Rapid environmental changes significantly impact and reshape our oceans. Elevated temperatures can alter marine host-pathogen dynamics by increasing host stress and pathogen virulence, expanding pathogen ranges, and altering host ranges, thus triggering increased occurrence and severity of disease outbreaks (Harvell et al., 2002; Burge et al., 2014; Cohen et al., 2018; Burge and Hershberger, 2020). Climate-driven disease outbreaks can be especially devastating when they target foundation species—like seagrass and corals—that structure nearshore communities and play vital roles in ecosystem function (Harvell and Lamb, 2020). This paper examines the impacts of seagrass wasting disease (SWD) on eelgrass (Zostera marina) health and productivity.

Seagrass wasting disease historically shaped eelgrass meadows and continues to persist today. In the 1930s, SWD outbreaks decimated up to 90% of eelgrass meadows throughout the North Atlantic (Renn, 1936; Short et al., 1987; Muehlstein, 1989), reducing waterfowl, shrimp, scallop, and fish populations (Renn, 1936; Stauffer, 1937; Moffitt and Cottam, 1941; Milne and Milne, 1951) and compromising eelgrass ecosystem services (Orth et al., 2006). These and subsequent die-offs were traced to Labyrinthula zosterae (Muehlstein et al., 1988), which is now recognized as a virulent pathogen in eelgrass (Groner et al., 2014, 2016; Martin et al., 2016) and other seagrasses worldwide (reviewed in Sullivan et al., 2018). Given that eelgrass creates nursery and feeding grounds (Orth et al., 1984), filters and oxygenates seawater (Costanza et al., 1997; Hasegawa et al., 2008), stabilizes sediments (Fonseca et al., 1983), efficiently stores carbon (Duarte et al., 2005; Röhr et al., 2018), and plays important roles in nutrient cycling in nearshore communities (reviewed in Moore and Short, 2006), SWD can compromise the health of eelgrass individuals, populations, and entire coastal communities.

Understanding the impact of SWD on eelgrass health and productivity under field conditions is particularly pertinent, given the synergistic relationship between warming temperatures L. zosterae (Rasmussen, 1977; Muehlstein, 1992; Bull et al., 2012; Bockelmann et al., 2013; Dawkins et al., 2018; Groner et al., in press; Aoki et al., in review). Laboratory studies indicate the pathogen grows faster in vitro under elevated temperatures (Dawkins et al., 2018), and warmer temperatures coincided with historic (Rasmussen, 1977) and more recent disease outbreaks (Bull et al., 2012; Bockelmann et al., 2013). More recently, field surveys of natural eelgrass meadows in the San Juan Islands, Washington, United States indicate that elevated levels of SWD and declines in meadow density were significantly correlated with warmer winter (Groner et al., in press) and summer temperatures (Aoki et al., in review).

Despite the growing body of literature on L. zosterae biology and ecology and continued monitoring of SWD in natural eelgrass meadows (Bockelmann et al., 2012; Groner et al., 2014, 2016, in press; Jakobsson-Thor et al., 2018; Aoki et al., in review), little is known about the impacts of SWD on eelgrass under natural conditions. Laboratory studies have shown that L. zosterae attacks and consumes plant chloroplasts (Muehlstein, 1992), reduces photosynthetic capabilities of tissue (Ralph and Short, 2002), and creates large areas of necrotic tissue (Pokorny, 1967; Short et al., 1986). SWD therefore likely compromise eelgrass growth rates and ability to accumulate non-structural carbon in rhizomes, which contain high concentrations of sugar. Normally, this sugar accumulates during the summer growing season and fuels regrowth in spring (Burke et al., 1996). However, since SWD prevalence peaks during warm summer months (Bockelmann et al., 2013), disease could reduce these valuable sugar reserves and impair eelgrass growth the subsequent year. Here, we coupled ecological surveys and image analysis using artificial intelligence to determine the effect of SWD on eelgrass growth, health, and rhizome sugar in the field.

Eelgrass meadows are considered bioindicators of health within the Salish Sea, an inland sea spanning the United States-Canada border in the northeastern Pacific Ocean (Dennison et al., 1993; McManus et al., 2020), and have experienced high levels of SWD in recent years (Groner et al., 2014, 2016, in press; Aoki et al., in review), making this region an important location for understanding the ecological impacts of SWD. The aim of this study was to examine the effect of SWD on aboveground eelgrass growth and productivity and belowground sugar. We measured blade-level disease status (healthy or diseased), site-level disease prevalence (proportion of shoots with SWD), severity (proportion of tissue damaged by wasting disease lesions), and specific productivity (percentage of new blade area produced per day). Given the significant historical role of L. zosterae in the extirpation of many eelgrass meadows globally, we expected SWD to compromise eelgrass growth. Specifically, we expected plants with elevated levels of disease to have reduced blade growth rates and rhizome sugar concentrations compared to eelgrass with lower disease levels.

Globally, seagrasses are declining under pressure from coastal development, climate change, and disease (Orth et al., 2006; Waycott et al., 2009; Dunic et al., 2021). To sustain and conserve these crucial habitats and their ecosystem services, we must determine the impacts of disease on eelgrass health. Though laboratory studies have identified the impact of SWD on eelgrass photosynthesis (Ralph and Short, 2002) and necrosis (Pokorny, 1967; Short et al., 1986; Muehlstein, 1992) and field surveys continue to highlight outbreak-levels of disease (Groner et al., 2014, 2016, in press; Jakobsson-Thor et al., 2018; Aoki et al., in review), the direct impact of SWD on eelgrass growth and sugar reserves in natural meadows remains unknown. Here we show that SWD predicts reduced blade growth rates and rhizome sugar concentrations in natural meadows. However, given the observational nature of this field study, reverse causality could account for the reduced blade growth among eelgrass with elevated SWD severity. For example, slower growing eelgrass could be more susceptible to SWD compared to faster-growing eelgrass. The observed reduced blade growth rates also could be due to other confounding factors like blade-level differences in epiphyte loads, which have been associated with higher probabilities of eelgrass having SWD (Groner et al., 2016). Shading due to epiphytes could then impact both SWD severity and eelgrass growth.

Our observed SWD prevalence and severity levels were higher than historical measurements from nearby sites. Previously, intertidal field surveys from 2012–2013 found disease prevalence ranged from 6–79% (Groner et al., 2014, 2016) elsewhere in the San Juan Islands, WA. These disparities may in part be due to different methods for calculating prevalence. Groner et al. (2014) measured prevalence—the proportion of diseased blades relative to total number of blades—based on the longest blade on each shoot, while Groner et al. (2016) used the second-oldest intact blade on each shoot. Our results based on the proportion of diseased shoots relative to the total number of shoots indicated elevated SWD levels, like observed prevalence of 95.8–100% in intertidal Swedish eelgrass (Jakobsson-Thor et al., 2018). While some spatiotemporal variation is expected, the near-100% prevalence we observed at Fourth of July Beach could be in part linked to warmer ocean temperatures in 2019 (Aoki et al., in review; Amaya et al., 2020). In comparison to historical sea surface temperature records, summer 2019 temperatures were warmer locally in the San Juan Islands (Aoki et al., in review) and more broadly for the North Pacific (Amaya et al., 2020). This is important for eelgrass growth and health, since warm temperatures are associated with reduced production of phenolic compounds (Vergeer et al., 1995), which are used in microbial defense. Among eelgrass, thermal stress during warmer summer months can also increase respiration compared to photosynthesis, altering photosynthetic and growth rates (Phillips and Menez, 1988; Lee et al., 2007). Taxed by thermal stress and compromised growth, eelgrass could be more susceptible to SWD in certain conditions. Indeed, warming temperatures have recently been suggested to contribute to SWD outbreaks (Groner et al., 2014, in press; Martin et al., 2016; Sullivan et al., 2018; Aoki et al., in review).

While outbreaks of SWD have been implicated in meadow decline and collapse, understanding how disease impacts at individual blade- and shoot-levels scale across eelgrass populations and ecosystems remains unclear. Our results suggest that consequences of disease may have ecosystem-wide effects under natural conditions. Diseased, first-rank blades grew nearly 25% slower than healthy, first-rank blades. Because blade growth is concentrated in the youngest two blades (Sand-Jensen, 1975), our findings suggest SWD in natural meadows may limit shoot size at maturity by compromising the growth of the young, fast-growing blades. Disease on mature blades may also reduce total shoot growth. Although third-rank blades have lower specific productivity rates (blade elongation as a percent of existing blade area per day), absolute blade growth rates could exceed 200 mm²d^–1 for third-rank blades. These growth rates declined significantly with more severe SWD, suggesting that greater disease severity could limit plant growth. Rapidly spreading SWD may further influence total shoot physiology by interrupting transport of oxygen, photosynthesis products, and/or nutrients (Ralph and Short, 2002). The reduced rhizome sugar concentrations in severely diseased plants indicate SWD likely affected belowground carbon accumulation. Indeed, reduced non-structural carbon reserves were likely related to the observed, compromised blade growth, as diseased eelgrass has reduced photosynthetic capacity and may dedicate more resources to immune response (Vergeer et al., 1995). Ultimately, the combination of compromised growth and diminished sugar stores may reduce shoot survival, and in meadows such as this study site, where almost every plant had SWD, the impacts could accumulate at the ecosystem scale.

Reduced blade growth and rhizome sugars associated with severe SWD suggest that the disease can limit the persistence of entire eelgrass meadows over time. Some eelgrass meadows experience increased thermal and pathogen stress during warmer summer months (Young, 1943; Bockelmann et al., 2013; Aoki et al., in review). Taken together, this could reduce not only immediate eelgrass growth, which normally peaks in summer (Sand-Jensen, 1975), but also alter seasonal patterns in eelgrass productivity. Heavily diseased eelgrass with compromised growth and rhizome sugars may be vulnerable to environmental stressors over winter or early spring when eelgrass draws upon critical carbohydrate reserves from the previous summer (Burke et al., 1996). Less robust plants may be further vulnerable to SWD the following summer, creating a reinforcing feedback loop that could drive meadow-wide declines. Prior studies have noted that while SWD outbreaks can cause large-scale meadow die-offs, other meadows can support widespread disease without collapsing (Short et al., 1987; Jakobsson-Thor et al., 2018). The results from this study show how SWD may negatively impact the health of a meadow without immediately causing an ecosystem collapse. A precipitating disturbance or change in environmental conditions may then trigger widespread die-offs of vulnerable eelgrass. The global losses of eelgrass in the 1930s likely resulted from some combination of SWD and environmental stressors (Sullivan et al., 2013). However, studies testing the combined effects of SWD and stressors such as light availability, salinity, and temperature tend to occur in short-term laboratory mesocosms experiments (e.g., Brakel et al., 2019; Jakobsson-Thor et al., 2020). While these allow for carefully controlled testing of multiple stressors, they do not fully capture the long-term effects of SWD and environmental conditions in natural meadows. Additional field-based studies are needed to better understand these dynamic interactions over time.

In addition to making meadows more vulnerable to collapse, SWD may also impair meadow recovery following disturbance. At the meadow scale, reduced growth rates and carbohydrate reserves may limit regrowth of diseased shoots compared to healthy shoots. Rapid regrowth following disturbance is key to maintaining seagrass ecosystem services, such as carbon sequestration and biodiversity (Nowicki et al., 2017; Aoki et al., 2021); slower recovery rates may also increase meadow vulnerability to repeated disturbance, such as successive marine heat waves. By both increasing vulnerability and impairing recovery, SWD reduces the ecological resilience of eelgrass meadows and may impede conservation of existing meadows. Given the significant role of eelgrass in structuring coastal ecosystems and driving biogeochemical processes (reviewed in Moore and Short, 2006), reduced meadow resilience will have negative consequences for habitat provisioning, nutrient cycling, and other ecosystem services. Better understanding of the impact of chronic SWD on meadow trajectories through time is needed to optimize seagrass conservation and restoration efforts.

Further work is needed to understand the complex interactions between climate change, SWD, and eelgrass meadow resilience. The effects of environmental stressors on eelgrass, including changes in sea surface temperatures, salinity, ocean acidification, and altered light availability due to sea level rise, are not well understood (Short et al., 2016). Recent field surveys indicate positive associations between temperature and SWD (Groner et al., in press; Aoki et al., in review), while others suggest the relationship may be more bell-shaped, given the optimal thermal ranges for L. zosterae (Young, 1943; Olsen et al., 2015). Furthermore, the interactions between SWD and other environmental stressors remains unclear. Some reports indicate future conditions may reduce the effects of disease (Brakel et al., 2019), while others determined SWD is correlated with salinity (Jakobsson-Thor et al., 2018) and may be sensitive to pH (Groner et al., 2018). Certainly, interactions between temperature and other aspects of climate change may influence SWD but necessitate further research to understand these complex relationships and determine drivers of eelgrass resilience.

This study emphasizes the importance of considering disease alongside other climate change stressors to better predict the health and functioning of seagrass meadows in the Anthropocene. To the best of our knowledge, this is the first project to demonstrate that L. zosterae can significantly compromise eelgrass growth and belowground, non-structural carbohydrates in natural meadows. This work broadens our understanding of the effects of SWD on eelgrass productivity and is particularly relevant given mounting environmental stressors. Of course, these analyses were limited to eelgrass in one region over one summer growing season. Furthermore, at a site there can be multiple L. zosterae strains, which can vary in virulence (Martin et al., 2016) and produce significant differences in disease severity (Dawkins et al., 2018). Other groups of seagrass pathogens, including oomycetes and Phytomyxea (reviewed in Sullivan et al., 2018), should also be considered in the context of eelgrass health and productivity. As such, more studies are needed to examine these plant-pathogen relationships across the range of environmental conditions of existing eelgrass meadows. Eelgrass is a foundation species of critical coastal habitat across the northern hemisphere. Understanding the vulnerability of these meadows to disease is essential to their conservation across the species’ range and in a changing climate.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: The datasets analyzed for this study can be found in the Zenodo repository (https://doi.org/10.5281/zenodo.5339331).

OG, TS, and CH conceived of this study. OG, LA, and SD developed the methods. OG, LA, TS, and JS collected and processed samples in the laboratory. BR and CG developed EeLISA. BR processed images. LA analyzed the data. OG and LA wrote the manuscript. CG and CH provided resources and supervision. CH helped in the field. All authors contributed to editing this manuscript.

TS is employed by Seagrove Kelp Co. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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