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

Community Responses to Climate-Related Variability and Disease: The Critical Importance of Long-Term Research

A major goal of the Partnership for Interdisciplinary Studies of Coastal Oceans (PISCO) has been to understand the impacts of climate change and variability on the coastal ecosystems of the inner shelf of the California Current Large Marine System in particular, and other marine and even nonmarine systems more generally. Insights can result from determination of impacts of climatic perturbations such as the El Niño-Southern Oscillation, the North Pacific Gyre Oscillation, and the Pacific Decadal Oscillation, as well as impacts of climate-related surprises on populations, communities, and ecosystems. To gain insight into warming impacts at organismal levels, we also investigated mechanistic suborganismal (physiological, molecular) responses to thermal conditions. Warmer water was connected to changes in ecological subsidies, growth of dominant space occupiers (mussels and barnacles), and heightened physiological stress impacts. Fortuitously, PISCO researchers were ideally positioned to document ecosystem vulnerability and resilience to an unprecedented ecological surprise—coast-wide collapse of keystone predator (sea star) populations—and to investigate its consequences. As these examples suggest, long-term sampling is critically important for helping society anticipate and adapt to present and future disruptions caused by global change

SEX AND MICROHABITAT INFLUENCE THE ALLOCATION OF MYCOSPORINE-LIKE AMINO ACIDS TO TISSUES IN THE PURPLE SEA URCHIN, STRONGYLOCENTROTUS PURPURATUS

Field surveys of Strongylocentrotus purpuratus demonstrated that concentrations of natural sunscreens, mycosporine-like amino acids (MAAs), were higher in females than males for both gonadal and epidermal tissues, increased in ovaries as spawning season approached, and were influenced by the sea urchins’ microhabitat. Sea urchins occupying burrows, or “pits”, had lower concentrations of MAAs than those outside pits, suggesting a trade-off between physical and UV protection. Overall, UV irradiance did not influence MAA accumulation in gonadal tissues. However, males increased their allocation of MAAs to epidermal tissues in the microhabitat with the highest irradiance. Relative concentrations of individual MAAs were similar for epidermal tissues from both sexes and ovaries, providing broadband UVA/UVB absorbance, but testes contained principally one MAA, palythine. This is the first study to demonstrate that S. purpuratus and eight species of macroalgae in California have MAAs, and that the concentrations can be influenced by microhabitat

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

Data from: Prey state alters trait-mediated indirect interactions in rocky tide pools

Several studies on trait-mediated indirect interactions (TMIIs) have shown that predators can initiate trophic cascades by altering prey behaviour. Although it is well recognized that individual prey state alters antipredator and foraging behaviour, few studies explore whether this state-dependent prey behaviour can alter the strength of the ensuing tritrophic cascade. Here, we link state-dependent individual behaviour to community processes by experimentally testing whether hunger level and body size of prey altered antipredator behaviour and thus changed the strength of trophic cascades between predators and primary producers. In rocky intertidal tide pools on the California Coast, waterborne cues from the predatory seastar Leptasterias spp. (Stimpson) can cause the herbivorous snail Tegula (Chlorostoma) funebralis (A. Adams) to reduce grazing and flee tide pools, resulting in positive indirect effects on tide pool microalgae. However, we show that the strength of this behaviourally-mediated cascade may be contingent on prey hunger level and body size. During short field experiments at low tide, medium-sized snails that were either newly collected from the field or fed for 1 week in the laboratory mediated strong TMIIs because they grazed less when seastars were present. In contrast, no TMIIs occurred when medium-sized snails had been starved for 1 week because they continued grazing regardless of seastar presence. Newly collected small snails fled from seastars but did not mediate cascades because they ate little algae. Despite reaching an apparent size refuge from predation, many newly collected large snails fled from seastars, but those individuals that remained tended to graze the algae more quickly, resulting in unexpected negative indirect effects of seastars on algae cover. The implication of this pattern for the natural system is unclear. Because average hunger level and size of snails vary over time and space in nature, a mosaic of TMII strength may exist. Overall, the strength of tritrophic TMIIs in tide pools depended on individual prey state, supporting model predictions and adding to sparse empirical evidence. This outcome suggests that patterns occurring system-wide over the long term may be influenced by the state-dependent decisions made by the individuals present

A unified meta‐ecosystem dynamics model: Integrating herbivore‐plant subwebs with the intermittent upwelling hypothesis

Abstract 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

MorganTraitMediatedIndirect.pdf

Trait-mediated indirect interactions (TMIIs) are an important component of food web structure and dynamics. We determined whether TMIIs occur in rocky tidepool communities on the west coast of the USA. In the laboratory, both adults and juveniles of the keystone predator Pisaster ochraceus and adults of a smaller predatory seastar Leptasterias spp. caused the abundant herbivorous snail Tegula funebralis to stop foraging and flee the water, inducing a positive TMII on micro- and macroalgae. Snails preferred 3 common species of macroalgae (Ulva lactuca, Cladophora columbiana and Porphyra spp.) over 4 others, indicating that seastars might provide the strongest benefits to these species in tidepools. In the laboratory, snails responded rapidly to both species of predatory seastars and many more snails responded than could be eaten; thus, there is a potential for TMIIs to occur in natural populations. Snails responded to waterborne cues from P. ochraceus by reducing grazing and leaving still water, and reducing grazing in laminar flow (0.5 l min-1), resulting in TMII effects at least as far as 75 cm away. Adult P. ochraceus and Leptasterias spp. introduced to tidepools during low tide induced many snails to flee the tidepools. Considerable individual variation occurred in the responses of snails. Medium and large snails mediated TMIIs and hungry snails were marginally less responsive to seastars potentially altering TMII strength in nature. Thus, we demonstrated that TMIIs could occur in natural tidepools and showed how predator and algal identity, predator and prey size, water flow and prey hunger level may influence these TMIIs.Keywords: Rocky intertidal tidepools, Chemical cue Community structure, Predator-prey interaction, Nonconsumptive effect, Trait-mediated indirect interactio