A tale of two sea stars: recovery (ochre star) or endangerment (sunflower star) following the 2014 epidemic

During the summers of 2013 and 2014, populations of sea stars along the west coast from Alaska to Mexico were decimated by the sea star wasting disease (SSWD) epizootic. Two of the most highly affected species along this range are Pisaster ochraceus (the ochre star), the most common intertidal species, and Pycnopodia helianthoides (the sunflower star), the most common subtidal species, both of which are endemic to the western coast of the U.S. For the ochre star, in the San Juan Islands of Washington State, we measured high case fatality rates associated with disease prevalence over 90% during the summer of 2014. Low levels of disease were observed in the summers of 2015, 2016, and 2017. Population levels following the epizootic remain stable but small, and shifted in size structure from larger to smaller stars. At one site, a dramatic increase in both juvenile and adult ochre stars occurred in 2017, giving hope for future recovery. In contrast, the most common subtidal species, the sunflower star, also suffered catastrophic mortality in 2014. However, in this case, Citizen Science Monitoring in all oceanographic basins of the Salish Sea through 2017 shows an extraordinary decimation of this species, with no sign of recovery three years after the SSWD epizootic. Extremely low population size of sunflower stars raises concern about the capacity of this species to recover, as well as to resist other stochastic events in the future

Characterizing host-pathogen interactions between Zostera marina and Labyrinthula zosterae

Introduction Seagrass meadows serve as an integral component of coastal ecosystems but are declining rapidly due to numerous anthropogenic stressors including climate change. Eelgrass wasting disease, caused by opportunistic Labyrinthula spp., is an increasing concern with rising seawater temperature. To better understand the host-pathogen interaction, we paired whole organism physiological assays with dual transcriptomic analysis of the infected host and parasite. Methods Eelgrass (Zostera marina) shoots were placed in one of two temperature treatments, 11° C or 18° C, acclimated for 10 days, and exposed to a waterborne inoculation containing infectious Labyrinthula zosterae (Lz) or sterile seawater. At two- and five-days post-exposure, pathogen load, visible disease signs, whole leaf phenolic content, and both host- and pathogen- transcriptomes were characterized. Results Two days after exposure, more than 90% of plants had visible lesions and Lz DNA was detectable in 100% percent of sampled plants in the Lz exposed treatment. Concentrations of total phenolic compounds were lower after 5 days of combined exposure to warmer temperatures and Lz, but were unaffected in other treatments. Concentrations of condensed tannins were not affected by Lz or temperature, and did not change over time. Analysis of the eelgrass transcriptome revealed 540 differentially expressed genes in response to Lz exposure, but not temperature. Lz-exposed plants had gene expression patterns consistent with increased defense responses through altered regulation of phytohormone biosynthesis, stress response, and immune function pathways. Analysis of the pathogen transcriptome revealed up-regulation of genes potentially involved in breakdown of host defense, chemotaxis, phagocytosis, and metabolism. Discussion The lack of a significant temperature signal was unexpected but suggests a more pronounced physiological response to Lz infection as compared to temperature. Pre-acclimation of eelgrass plants to the temperature treatments may have contributed to the limited physiological responses to temperature. Collectively, these data characterize a widespread physiological response to pathogen attack and demonstrate the value of paired transcriptomics to understand infections in a host-pathogen system

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

Effects of Tidal Current Phase on the Distribution and Abundance of Rhinoceros Auklets (Cerorhinca monocerata) in Cattle Pass, Washington

The distribution and abundance of Rhinoceros Auklets is related to the tide cycle. I examined the effects of tidal currents phase on the distribution and abundance of the Rhinoceros Auklets though land-based surveys of the waters within Cattle Pass, Washington. Auklets aggregated in large groups inside Cattle Pass during flooding tides. During the slack high tide numbers dropped to intermediate levels, and then declined during ebbing tides and remained very low until the next flooding tide. During flooding tides the birds aggregated in the north end of the pass where prey availability was highest. Low abundance during the ebbing tide was attributed to high prey concentrations in the south end of the pass outside of the survey area. Auklets strongly preferred the center of the pass, where the main current flowed, over the calmer water closer to shore. This study shows the importance of the tide cycle in influencing the daily movements of Rhinoceros Auklets

Fine temporal scale sampling of tides, water masses, and seabirds

The main driver of ecosystem processes in northern coastal ecosystems is tidal current. Previous Pelagic Ecosystems Functions projects have examined relationships of tidal current throughout the channel, but they were not able to document and quantify temporal patterns. My objective was to investigate the fine scale temporal changes of physical and biological factors over a flooding tide through repeated sampling over a short temporal scale. I did this through sampling water masses and seabird abundance. Oceanography results indicated sampling water masses on a fine temporal scale can reveal previously undetected inputs and tidal patterns. Seabird results showed strong temporal patterns in abundance in response to tidal phase in overall abundance and on the species level. These results suggest fine temporal scale sampling can quantify patterns in seabird response to tidal phase that could be used to calibrate coarse scale sampling methods. Based on these results, I suggest fine temporal scale sampling be used in future studies to determine tidal relationships between seabirds and tides

A dangerous mix: Strain, dosage, and environment increase virulence of eelgrass wasting disease

Seagrass wasting disease, caused by the opportunistic marine pathogen Labyrinthula zosterae, has the potential to devastate important eelgrass habitats worldwide, yet little is known about the host-pathogen interaction and how the disease will be impacted by climate change. L. zosterae is part of a diverse taxon of opportunistic invertebrate and plant pathogens, which directly threaten fisheries and critical fisheries habitat. An area of particular concern is the role of virulence, the degree of host damage caused by a pathogen, often the product of its growth rate. Recent data suggests that temperature increases the virulence of Labyrinthulas, providing a mechanism for climate sensitivity. In this study we investigate the effect of L. zosterae strain, pathogen dosage, and temperature on the pathogen virulence. We tested L. zosterae virulence in Zostera marina by inoculating plant tissue with strains collected from a range of eelgrass populations. The 11 strains tested displayed qualitatively different virulence, with infection rates ranging from 0 to 100%. Pathogen virulence increased with dosage. Growth rates at a range of temperatures were tested for a subset of these strains. Results suggest the temperature increases growth rates, but the degree differs between strains. We conducted a controlled temperature experiment in which Z. marina adults and seedlings were allowed to acclimate to low (11° C), high (18° C) and fluctuating (between 11 and 18° C) water temperatures and then half these individuals were exposed to L. zosterae. Disease occurred more rapidly and with higher severity in seedlings and at high temperatures. Our results show that pathogen virulence is impacted by strain, dosage, and environment and suggests L zosterae will cause increased damage to eelgrass beds as water temperatures warm

EeLISA: Combating Global Warming Through the Rapid Analysis of Eelgrass Wasting Disease

Global warming is the greatest threat facing our planet, and is causing environmental disturbance at an unprecedented scale. We are strongly positioned to leverage the advancements of Artificial Intelligence (AI) and Machine Learning (ML) which provide humanity, for the first time in history, an analysis and decision making tool at massive scale. Strong evidence supports that global warming is contributing to marine ecosystem decline, including eelgrass habitat. Eelgrass is affected by an opportunistic marine pathogen and infections are likely exacerbated by rising ocean temperatures. The necessary disease analysis required to inform conservation priorities is incredibly laborious, and acts as a significant bottleneck for research. To this end, we developed EeLISA (Eelgrass Lesion Image Segmentation Application). EeLISA enables ecologist experts to train a segmentation module to perform this crucial analysis at human level accuracy, while minimizing their labeling time and integrating into their existing workflow. EeLISA has been deployed for over 16 months, and has facilitated the preparation of four manuscripts including a critical eelgrass study ranging from Southern California to Alaska. These studies, utilizing EeLISA, have led to scientific insight and discovery in marine disease ecology

Devastating Transboundary Impacts of Sea Star Wasting Disease on Subtidal Asteroids.

Sea star wasting disease devastated intertidal sea star populations from Mexico to Alaska between 2013-15, but little detail is known about its impacts to subtidal species. We assessed the impacts of sea star wasting disease in the Salish Sea, a Canadian / United States transboundary marine ecosystem, and world-wide hotspot for temperate asteroid species diversity with a high degree of endemism. We analyzed roving diver survey data for the three most common subtidal sea star species collected by trained volunteer scuba divers between 2006-15 in 5 basins and on the outer coast of Washington, as well as scientific strip transect data for 11 common subtidal asteroid taxa collected by scientific divers in the San Juan Islands during the spring/summer of 2014 and 2015. Our findings highlight differential susceptibility and impact of sea star wasting disease among asteroid species populations and lack of differences between basins or on Washington's outer coast. Specifically, severe depletion of sunflower sea stars (Pycnopodia helianthoides) in the Salish Sea support reports of major declines in this species from California to Alaska, raising concern for the conservation of this ecologically important subtidal predator

High infectivity and waterborne transmission of seagrass wasting disease

Pathogen transmission pathways are fundamental to understanding the epidemiology of infectious diseases yet are challenging to estimate in nature, particularly in the ocean. Seagrass wasting disease (SWD), caused by Labyrinthula zosterae, impacts seagrass beds worldwide and is thought to be a contributing factor to declines; however, little is known about natural transmission of SWD. In this study, we used field and laboratory experiments to test SWD transmission pathways and temperature sensitivity. To test transmission modes in nature, we conducted three field experiments out-planting sentinel Zostera marina shoots within and adjacent to natural Z. marina beds (20 ± 5 and 110 ± 5 m from bed edge). Infection rates and severity did not differ among outplant locations, implicating waterborne transmission. The infectious dose of L. zosterae through waterborne exposure was assessed in a controlled laboratory experiment. The dose to 50% disease was 6 cells ml−1 and did not differ with the temperatures tested (7.5°C and 15°C). Our results show L. zosterae is transmissible through water without direct contact with infected plants. Understanding the transmission dynamics of this disease in the context of changing ocean conditions will improve Z. marina protection and restoration in critical coastal habitats worldwide

Number of REEF surveys conducted by year in each studied basin in the Salish Sea.

<p>Number of REEF surveys conducted by year in each studied basin in the Salish Sea.</p