ABSTRACT
In seagrass food webs, small invertebrate mesograzers often exert top-down control on algal epiphytes growing on seagrass blades, which in turn releases the seagrass from competition for light and nutrients. Yet, nearshore habitat boundaries are permeable, and allochthonous subsidies can provide alternative food sources to in-situ production in seagrass meadows, which may in turn alter mesograzer-epiphyte interactions. We examined the contribution of allochthonous kelp (Nereocystis luetkeana), autochthonous epiphytic macroalgal (Smithora naiadum), Ulva lactuca, and seagrass production to mesograzer diets in a subtidal Zostera marina (eelgrass) meadow. In both choice feeding experiments and isotopic analysis, mesograzer diets revealed a preference for allochthonous N. luetkeana over Z. marina, S. naiadum, and U. lactuca. Notably, Idotea resecata showed an ~20x greater consumption rate for N. luetkeana in feeding experiments over other macrophytes. In the meadow, we found a positive relationship between epiphytic S. naiadum and gammarid amphipod biomass suggesting weak top-down control on the S. naiadum biomass. Epiphyte biomass may be driven by bottom-up factors such as environmental conditions, or the availability and preference of allochthonous kelp, though further work is needed to disentangle these interactions. Additionally, we found that gammarid and caprellid amphipod biomass were positively influenced by adjacency to kelp at seagrass meadow edges. Our findings suggest that N. luetkeana kelp subsidies are important to the diets of mesograzers in Z. marina meadows. Spatial planning and management of marine areas should consider trophic linkages between kelp and eelgrass habitats as a critical seascape feature if the goal is to conserve nearshore food web structure and function.
ABSTRACT
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.
