Resistance of rocky intertidal communities to oceanic climate fluctuations.

A powerful way to predict how ecological communities will respond to future climate change is to test how they have responded to the climate of the past. We used climate oscillations including the Pacific Decadal Oscillation (PDO), North Pacific Gyre Oscillation, and El Niño Southern Oscillation (ENSO) and variation in upwelling, air temperature, and sea temperatures to test the sensitivity of nearshore rocky intertidal communities to climate variability. Prior research shows that multiple ecological processes of key taxa (growth, recruitment, and physiology) were sensitive to environmental variation during this time frame. We also investigated the effect of the concurrent sea star wasting disease outbreak in 2013-2014. We surveyed nearly 150 taxa from 11 rocky intertidal sites in Oregon and northern California annually for up to 14-years (2006-2020) to test if community structure (i.e., the abundance of functional groups) and diversity were sensitive to past environmental variation. We found little to no evidence that these communities were sensitive to annual variation in any of the environmental measures, and that each metric was associated with < 8.6% of yearly variation in community structure. Only the years elapsed since the outbreak of sea star wasting disease had a substantial effect on community structure, but in the mid-zone only where spatially dominant mussels are a main prey of the keystone predator sea star, Pisaster ochraceus. We conclude that the established sensitivity of multiple ecological processes to annual fluctuations in climate has not yet scaled up to influence community structure. Hence, the rocky intertidal system along this coastline appears resistant to the range of oceanic climate fluctuations that occurred during the study. However, given ongoing intensification of climate change and increasing frequencies of extreme events, future responses to climate change seem likely.

Strategies for managing marine disease.

The incidence of emerging infectious diseases (EIDs) has increased in wildlife populations in recent years and is expected to continue to increase with global environmental change. Marine diseases are relatively understudied compared with terrestrial diseases but warrant parallel attention as they can disrupt ecosystems, cause economic loss, and threaten human livelihoods. Although there are many existing tools to combat the direct and indirect consequences of EIDs, these management strategies are often insufficient or ineffective in marine habitats compared with their terrestrial counterparts, often due to fundamental differences between marine and terrestrial systems. Here, we first illustrate how the marine environment and marine organism life histories present challenges and opportunities for wildlife disease management. We then assess the application of common disease management strategies to marine versus terrestrial systems to identify those that may be most effective for marine disease outbreak prevention, response, and recovery. Finally, we recommend multiple actions that will enable more successful management of marine wildlife disease emergencies in the future. These include prioritizing marine disease research and understanding its links to climate change, improving marine ecosystem health, forming better monitoring and response networks, developing marine veterinary medicine programs, and enacting policy that addresses marine and other wildlife diseases. Overall, we encourage a more proactive rather than reactive approach to marine wildlife disease management and emphasize that multidisciplinary collaborations are crucial to managing marine wildlife health.

Increasing instability of a rocky intertidal meta-ecosystem.

Climate change threatens to destabilize ecological communities, potentially moving them from persistently occupied "basins of attraction" to different states. Increasing variation in key ecological processes can signal impending state shifts in ecosystems. In a rocky intertidal meta-ecosystem consisting of three distinct regions spread across 260 km of the Oregon coast, we show that annually cleared sites are characterized by communities that exhibit signs of increasing destabilization (loss of resilience) over the past decade despite persistent community states. In all cases, recovery rates slowed and became more variable over time. The conditions underlying these shifts appear to be external to the system, with thermal disruptions (e.g., marine heat waves, El Niño-Southern Oscillation) and shifts in ocean currents (e.g., upwelling) being the likely proximate drivers. Although this iconic ecosystem has long appeared resistant to stress, the evidence suggests that subtle destabilization has occurred over at least the last decade.

Little evidence for genetic variation associated with susceptibility to sea star wasting syndrome in the keystone species Pisaster ochraceus.

The keystone species Pisaster ochraceus suffered mass mortalities along the northeast Pacific Ocean from Sea Star Wasting Syndrome (SSWS) outbreaks in 2013-2016. SSWS causation remains of debate, leading to concerns as to whether outbreaks will continue to impact this species. Considering the apparent link between ocean temperature and SSWS, the future of this species and intertidal communities remains uncertain. Surveys of co-occurring apparently normal and wasting P. ochraceus along the central Oregon coast in 2016 allowed us to address whether variation in disease status showed genetic variation that may be associated with differences in susceptibility to SSWS. We performed restriction site-associated DNA sequencing (2bRAD-seq) to genotype ~72,000 single nucleotide polymorphism (SNP) loci across apparently normal and wasting sea stars. Locus-specific analyses of differentiation (FST ) between disease-status groups revealed no signal of genetic differences separating the two groups. Using a multivariate approach, we observed weak separation between the groups, but identified 18 SNP loci showing highest discriminatory power between the groups and scanned the genome annotation for linked genes. A total of 34 protein-coding genes were found to be located within 15 kb (measured by linkage disequilibrium decay) of at least one of the 18 SNPs, and 30 of these genes had homologies to annotated protein databases. Our results suggest that the likelihood of developing SSWS symptoms does not have a strong genetic basis. The few genomic regions highlighted had only modest levels of differentiation, but the genes associated with these regions may form the basis for functional studies aiming to understand disease progression.

Transformative Research Is Not Easily Predicted.

Transformative research (TR) statements in scientific grant proposals have become mainstream. However, TR is defined as radically changing our understanding of a concept, causing a paradigm shift, or opening new frontiers. We argue that it is rarely possible to predict the transformative nature of research. Interviews and surveys of 78 transformative ecologists suggest that most TR began with incremental goals, while transformative potential was recognized later. Most respondents thought TR is unpredictable and should not be prioritized over 'incremental' research that typically leads to breakthroughs. Importantly, TR directives might encourage scientists to overstate the importance of their research. We recommend that granting agencies (i) allocate only a subset of funds to TR and (ii) solicit more realistic proposal statements.

Shifts in intertidal zonation and refuge use by prey after mass mortalities of two predators.

Recent mass mortalities of two predatory sea star species provided an unprecedented opportunity to test the effect of predators on rocky intertidal prey. Mass mortalities provide insight that manipulative experiments cannot because they alter ecosystems on a larger scale, for longer time periods, and remove both organisms and their cues from the environment. We examined shifts in population size structure, vertical zonation, and use of emersed refuge habitats outside tidepools by the abundant herbivorous black turban snail Tegula funebralis, both before and after the successive mortalities of two predatory sea stars. The small cryptic predator Leptasterias spp. suffered a localized but extreme mortality event in November 2010, followed by two mass mortalities of the keystone predator Pisaster ochraceus in August 2011 and autumn 2013. After the local extinction of Leptasterias, the population size of Tegula more than doubled. Also, since Leptasterias primarily inhabited only mid to low intertidal tidepools at this site, small and medium sized snails (which are preferred by Leptasterias) shifted lower in the intertidal and into tidepools after the mortality of Leptasterias. After the mortality of Pisaster in August 2011, large snails did not shift lower in the intertidal zone despite being preferred by Pisaster. Small and medium sized snails became denser in the higher zone and outside tidepools, which was not likely due to Pisaster mortality. Previous studies concluded that Pisaster maintained vertical size gradients of snails, but our data implicate the overlooked predator Leptasterias as the primary cause. This natural experiment indicated that (1) predators exert top-down control over prey population sizes and lower limits, (2) vertical zonation of prey are dynamic and controlled in part by prey behavior, and (3) predators exert the strongest effects on more vulnerable individuals, which typically inhabit stressful habitats higher on the shore or outside tidepools to avoid predation. Because the mass mortalities of two predators drastically reduced both the predation pressure and the chemical cues of predators in the environment, we were able to investigate both the effects of predators on prey populations and the effects on mobile prey behavior.

Correction: Sea Star Wasting Disease in the Keystone Predator Pisaster ochraceus in Oregon: Insights into Differential Population Impacts, Recovery, Predation Rate, and Temperature Effects from Long-Term Research.

[This corrects the article DOI: 10.1371/journal.pone.0153994.].

Sea Star Wasting Disease in the Keystone Predator Pisaster ochraceus in Oregon: Insights into Differential Population Impacts, Recovery, Predation Rate, and Temperature Effects from Long-Term Research.

Sea star wasting disease (SSWD) first appeared in Oregon in April 2014, and by June had spread to most of the coast. Although delayed compared to areas to the north and south, SSWD was initially most intense in north and central Oregon and spread southward. Up to 90% of individuals showed signs of disease from June-August 2014. In rocky intertidal habitats, populations of the dominant sea star Pisaster ochraceus were rapidly depleted, with magnitudes of decline in density among sites ranging from -2x to -9x (59 to 84%) and of biomass from -2.6x to -15.8x (60 to 90%) by September 2014. The frequency of symptomatic individuals declined over winter and persisted at a low rate through the spring and summer 2015 (~5-15%, at most sites) and into fall 2015. Disease expression included six symptoms: initially with twisting arms, then deflation and/or lesions, lost arms, losing grip on substrate, and final disintegration. SSWD was disproportionally higher in orange individuals, and higher in tidepools. Although historically P. ochraceus recruitment has been low, from fall 2014 to spring 2015 an unprecedented surge of sea star recruitment occurred at all sites, ranging from ~7x to 300x greater than in 2014. The loss of adult and juvenile individuals in 2014 led to a dramatic decline in predation rate on mussels compared to the previous two decades. A proximate cause of wasting was likely the "Sea Star associated Densovirus" (SSaDV), but the ultimate factors triggering the epidemic, if any, remain unclear. Although warm temperature has been proposed as a possible trigger, SSWD in Oregon populations increased with cool temperatures. Since P. ochraceus is a keystone predator that can strongly influence the biodiversity and community structure of the intertidal community, major community-level responses to the disease are expected. However, predicting the specific impacts and time course of change across west coast meta-communities is difficult, suggesting the need for detailed coast-wide investigation of the effects of this outbreak.