Juvenile Dungeness crab foraging behavior and lipid composition is altered more by food quantity than seawater pH in a multi-stressor experiment

Increases in atmospheric, anthropogenic carbon are driving reductions in seawater pH, a process referred to as ocean acidification. Reduced seawater pH can influence behavior of marine animals, but little is currently known about how juvenile crustaceans will respond. We conducted lab experiments to improve our understanding of the consequences of pH exposure and food quantity on juvenile Dungeness crab (Metacarcinus magister, (Dana, 1852)) behavior and nutritional condition. To understand the foraging and pH sensing behavior of juvenile crab, and how this interacts with their nutritional status, we exposed recently settled second instar juveniles to either ambient pH or reduced pH for 42-d, crossed with either a ‘maintenance’- or low-quantity ‘challenge’ diet treatment. After the experimental exposure period, we introduced crab into foraging and sensing pH behavior experiments. In the foraging experiment, we placed crab in a behavior arena with unidirectional flow, where we measured the food discovery time and time allocation of activities in 300-s trials for all individual crab. Food quantity and pH exposure influenced both the speed with which juvenile crab identified and allocation of activities but there was no interactive effect of experimental factors. For our pH sensing experiment, we used a two-current flume plumbed with both ambient and reduced pH seawater. This flow-through flume provided a choice between the pH treatment waters and allowed us to measure the amount of time individuals spent on either side of the arena in 300-s trials. There was no effect of prior diet or pH exposure on the amount of time juvenile crab spent in either seawater pH condition. In addition to the behavior trials, we evaluated crab nutritional condition by quantifying the total lipid content of whole-body tissues and fatty acid profile composition of juvenile crab fed either the maintenance or low-quantity diet during the experimental pH exposure period. The proportional fatty acid profiles differed for crab based on their diet and pH exposure, with no interactive effects. However, we did not detect differences in the concentrations of key summary categories of fatty acids (e.g., saturated, monounsaturated, or polyunsaturated) based on pH exposure. Our results indicate that reduced food availability has a greater impact on juvenile Dungeness crab foraging behavior and nutritional condition than reduced seawater pH exposure representing the 0.3 pH unit decrease predicted by 2100.National Oceanic and Atmospheric Administration's National Sea Grant College Program. National Science Foundation. US Department of Commerce. Oregon State Legislature. M. J. Murdock Trust Partners-in-Science.Highlights -- Abstract -- Keywords -- 1. Introduction -- 2. Materials and methods -- 3. Results -- 4. Discussion -- CRediT authorship contribution statement -- Declaration of Competing Interest -- Acknowledgements -- Appendix A. Supplementary data -- Data availability -- References.Ye

Tipping the balance: the impact of eelgrass wasting disease in a changing ocean

Infectious disease has the potential to cause devastating damage to valuable marine organisms and habitats. Eelgrass wasting disease (EGWD), caused by the pathogenic protist Labyrinthula zosterae (LZ), has caused mass die-offs in Zostera marina at regional and global scales. Despite this, little is known about the host-pathogen interaction or disease drivers in the Salish Sea. To determine the regional impact of EGWD, we measured summer prevalence and severity in the San Juan Islands, Padilla Bay, Hood Canal, South Puget Sound, and Willapa Bay. We used cultures and quantitative PCR to verify results, measuring LZ load in lesioned tissue from multiple sites. EGWD was present at all 16 sites surveyed, with prevalence ranging from 80% disease prevalence. Recent data suggest water temperature increases the virulence of LZ, indicating possible climate sensitivity. At our sites, water temperatures influenced both EGWD prevalence and severity, suggesting environmental conditions and climate change could impact the eelgrass-LZ relationship and lead to increased virulence. We ran a three-week controlled experiment to examine the impact of LZ infection on eelgrass shoots over time. We exposed half the eelgrass shoots to LZ infection and sampled shoots at seven time points. All exposed shoots showed signs of infection. EGWD severity and lesion number increased through time, corresponding with a measurable decrease in leaf and root growth and increased phenols. Our results show EGWD is widespread in Washington state eelgrass beds and suggests that EGWD severity is positively correlated with water temperature. Furthermore, EGWD has a detrimental effect on eelgrass health, potentially contributing to decreased density and meadow declines. While levels of EGWD in the field are variable, we identified four sites that are experiencing high prevalence. Further research is needed to understand the conditions leading to EGWD outbreaks

Food Web Consequences of a Seagrass Microparasite and a Crustacean Macroparasite

Despite their ubiquity and known ecological impacts, parasites are still infrequently considered in studies of trophic ecology. Additionally, the most recognized effects of marine parasites on food webs are those caused by mass mortalities. In contrast to these density-mediated effects, trait-mediated indirect interactions (TMII), where host ecological function is altered through parasitism, are less conspicuous but not necessarily less important. In this dissertation, I present studies of potential TMIIs of two marine parasites. The protist Labyrinthula zosterae D. Porter & Muehlstein (Lz) infects the eelgrass Zostera marina L. First, in Chapter II, I ask whether Lz may increase the nutrition of eelgrass tissue by synthesizing DHA, a nutritious ω-3 fatty acid (FA), based on Lz’s relatives. By culturing Lz on various substrates, I found that Lz produces DHA as its primary FA and in detectable amounts in diseased tissue. This suggested that diseased tissue may be more nutritious for eelgrass consumers, which I tested in Chapter III using the detritivorous copepod Tisbe sp. Lilljeborg. Providing Tisbe either healthy or diseased eelgrass segments, I asked whether diseased eelgrass was functionally like detritus and fostered copepod population growth. Diseased eelgrass segments produced greater copepod numbers than healthy ones. Resulting copepods did not show clear differences in DHA, suggesting that FA changes were less important than eelgrass material becoming more labile via disease. Nonetheless, this showed that disease may foster secondary production. In Chapter IV, I studied the effects of the rhizocephalan Sylon hippolytes M. Sars infecting the shrimp Pandalus danae Stimpson. Using a field survey, I found that Sylon increased rates of epibiosis on hosts, which may interfere with shrimp antipredator defenses. Infected shrimp also showed distinct FA profiles relative to uninfected ones, with changes substantial enough to alter dietary mixing model predictions. Thus, Sylon may affect marine trophic interactions and our understanding of them. Altogether, this work shows that Lz and Sylon can substantially alter their hosts, producing unrecognized TMIIs in their ecosystems. The results encourage further research into these systems and a greater appreciation for marine parasites in food webs. This dissertation includes both previously published and unpublished coauthored material

KEEN

Data from the Kelp Ecosystem Ecology Network project collected by CTEL

Eelgrass Wasting Disease: a Contributor to Decline in the San Juan Islands?

Understanding the possible reasons for eelgrass decline is especially important considering the importance of seagrasses as essential marine habitat and potential for mitigation of climate impacts. Eelgrass wasting disease of Zostera marina caused by the protist Labyrinthula zosterae presents as necrotic, black-edged lesions on eelgrass leaves and can destroy seagrass beds. This disease devastated Atlantic Z. marina beds in the 1930s and is currently common in the San Juan Archipelago. The prevalence of eelgrass wasting disease in the field varies over space and time, from nearly absent in some sites to almost 100% in other sites during its peak during the summer. Our 11 sites surveyed from 2012-2015 around the San Juan Islands show site-specific patterns of disease prevalence and severity over time but an overall increase in wasting disease prevalence between August 2013 and 2015. A four-month time series of surveys in 2015 shows the annual pattern of wasting disease outbreak between May and August. Furthermore, host demography influenced disease patterns, where the oldest, longest, and most dense beds are the most susceptible to disease. Further surveys coupled with laboratory and mesocosm experiments will investigate what local and regional factors facilitate eelgrass wasting disease in the San Juan Islands and its role in seagrass decline

Turning up the Heat on Sea Star Wasting DIsease

A sea star wasting disease (SSWD) epizootic linked to a densovirus devastated populations of Asteroidea over thousands of miles of the North American Pacific Coast in 2013, 2014 and 2015. Time series monitoring of the keystone intertidal species Pisaster ochraceus from the San Juan Islands, South Puget Sound, and Washington outer coast, showed rapid progression of the outbreak, extremely high mortality rates in 2014, and continuing levels of wasting in the survivors in 2015. Peak prevalence of disease and mortality at 16 sites ranged to 100%, with a mean of 61%. Analysis of field surveys showed strong size-specific and temperature-dependent disease risk. In laboratory experiments increased temperature accelerated disease progression and differentially affected adult and juvenile ochre stars. Warm temperature anomalies recorded in the summer of 2014 may have contributed to the rate and extent of SSWD impacts in the San Juan Islands. A subtidal species, Pycnopodia helianthoides, is more severely affected and currently undetected in our San Juan Island surveys and many diver reports from California to SE Alaska. This raises the question of what the longer term biodiversity impacts will be from this epizootic

Increases and decreases in marine disease reports in an era of global change

Outbreaks of marine infectious diseases have caused widespread mass mortalities, but the lack of baseline data has precluded evaluating whether disease is increasing or decreasing in the ocean. We use an established literature proxy method from Ward and Lafferty (Ward and Lafferty 2004 PLoS Biology2, e120 (doi:10.1371/journal.pbio.0020120)) to analyse a 44-year global record of normalized disease reports from 1970 to 2013. Major marine hosts are combined into nine taxonomic groups, from seagrasses to marine mammals, to assess disease swings, defined as positive or negative multi-decadal shifts in disease reports across related hosts. Normalized disease reports increased significantly between 1970 and 2013 in corals and urchins, indicating positive disease swings in these environmentally sensitive ectotherms. Coral disease reports in the Caribbean correlated with increasing temperature anomalies, supporting the hypothesis that warming oceans drive infectious coral diseases. Meanwhile, disease risk may also decrease in a changing ocean. Disease reports decreased significantly in fishes and elasmobranchs, which have experienced steep human-induced population declines and diminishing population density that, while concerning, may reduce disease. The increases and decreases in disease reports across the 44-year record transcend short-term fluctuations and regional variation. Our results show that long-term changes in disease reports coincide with recent decades of widespread environmental change in the ocean

Linking sewage pollution and water quality to spatial patterns of Porites lobata growth anomalies in Puako, Hawaii

Sewage pollution threatens the health of coastal populations and ecosystems, including coral reefs. We investigated spatial patterns of sewage pollution in Puako, Hawaii using enterococci concentrations and δN Ulva fasciata macroalgal bioassays to assess relationships with the coral disease Porites lobata growth anomalies (PGAs). PGA severity and enterococci concentrations were high, spatially variable, and positively related. Bioassay algal δN showed low sewage pollution at the reef edge while high values of resident algae indicated sewage pollution nearshore. Neither δN metric predicted PGA measures, though bioassay δN was negatively related to coral cover. Furthermore, PGA prevalence was much higher than previously recorded in Hawaii and the greater Indo-Pacific, highlighting Puako as an area of concern. Although further work is needed to resolve the relationship between sewage pollution and coral cover and disease, these results implicate sewage pollution as a contributor to diminished reef health

Seawater carbonate chemistry and juvenile dungeness crab foraging behavior and lipid composition

To understand the foraging and pH sensing behavior of juvenile crab, and how this interacts with their nutritional status, we exposed recently settled second instar juveniles to either ambient pH or reduced pH for 42-d, crossed with either a 'maintenance'- or low-quantity 'challenge' diet treatment. After the experimental exposure period, we introduced crab into foraging and sensing pH behavior experiments. In the foraging experiment, we placed crab in a behavior arena with unidirectional flow, where we measured the food discovery time and time allocation of activities in 300-s trials for all individual crab. This dataset is included in the OA-ICC data compilation maintained in the framework of the IAEA Ocean Acidification International Coordination Centre (see https://oa-icc.ipsl.fr). Original data were provided by the author of the related paper (see Related to) to the OA-ICC data curator. In order to allow full comparability with other ocean acidification data sets, the R package seacarb (Gattuso et al, 2024) was used to compute a complete and consistent set of carbonate system variables, as described by Nisumaa et al. (2010). In this dataset the original values were archived in addition with the recalculated parameters (see related PI). The date of carbonate chemistry calculation by seacarb is 2024-05-06

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