Pycnopodia Research Articles

The sunflower sea star reduces grazing rates of purple sea urchins dependent upon urchin starvation state

AbstractEcosystem 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.

Nearshore subtidal community response during and after sediment disturbance associated with dam removal

Dam removal is used increasingly to restore aquatic ecosystems and remove unnecessary or high-risk infrastructure. As the number of removals increases, there is a growing understanding about the hydrologic, geomorphic, and ecological responses to these removals. Most dam removal studies, however, focus on river and watershed responses to dam removal. The removal of two dams on the Elwha River provided a unique opportunity to characterize the response of nearshore (coastal) ecosystems. We conducted SCUBA surveys between 2011 and 2022 to quantify trajectories of change in a nearshore ecosystem during and after dam removal. We focused on the degree to which the abundances of kelp, benthic invertebrates, and fish changed in response to patterns of sediment fluxes during and after dam removal. Our findings point to two pathways of response depending on the disturbance mechanism and species type. Sites with persistent sediment deposition were characterized by wholesale community changes that did not recover to a before dam removal condition. Instead, the sites were colonized by new species that were largely absent prior to dam removal. Sites that experienced high turbidity but lacked persistent seafloor deposition were primarily characterized by a reduction in the abundance of kelp and other algae during dam removal and a rapid recovery after sediment flux to the nearshore declined. Dam removal influences on invertebrates and fish at these sites were more variable, benefiting some species and disadvantaging others. In addition to dam removal, sea star wasting syndrome and a marine heatwave exerted distinct controls on subtidal communities during the same period. The loss of the predatory sea star Pycnopodia helianthoides was associated with gains in some of its prey species, and kelp community changes reflected regional trends in ocean temperature and kelp abundance. The results presented here have important implications for understanding the response of marine ecosystems to future dam removals and similar sediment perturbation events.

Microbial dysbiosis precedes signs of sea star wasting disease in wild populations of Pycnopodia helianthoides

Sea star wasting (SSW) disease, a massive and ongoing epidemic with unknown cause(s), has led to the rapid death and decimation of sea star populations with cascading ecological consequences. Changes in microbial community structure have been previously associated with SSW, however, it remains unknown if SSW-associated dysbiosis is a mechanism or artifact of disease progression, particularly in wild populations. Here, we compare the microbiomes of the sunflower sea star, Pycnopodia helianthoides, before (Naïve) and during (Exposed and Wasting) the initial outbreak in Southeast Alaska to identify changes and interactions in the microbial communities associated with sea star health and disease exposure. We found an increase in microbial diversity (both alpha and beta diversity) preceding signs of disease and an increase in abundance of facultative and obligate anaerobes (most notably Vibrio) in both Exposed (apparently healthy) and Wasting animals. Complementing these changes in microbial composition was the initial gain of metabolic functions upon disease exposure, and loss of function with signs of wasting. Using Bayesian network clustering, we found evidence of dysbiosis in the form of co-colonization of taxa appearing in large numbers among Exposed and Wasting individuals, in addition to the loss of communities associated with Naïve sea stars. These changes in community structure suggest a shared set of colonizing microbes that may be important in the initial stages of SSW. Together, these results provide several complementary perspectives in support of an early dysbiotic event preceding visible signs of SSW.

Sunflower sea star predation on urchins can facilitate kelp forest recovery.

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.

Impact of the extinct megaherbivore Steller's sea cow (Hydrodamalis gigas) on kelp forest resilience

Giant kelp forests off the west coast of North America are maintained primarily by sea otter (Enhydra lutris) and sunflower sea star (Pycnopodia helianthoides) predation of sea urchins. Human hunting of sea otters in historical times, together with a marine heat wave and sea star wasting disease epidemic in the past decade, devastated these predators, leading to widespread occurrences of urchin barrens. Since the late Neogene, species of the megaherbivorous sirenian Hydrodamalis ranged throughout North Pacific giant kelp forests. The last species, H. gigas, was driven to extinction by human hunting in the mid-eighteen century. H. gigas was an obligate kelp canopy browser, and its body size implies that it would have had a significant impact on the system. Here, we hypothesize that sea cow browsing may have enhanced forest resilience. We tested this hypothesis with a mathematical model, comparing historical and modern community responses to marine heat waves and sea star wasting disease. Results indicate that forest communities were highly resistant to marine heat waves, yet susceptible to sea star wasting disease, and to disease in combination with warming. Resistance was greatest among systems with both sea cows and sea otters present. The model additionally predicts that historical communities may have exhibited delayed transitions after perturbation and faster recovery times. Sea cow browsing may therefore have enhanced resilience against modern perturbations. We propose that operationalizing these findings by mimicking sea cow herbivory could enhance kelp forest resilience.

Death of A Star


 Sea star wasting disease (SSWD), originally identified in 2013, is an epidemic impacting 20 species of sea stars along the west coast of North America. Two of the most impacted species, Pisaster ochraceus and Pycnopodia helianthoides are keystone species. The loss of these sea stars impacts oceanic life. Literature reviews were conducted from January to May 2022 to investigate the effect of SSWD on the food web of sea stars and decline of kelp. The apex predators of the ecosystem, P. helianthoides and P. ochraceus, have decreased drastically, while their prey, urchins, have increased immensely. As a result, kelp, a producer, has decreased significantly. The decline of the keystone species is highly concerning and could have drastic ecological impacts. The loss of kelp is extremely damaging for both marine life and Earth itself. If sea stars continue to decline, the amount of carbon dioxide and loss of kelp will become increasingly problematic for the ocean and health of the planet.

Changes in kelp forest communities off Washington, USA, during and after the 2014-2016 marine heatwave and sea star wasting syndrome

Canopy-forming kelps are foundation species in many coastal ecosystems, but kelp-forest communities are subject to abrupt state changes caused by environmental drivers and trophic dynamics. We examined changes in kelp communities at 5 sites along the Olympic Coast of Washington State, USA, during and following the recent perturbations of anomalous warm-water events and sea star wasting syndrome (SSWS). Anomalously warm water in 2013 and 2014 corresponded with a loss of approximately 50% of Macrocystis pyrifera and Nereocystis luetkeana canopy. However, the canopy quickly recovered, and stipe density increased after 2015. Purple sea urchins Strongylocentrotus purpuratus increased in density 164-fold, largely at one site, but this increase was first observed in 2017 and peaked in 2019, after the warm period. Sea stars did not show recovery from SSWS, with several species including Pycnopodia helianthoides continuing to decline. The majority of variation in assemblage structure occurred at the site level for kelps, macroinvertebrates, and fishes, while year explained most of the variability for juvenile rockfishes Sebastes spp. We did not see strong top-down effects of urchins on kelp, suggesting that top-down impacts were not dominant regionally during this period. In contrast, we found evidence for a bottom-up influence of kelp habitat on juvenile rockfishes, as rockfish recruits occurred with higher probability where kelp stipe density was higher. Our analyses highlight the importance of spatial variation in structuring changes in kelp forest communities associated with disturbance and suggest that it is essential to ensure the protection of a diversity of kelp forests.

Progress Toward Complete Life-Cycle Culturing of the Endangered Sunflower Star, Pycnopodia helianthoides.

AbstractUntil recently, the sunflower star, Pycnopodia helianthoides, was a dominant and common predator in a wide variety of benthic habitats in the northeast Pacific. Then, in 2013, its populations began to plummet across its entire range as a result of the spread of a phenomenon known as sea star wasting disease, or sea star wasting. Although dozens of sea star species were impacted by this wasting event, P. helianthoides seems to have suffered the greatest losses and is now listed by the International Union for the Conservation of Nature as the first critically endangered sea star. In order to learn more about the life history of this endangered predator and to explore the potential for its restoration, we have initiated a captive rearing program to attempt complete life-cycle (egg-to-egg) culture for P. helianthoides. We report our observations on holding and distinguishing individual adults, reproductive seasonality, larval development, inducers of settlement, and early juvenile growth and feeding. These efforts will promote and help guide conservation interventions to protect remaining populations of this species in the wild and facilitate its ultimate return.

Behavioral responses across a mosaic of ecosystem states restructure a sea otter–urchin trophic cascade

Consumer and predator foraging behavior can impart profound trait-mediated constraints on community regulation that scale up to influence the structure and stability of ecosystems. Here, we demonstrate how the behavioral response of an apex predator to changes in prey behavior and condition can dramatically alter the role and relative contribution of top-down forcing, depending on the spatial organization of ecosystem states. In 2014, a rapid and dramatic decline in the abundance of a mesopredator (Pycnopodia helianthoides) and primary producer (Macrocystis pyrifera) coincided with a fundamental change in purple sea urchin (Strongylocentrotus purpuratus) foraging behavior and condition, resulting in a spatial mosaic of kelp forests interspersed with patches of sea urchin barrens. We show that this mosaic of adjacent alternative ecosystem states led to an increase in the number of sea otters (Enhydra lutris nereis) specializing on urchin prey, a population-level increase in urchin consumption, and an increase in sea otter survivorship. We further show that the spatial distribution of sea otter foraging efforts for urchin prey was not directly linked to high prey density but rather was predicted by the distribution of energetically profitable prey. Therefore, we infer that spatially explicit sea otter foraging enhances the resistance of remnant forests to overgrazing but does not directly contribute to the resilience (recovery) of forests. These results highlight the role of consumer and predator trait-mediated responses to resource mosaics that are common throughout natural ecosystems and enhance understanding of reciprocal feedbacks between top-down and bottom-up forcing on the regional stability of ecosystems.

An initial comparative genomic autopsy of wasting disease in sea stars.

Beginning in 2013, sea stars throughout the Eastern North Pacific were decimated by wasting disease, also known as "asteroid idiopathic wasting syndrome" (AIWS) due to its elusive aetiology. The geographic extent and taxonomic scale of AIWS meant events leading up to the outbreak were heterogeneous, multifaceted, and oftentimes unobserved; progression from morbidity to death was rapid, leaving few tell-tale symptoms. Here, we take a forensic genomic approach to discover candidate genes that may help explain sea star wasting syndrome. We report the first genome and annotation for Pisaster ochraceus, along with differential gene expression (DGE) analyses in four size classes, three tissue types, and in symptomatic and asymptomatic individuals. We integrate nucleotide polymorphisms associated with survivors of the wasting disease outbreak, DGE associated with temperature treatments in P. ochraceus, and DGE associated with wasting in another asteroid Pycnopodia helianthoides. In P. ochraceus, we found DGE across all tissues, among size classes, and between asymptomatic and symptomatic individuals; the strongest wasting-associated DGE signal was in pyloric caecum. We also found previously identified outlier loci co-occur with differentially expressed genes. In cross-species comparisons of symptomatic and asymptomatic individuals, consistent responses distinguish genes associated with invertebrate innate immunity and chemical defence, consistent with context-dependent stress responses, defensive apoptosis, and tissue degradation. Our analyses thus highlight genomic constituents that may link suspected environmental drivers (elevated temperature) with intrinsic differences among individuals (age/size, alleles associated with susceptibility) that elicit organismal responses (e.g., coelomocyte proliferation) and manifest as sea star wasting mass mortality.

Trophic redundancy and predator size class structure drive differences in kelp forest ecosystem dynamics.

Ecosystems are changing at alarming rates because of climate change and a wide variety of other anthropogenic stressors. These stressors have the potential to cause phase shifts to less productive ecosystems. A major challenge for ecologists is to identify ecosystem attributes that enhance resilience and can buffer systems from shifts to less desirable alternative states. In this study, we used the Northern Channel Islands, California, as a model kelp forest ecosystem that had been perturbed from the loss of an important sea star predator due to a sea star wasting disease. To determine the mechanisms that prevent phase shifts from productive kelp forests to less productive urchin barrens, we compared pre‐ and postdisease predator assemblages as predictors of purple urchin densities. We found that prior to the onset of the disease outbreak, the sunflower sea star exerted strong predation pressures and was able to suppress purple urchin populations effectively. After the disease outbreak, which functionally extirpated the sunflower star, we found that the ecosystem response—urchin and algal abundances—depended on the abundance and/or size of remaining predator species. Inside Marine Protected Areas (MPAs), the large numbers and sizes of other urchin predators suppressed purple urchin populations resulting in kelp and understory algal growth. Outside of the MPAs, where these alternative urchin predators are fished, less abundant, and smaller, urchin populations grew dramatically in the absence of sunflower stars resulting in less kelp at these locations. Our results demonstrate that protected trophic redundancy inside MPAs creates a net of stability that could limit kelp forest ecosystem phase shifts to less desirable, alternative states when perturbed. This highlights the importance of harboring diversity and managing predator guilds.

Disease epidemic and a marine heat wave are associated with the continental-scale collapse of a pivotal predator (Pycnopodia helianthoides).

Multihost infectious disease outbreaks have endangered wildlife, causing extinction of frogs and endemic birds, and widespread declines of bats, corals, and abalone. Since 2013, a sea star wasting disease has affected >20 sea star species from Mexico to Alaska. The common, predatory sunflower star (Pycnopodia helianthoides), shown to be highly susceptible to sea star wasting disease, has been extirpated across most of its range. Diver surveys conducted in shallow nearshore waters (n = 10,956; 2006-2017) from California to Alaska and deep offshore (55 to 1280 m) trawl surveys from California to Washington (n = 8968; 2004-2016) reveal 80 to 100% declines across a ~3000-km range. Furthermore, timing of peak declines in nearshore waters coincided with anomalously warm sea surface temperatures. The rapid, widespread decline of this pivotal subtidal predator threatens its persistence and may have large ecosystem-level consequences.

The importance of kelp to an intertidal ecosystem varies by trophic level: insights from amino acid δ13C analysis

AbstractA fundamental question in ecology is understanding how energy and nutrients move through and between food webs, and which sources of production support consumers. In marine ecosystems, these basic questions have been challenging to answer given the limitation of observational methods. Stable isotope analysis of essential amino acids (EAA δ13C) has great potential as a tool to quantify energy and nutrient flow through marine food webs; however, it has been primarily utilized at large spatial scales. Here, we used EAA δ13C analysis to test for connectivity between adjacent subtidal and intertidal components of a nearshore ecosystem in south central Alaska. We measured δ13C of six EAA from four marine producer groups: subtidal kelp (Laminaria sp.), offshore particulate organic matter (POM), and intertidal red (Neorhodomela sp.) and green (Ulva sp.) algae. In addition, we sampled four intertidal invertebrate consumer species spanning a range of trophic/functional groups: Mytilus sp., Strongylocentrotus droebachiensis, Nucella sp., and Pycnopodia helianthoides. Using canonical analysis of principal coordinates (CAP) and isotope mixing models (MixSIAR), we tested for differences among producer EAA δ13C fingerprints and quantified the contribution of producer EAA to consumers. We compared these results to previously published EAA δ13C data on marine producers to examine the generality of this technique. We found the EAA δ13C fingerprints of subtidal kelps (Laminaria), Ulva, and Neorhodomela were highly distinct from one another. Further, our measured EAA δ13C patterns for kelp and red algae matched those previously reported from other localities, suggesting unique and universal EAA δ13C signatures for these groups. However, CAP could not distinguish between microalgae (POM) and Ulva, possibly due to similar biochemical pathways for the synthesis of EAA. Using these producer fingerprints, we found upper trophic‐level invertebrate consumers, Nucella and Pycnopodia, derived more than 60% of their essential amino acids from subtidal kelps. In contrast, the sampled primary consumers in the system, Mytilus and Strongylocentrotus, relied more heavily on Ulva and/or offshore POM. Our results provide evidence for connectivity between two adjacent nearshore ecosystems and exemplify EAA δ13C as a powerful new tool in tracing energy and nutrient flow within and among marine food webs.

Sudden collapse of a mesopredator reveals its complementary role in mediating rocky reef regime shifts.

While changes in the abundance of keystone predators can have cascading effects resulting in regime shifts, the role of mesopredators in these processes remains underexplored. We conducted annual surveys of rocky reef communities that varied in the recovery of a keystone predator (sea otter, Enhydra lutris) and the mass mortality of a mesopredator (sunflower sea star, Pycnopodia helianthoides) due to an infectious wasting disease. By fitting a population model to empirical data, we show that sea otters had the greatest impact on the mortality of large sea urchins, but that Pycnopodia decline corresponded to a 311% increase in medium urchins and a 30% decline in kelp densities. Our results reveal that predator complementarity in size-selective prey consumption strengthens top-down control on urchins, affecting the resilience of alternative reef states by reinforcing the resilience of kelp forests and eroding the resilience of urchin barrens. We reveal previously underappreciated species interactions within a 'classic' trophic cascade and regime shift, highlighting the critical role of middle-level predators in mediating rocky reef state transitions.

Investigating the Complex Association Between Viral Ecology, Environment, and Northeast Pacific Sea Star Wasting

Sea Star Wasting Disease (SSWD) describes a suite of disease signs that affected > 20 species of asteroid since 2013 along a broad geographic range from the Alaska Peninsula to Baja California. Previous work identified the Sea Star associated Densovirus (SSaDV) as the best candidate pathogen for SSWD in 3 species of common asteroid (Pycnopodia helianthoides, Pisaster ochraceus and Evasterias troscheli), and virus-sized material (<0.22 µm) elicited SSWD signs in P. helianthoides. However, the ability of virus-sized material to elicit SSWD in other species of asteroids was not known. Discordance between detection of SSaDV by qPCR and by viral metagenomics inspired the redesign of qPCR primers to encompass SSaDV and two densoviral genotypes detected in wasting asteroids. Analysis of asteroid samples collected during SSWD emergence in 2013-2014 showed an association between wasting asteroid-associated densoviruses (WAaDs) and SSWD in only one species (P. helianthoides). WAaDs were found in association with asymptomatic asteroids in contemporary (2016 and later) populations, suggesting that they form subclinical infections at the times they were sampled. WAaDs were found in SSWD-affected P. helianthoides after being absent in asymptomatic individuals a year earlier at one location (Kodiak). Direct challenge of P. ochraceus, Pisaster brevispinus and E. troscheli with virus-sized material from SSWD-affected individuals did not elicit SSWD in any trial. RNA viral genomes discovered in viral metagenomes and host transcriptomes had viral loads and metagenome fragment recruitment patterns that were inconsistent with SSWD. Analysis of water temperature and precipitation patterns on a regional scale suggests that SSWD occurred following dry conditions at several locations, but mostly was inconsistently associated with either parameter. Semi-continuous monitoring of SSWD subtidally at two sites in the Salish Sea from 2013-2017 indicated that SSWD in E. troscheli and P. ochraceus was associated with elevated water temperatures, but wasting in P. helianthoides occurred irrespective of environmental conditions. Our data therefore do not support that widespread SSWD in species other than P. helianthoides is associated with potential viral pathogens. Rather, we speculate that SSWD may represent a syndrome of heterogeneous etiologies between geographic locations, between species, or even within a species between locations.

A swath across the great divide: Kelp forests across the Samalga Pass biogeographic break

Biogeographic breaks are often described as locations where a large number of species reach their geographic range limits. Samalga Pass, in the eastern Aleutian Archipelago, is a known biogeographic break for the spatial distribution of several species of offshore-pelagic communities, including numerous species of cold-water corals, zooplankton, fish, marine mammals, and seabirds. However, it remains unclear whether Samalga Pass also serves as a biogeographic break for nearshore benthic communities. The occurrence of biogeographic breaks across multiple habitats has not often been described. In this study, we examined if the biogeographic break for offshore-pelagic communities applies to nearshore kelp forests. To examine whether Samalga Pass serves as a biogeographic break for kelp forest communities, this study compared abundance, biomass and percent bottom cover of species associated with kelp forests on either side of the pass. We observed marked differences in kelp forest community structure, with some species reaching their geographic range limits on the opposing sides of the pass. In particular, the habitat-forming kelp Nereocystis luetkeana, and the predatory sea stars Pycnopodia helianthoides and Orthasterias koehleri all occurred on the eastern side of Samalga Pass but were not observed west of the pass. In contrast, the sea star Leptasterias camtschatica dispar was observed only on the western side of the pass. We also observed differences in overall abundance and biomass of numerous associated fish, invertebrate and macroalgal species on opposing sides of the pass. We conclude that Samalga Pass is important biogeographic break for kelp forest communities in the Aleutian Archipelago and may demark the geographic range limits of several ecologically important species.

Warmer temperatures reduce the influence of an important keystone predator.

Predator-prey interactions may be strongly influenced by temperature variations in marine ecosystems. Consequently, climate change may alter the importance of predators with repercussions for ecosystem functioning and structure. In North-eastern Pacific kelp forests, the starfish Pycnopodia helianthoides is known to be an important predator of the purple sea urchin Strongylocentrotus purpuratus. Here we investigated the influence of water temperature on this predator-prey interaction by: (i) assessing the spatial distribution and temporal dynamics of both species across a temperature gradient in the northern Channel Islands, California, and (ii) investigating how the feeding rate of P.helianthoides on S.purpuratus is affected by temperature in laboratory tests. On average, at sites where mean annual temperatures were <14°C, P.helianthoides were common, S.purpuratus was rare and kelp was persistent, whereas where mean annual temperatures exceeded 14°C, P.helianthoides and kelp were rare and S.purpuratus abundant. Temperature was found to be the primary environmental factor influencing P.helianthoides abundance, and in turn P.helianthoides was the primary determinant of S.purpuratus abundance. In the laboratory, temperatures >16°C (equivalent to summer temperatures at sites where P.helianthoides were rare) reduced predation rates regardless of predator and prey sizes, although larger sea urchins were consumed only by large starfishes. These results clearly demonstrate that the effect of P.helianthoides on S.purpuratus is strongly mediated by temperature, and that the local abundance and predation rate of P.helianthoides on sea urchins will likely decrease with future warming. A reduction in top-down control on sea urchins, combined with other expected impacts of climate change on kelp, poses significant risks for the persistence of kelp forests in the future.

Indirect effects and prey behavior mediate interactions between an endangered prey and recovering predator

AbstractManaging for simultaneous recovery of interacting species, particularly top predators and their prey, is a longstanding challenge in applied ecology and conservation. The effects of sea otters (Enhydra lutris kenyoni) on abalone (Haliotis spp.) is a salient example along North America's west coast where sea otters are recovering from 18th‐ and 19th‐century fur trade while efforts are being made to recover abalone from more recent overfishing. To understand the direct and indirect effects of sea otters on northern abalone (H. kamtschatkana) and the relative influence of biotic and abiotic conditions, we surveyed subtidal rocky reef sites varying in otter occupation time in three regions of British Columbia, Canada. Sites occupied by sea otters for over 30 years had 16 times lower densities of exposed abalone than sites where otters have yet to recover (0.46 ± 0.08/20 m2 vs. 7.56 ± 0.98/20 m2), but they also had higher densities of cryptic abalone (2.17 ± 1.31/20 m2 vs. 1.31 ± 0.20/20 m2). Abalone densities were greater in deeper vs. shallower habitats at sites with sea otters compared to sites without otters. Sea otter effects on exposed abalone density were three times greater in magnitude than those of any other factor, whereas substrate and wave exposure effects on cryptic abalone were six times greater than those of sea otters. While higher substrate complexity may benefit abalone by providing refugia from sea otter predation, laboratory experiments revealed that it may also lead to higher capture efficiency by sunflower stars (Pycnopodia helianthoides), a ubiquitous mesopredator, compared to habitat with lower complexity. Sea otter recovery indirectly benefitted abalone by decreasing biomass of predatory sunflower stars and competitive grazing sea urchins, while increasing stipe density and depth of kelp that provides food and protective habitat. Importantly, abalone persisted in the face of sea otter recovery, albeit at lower densities of smaller and more cryptic individuals. We provide empirical evidence of how complex ecological interactions influence the effects of recovering predators on their recovering prey. This ecosystem‐based understanding can inform conservation trade‐offs when balancing multifaceted ecological, cultural, and socio‐economic objectives for species at risk.

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.

Up in Arms: Immune and Nervous System Response to Sea Star Wasting Disease.

Echinoderms, positioned taxonomically at the base of deuterostomes, provide an important system for the study of the evolution of the immune system. However, there is little known about the cellular components and genes associated with echinoderm immunity. The 2013–2014 sea star wasting disease outbreak is an emergent, rapidly spreading disease, which has led to large population declines of asteroids in the North American Pacific. While evidence suggests that the signs of this disease, twisting arms and lesions, may be attributed to a viral infection, the host response to infection is still poorly understood. In order to examine transcriptional responses of the sea star Pycnopodia helianthoides to sea star wasting disease, we injected a viral sized fraction (0.2 μm) homogenate prepared from symptomatic P. helianthoides into apparently healthy stars. Nine days following injection, when all stars were displaying signs of the disease, specimens were sacrificed and coelomocytes were extracted for RNA-seq analyses. A number of immune genes, including those involved in Toll signaling pathways, complement cascade, melanization response, and arachidonic acid metabolism, were differentially expressed. Furthermore, genes involved in nervous system processes and tissue remodeling were also differentially expressed, pointing to transcriptional changes underlying the signs of sea star wasting disease. The genomic resources presented here not only increase understanding of host response to sea star wasting disease, but also provide greater insight into the mechanisms underlying immune function in echinoderms.