Sarah A. Gravem

Marine diseases are increasing globally, posing significant threats to both marine and human populations. Establishing ecosystem health baselines, detecting emerging diseases in marine wildlife and responding in time to manage an outbreak require a plan to be in place before a disease emergency unfolds. This enables monitoring and response networks to immediately begin to identify the etiologic agent, track disease progression, assess the ecological or economic risks, and prioritize the most appropriate and effective management strategies. Here, we present a marine disease outbreak contingency plan where a suspected infectious disease has caused a sudden increase in mortality of a generic marine wildlife host species, and much of the plan is also relevant for non-pathogenic mortality events and protected or economically valuable host species. The contingency plan has three sections: Diagnostics and Disease Dynamics, Ecology and Environment, and Mitigation and Remediation. Each section describes major goals and action items at different phases of an outbreak and highlights actions taken during the sea star wasting disease outbreak as a case study in disease response. We recommend strategies for increasing the overall preparedness for disease emergencies. Given our collective dependence on coastal ocean resources and the expected increase in marine disease outbreaks with climate change, we emphasize the importance of infrastructure and a network of human communities to address disease emergencies. This article is part of the theme issue ‘Managing infectious marine diseases in wild populations’.

Mass mortality from disease epidemics challenges the resistance and resilience of populations and communities. Assessing the impacts and consequences of such events is crucially dependent on long‐term datasets. In 2013–2016, sea star wasting disease (SSWD) caused population‐wide crashes of the archetypal keystone species, the sea star Pisaster ochraceus , along the North American west coast. We used two long‐term datasets to assess the resilience of Pisaster populations to this perturbation in Oregon: a 16‐year time series (2007–2023) of annual predation rate at seven sites and a 23‐year time series (2001–2024) of density and size of Pisaster at eight sites. In spring 2015, a novel and massive Pisaster recruitment event occurred at all sites, averaging 3.00 ± 0.57 recruits m ⁻² (±SE), an 8100% increase compared to Pre‐SSWD. Elevated but spatiotemporally variable recruitment has persisted over the subsequent decade. As expected, SSWD drove predation rates to near‐zero. This persisted for 3–8 years depending on site, and as of 2024, predation rates at two sites remain unrecovered. Before SSWD, population size structure was relatively stable, consisting mostly of large adults with virtually no recruitment. After the outbreak, density, average size, and biomass density declined at most sites, while SSWD persisted at low levels, averaging ~4% symptomatic per year. As of the Current period (2021–2024), density and biomass density had recovered at all sites and often overshot prior levels, but average body size recovered at only three of seven sites. However, the 2014 crash and the post‐2014 recruitment events apparently destabilized the populations; density remains more variable among years at all but two sites. To test the return of populations to Pre‐SSWD structure, we developed a novel ‘recovery index’ based on density and size structure and found that only half the sites had recovered. This index tests the classic “ball and cup” stability heuristic and suggests that the epidemic shifted the prior adult‐dominated state into an alternate persistent state characterized by pulses of recruits and juveniles. However, the system is clearly recovering, and if a causal link exists between the adult crash and the recruitment boom, this metapopulation may be resilient to mass mortality.

Predator loss can cause shifts in ecosystem state, especially when accompanied by changes in the behaviour of its prey. The recent decline of predatory sunflower sea stars Pycnopodia helianthoides and a coincident a decline of kelp forests across the northeastern Pacific raises questions about their role in kelp forest ecosystem maintenance and recovery. While P. helianthoides may support kelp forests by consuming herbivorous sea urchins, less is known about their non-consumptive effects, especially in degraded habitats. Here, we ask: How do the non-consumptive effects of this predator vary among prey species, and what are the emergent effects on community-level grazing pressure in a degraded habitat when kelp is reintroduced? We conducted a field experiment, where we deployed kelp blades in urchin barrens at discrete distances from caged P. helianthoides and control cages for 24 h. We demonstrate a reduction in the density of red sea urchins Mesocentrotus franciscanus nearest the sunflower star and no effect on green sea urchins Strongylocentrotus droebachiensis . Our results suggest the chemical cue of P. helianthoides elicits a localized landscape of fear of approximately 15 m ² that suppresses grazing, and that the non-consumptive effects of P. helianthoides on sea urchin behaviour may be important for kelp restoration.

Aim: Surveying the demography of populations near species range edges may indicate their vulnerability to range contractions or local extinction as the climate changes. In the rocky intertidal, not only are latitudinal ranges constricted by thermal stress, but tides also create zonation or a ‘vertical range’ driven by sharp environmental gradients. By investigating demographics along the latitudinal and vertical ranges simultaneously, we can investigate whether populations may be vulnerable to a changing climate.Location: Rocky intertidal habitats along west coast of the United States.Taxa: Ochre sea star Pisaster ochraceus, six‐armed sea star Leptasterias spp., emarginate whelks (Nucella ostrina and N. emarginata) and channeled whelk N. canaliculata.Methods: In 2018, we surveyed the demographics of the taxa above at 33 sites spanning > 11° latitude from central Oregon to southern California, near the southern range limits of each taxon. We counted and sized individuals from the high to low intertidal zone. To understand how environmental stress changed with latitude, we evaluated intertidal temperatures in situ, as well as tidal extremes, tidal amplitude and wave exposure using offshore buoys.Results: For all taxa, population density, the relative proportion of smaller individuals (except for emarginate whelks) and the upper vertical limits on the shore declined from north to south as temperatures increased and high tide height, tidal amplitude and wave heights decreased. In addition, smaller individual Leptasterias spp. generally inhabited lower shore levels while smaller individual emarginate whelks inhabited higher shore levels coastwide. For N. canaliculata, smaller animals were higher on shore northward, but lower on shore southward.Main Conclusions: While this study is a snapshot in time and cannot assess impacts of climate change, our surveys suggest environmentally‐related demographic limitation toward southern range limits and demographically vulnerable southern populations. Therefore, a warming climate may cause local extinctions or range contractions near southern limits.

Human‐caused global change produces biotic and abiotic conditions that increase the uncertainty and risk of failure of restoration efforts. A focus of managing for resiliency, that is, the ability of the system to respond to disturbance, has the potential to reduce this uncertainty and risk. However, identifying what drives resiliency might depend on how one measures it. An example of a system where identifying how the drivers of different aspects of resiliency can inform restoration under climate change is the northern coast of California, where kelp experienced a decline in coverage of over 95% due to the combination of an intense marine heat wave and the functional extinction of the primary predator of the kelp‐grazing purple sea urchin, the sunflower sea star. Although restoration efforts focused on urchin removal and kelp reintroduction in this system are ongoing, the question of how to increase the resiliency of this system to future marine heat waves remains open. In this paper, we introduce a dynamical model that describes a tritrophic food chain of kelp, purple urchins, and a purple urchin predator such as the sunflower sea star. We run a global sensitivity analysis of three different resiliency metrics (recovery likelihood, recovery rate, and resistance to disturbance) of the kelp forest to identify their ecological drivers. We find that each metric depends the most on a unique set of drivers: Recovery likelihood depends the most on live and drift kelp production, recovery rate depends the most on urchin production and feedbacks that determine urchin grazing on live kelp, and resistance depends the most on feedbacks that determine predator consumption of urchins. Therefore, an understanding of the potential role of predator reintroduction or recovery in kelp systems relies on a comprehensive approach to measuring resiliency.

Ecosystem function is maintained in part by direct species interactions, but indirect interactions and non‐consumptive effects may be of equal ecological importance. Along the west coast of North America, the recent population collapse of the predatory sunflower sea star Pycnopodia helianthoides has been implicated in the proliferation of the purple sea urchin Strongylocentrotus purpuratus, and a concurrent decline in kelp canopy cover in several locales. Recent work began to quantify the predation rates effects (i.e., direct consumptive effects) of Pycnopodia on sea urchins that may lead to density‐mediated indirect effects on kelp. However, the importance of non‐consumptive effects on urchin behavior and the possible trait‐mediated indirect effects of Pycnopodia on kelp are not well understood. This leaves a critical gap in our knowledge about how these predators may be controlling grazer populations and, indirectly, primary production by macroalgae in nearshore habitats. We measured the non‐consumptive behavioral effects of Pycnopodia on S. purpuratus in the laboratory including grazing rates, feeding behavior, and movement of starved versus fed urchins, the latter simulating urchin metabolic conditions within urchin barrens. We found that the presence of a waterborne Pycnopodia cue reduced the grazing rate of fed urchins by 50% over short (~24 h) time scales. In contrast, starved urchins consumed kelp and did not exhibit an escape response in the presence of a Pycnopodia cue. This study highlights a trait‐mediated indirect interaction between Pycnopodia, S. purpuratus, and kelp, showing how the urchin response to a predator cue may differ based on urchin metabolic conditions or ecosystem state, and helps clarify the positive role of Pycnopodia on kelp forest health.

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.

Research on intertidal community structure and recovery in the California Current System has largely focused on macrophytes and invertebrates occupying two‐dimensional, readily studied “open” rock surfaces. However, most rocky shores have a “third” dimension that includes channels, cracks, crevices, and overhangs whose organismal assemblages, termed “cryptic communities,” are poorly studied. Cryptic communities not only share many species with those on more accessible surfaces but also include high abundances of colonial invertebrates such as tunicates, sponges, bryozoans, and hydrozoans. We investigated species abundance and diversity of cryptic communities and tested their recovery from disturbance by comparing removal plots to undisturbed controls for ~1.5 years. Additionally, we tested whether community structure and recovery varied with contrasting large‐scale levels of ecological subsidies (invertebrate recruitment, nutrients, and phytoplankton) and local‐scale microhabitat differences (emersion and solar irradiation) on the Oregon Coast. We compared cryptic recovery rates to recovery rates on open‐surface communities. In cryptic communities, site explained most (92%) variance in community structure of undisturbed plots, while microhabitat metrics had little (1.2%) effect. Further, recovery rates were faster at a site with higher subsidy inputs than one with lower subsidies in both cryptic and noncryptic communities. Hence, larger scale environmental drivers appeared more important than local‐scale drivers within cryptic communities. Our research provides novel insight into intertidal cryptic surge channel community structure and dynamics.

Determining the relative influence of biotic and abiotic processes in structuring communities at local to large spatial scales is best understood using a biogeographic comparative‐experimental approach. Using this approach, previous work suggests that intertidal community dynamics (top‐down and bottom‐up effects) vary unimodally along an upwelling‐based productivity gradient, termed the Intermittent Upwelling Hypothesis (IUH). Evidence consistent with the IUH comes from the sessile invertebrate/predator (SIP) subweb in certain rocky intertidal communities, but whether this pattern extends to macrophyte/herbivore (MH) subwebs is unknown. Here we ask: Are MH subwebs also structured as predicted by the IUH? What is the relative importance of herbivory and predation in structuring these communities? Under what conditions do ecological subsidies like nutrients or propagule production drive community dynamics? And are omnivorous interactions important? We hypothesize that MH subwebs are driven by a new construct, the Grazing‐Weakening Hypothesis (GWH), which states that MH interactions weaken monotonically with increasing nutrients, with strong (weak) herbivory and low (high) macrophyte productivity at low (high) nutrients. We explored local‐to‐large spatial scale dynamics of both subwebs using a biogeographic comparative‐experimental factorial field experiment testing joint and separate effects of herbivores and predators between two continents. Experiments at 10 sites ranging from persistent upwelling to persistent downwelling regimes ran for 26–29 months in Oregon and California, and New Zealand (NZ) South Island. For the MH subweb, results were consistent with the GWH: herbivory declined and macrophytes increased with increasing nutrients. As expected, results for the SIP subweb were consistent with the IUH: predator effect size was unimodally related to upwelling. Overall, herbivory explained more variation in community structure than did predation, especially in NZ. Omnivory was weak, sessile invertebrates outcompeted macrophytes, and ocean‐driven subsidies provided the basic template driving ecosystem dynamics. We propose a unified meta‐ecosystem dynamics model combining MH and SIP results: with increased upwelling, sessile invertebrates and underlying dynamics vary unimodally (as in the IUH), while herbivory decreases and macrophytes generally increase. While this model was based on research in temperate ecosystems varying in upwelling regime, its wider applicability remains to be tested.

The recent collapse of predatory sunflower sea stars ( Pycnopodia helianthoides ) owing to sea star wasting disease (SSWD) is hypothesized to have contributed to proliferation of sea urchin barrens and losses of kelp forests on the North American west coast. We used experiments and a model to test whether restored Pycnopodia populations may help recover kelp forests through their consumption of nutritionally poor purple sea urchins ( Strongylocentrotus purpuratus ) typical of barrens. Pycnopodia consumed 0.68 S. purpuratus d ⁻¹ , and our model and sensitivity analysis shows that the magnitude of recent Pycnopodia declines is consistent with urchin proliferation after modest sea urchin recruitment, and even small Pycnopodia recoveries could generally lead to lower densities of sea urchins that are consistent with kelp-urchin coexistence. Pycnopodia seem unable to chemically distinguish starved from fed urchins and indeed have higher predation rates on starved urchins owing to shorter handling times. These results highlight the importance of Pycnopodia in regulating purple sea urchin populations and maintaining healthy kelp forests through top-down control. The recovery of this important predator to densities commonly found prior to SSWD, whether through natural means or human-assisted reintroductions, may therefore be a key step in kelp forest restoration at ecologically significant scales.