even in the ecologically most valuable subtidal meadows, we observed high disease levels, with half of the sites exceeding 50% prevalence. Disease models predicted reduced disease prevalence and severity under cooler conditions, confirming a strong interaction between disease and temperature. Finally, at both tidal zones, prevalence was reduced in more dense eelgrass meadows, suggesting disease is suppressed in healthy, higher density meadows. These results highlight the value of subtidal eelgrass meadows and meadows in cooler locations as refugia from the highest disease levels, indicate cooling can suppress disease, and have implications for eelgrass conservation and management under future climate change scenarios.The following generous funds supported this work: Cornell University’s Atkinson Center for Sustainable Biodiversity Fund, Cornell Engaged Graduate Student Grant, Cornell Sigma Xi Research Grant, Andrew W. Mellon Student Research Grant, Dr. Carolyn Haugen, University of Washington Friday Harbor Labs Graduate Research Fellowship Endowment, Women Diver’s Hall of Fame Scholarship in Marine Conservation to OJG; NSF-REU and Susan Lynch support for the Cornell Ocean Research Apprenticeship for Lynch Scholars to CK and SD; NSF awards OCE-1829921 and Washington SeaGrant (grant #NA18OAR4170095) to CB, Carolyn Friedman, CDH; NSF CompSustNet: Expanding the Horizons of Computational Sustainability (grant #1522054) to CG; Tula Foundation to OJG, EA, AO, MHL

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