The role of apex predators, habitat, and seascape complexity on nearshore fish assemblages in Southeast, Alaska

Dissertation (Ph.D.) University of Alaska Fairbanks, 2023Nearshore marine ecosystems contain dynamic and complex submerged vegetated habitats that offer shelter and prey for juvenile, migratory, and residential species, including many commercial, subsistence, and recreationally important species. The efficacy of the nursery role, shelter, and source of prey of the nearshore is influenced by various abiotic and biotic forces and in this dissertation, we examine the influence of submerged vegetation type, presence of apex predators, and the seascape context on patterns of nearshore fish assemblages in southern Southeast Alaska. We found species-specific responses by juvenile salmon in the nearshore, with seasonality overwhelmingly driving juvenile salmon abundance in eelgrass meadows and Chum Salmon present in greater abundance in understory kelp beds compared to eelgrass meadows, whereas Pink Salmon exhibited no difference. As a known apex predator, the reintroduction of sea otters likewise altered the nearshore fish assemblage with increased richness in eelgrass meadows and assemblage-wide shifts in understory kelps. Finally, in addition to habitat type and apex predators, spatial patterning and presence of adjacent vegetation can affect the nursery role of nearshore habitats. We observed differences in the fish assemblage in eelgrass meadows sampled in homogeneous seascapes with continuous eelgrass meadows and heterogeneous seascapes that included adjacent habitats, including more abundant commercial and forage species in heterogeneous seascapes. This research reinforces the importance of nearshore ecosystems in supporting robust fisheries and highlights the structuring role that submerged vegetation, apex predators, and complex seascapes have in sustaining diverse fish populations. Considering the greater ecological dynamics in the nearshore is vital for decision making in habitat conservation and management and for evaluating its role for fisheries, particularly in the context of increased threats to nearshore ecosystems.National Science Foundation Biological Oceanography grant (#1635716), Coastal Science, Engineering and Education for Sustainability (SEES) grant (#1600230), the Earthwatch Institute, National Science Foundation Graduate Research Fellowship, Biomedical Learning and Student Training (BLaST), Rasmuson Foundation, American Fisheries Society Hutton Scholarship, and Sealaska Heritage Institute ‘Opening the Box’ grant, Established Program to Stimulate Competitive Research (EPSCoR), the University of Alaska Fairbanks Graduate School, and the Alaska Chapter of the American Fisheries SocietyChapter 1: General introduction -- Chapter 2: Juvenile Chum and Pink Salmon use of submerged vegetative habitats in Southeast Alaska -- Chapter 3: Shifts in nearshore fish assemblages following reintroduction of an apex predator -- Chapter 4: Seascape complexity and habitat heterogeneity influences Alaskan eelgrass fish assemblages -- Chapter 5: General conclusion -- Appendices

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

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

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

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