Regime shifts in rocky intertidal communities associated with a marine heatwave and disease outbreak.

Long-term, large-scale experimental studies provide critical information about how global change influences communities. When environmental changes are severe, they can trigger abrupt transitions from one community type to another leading to a regime shift. From 2014 to 2016, rocky intertidal habitats in the northeast Pacific Ocean experienced extreme temperatures during a multi-year marine heatwave (MHW) and sharp population declines of the keystone predator Pisaster ochraceus due to sea star wasting disease (SSWD). Here we measured the community structure before, during and after the MHW onset and SSWD outbreak in a 15-year succession experiment conducted in a rocky intertidal meta-ecosystem spanning 13 sites on four capes in Oregon and northern California, United States. Kelp abundance declined during the MHW due to extreme temperatures, while gooseneck barnacle and mussel abundances increased due to reduced predation pressure after the loss of Pisaster from SSWD. Using several methods, we detected regime shifts from substrate- or algae-dominated to invertebrate-dominated alternative states at two capes. After water temperatures cooled and Pisaster population densities recovered, community structure differed from pre-disturbance conditions, suggesting low resilience. Consequently, thermal stress and predator loss can result in regime shifts that fundamentally alter community structure even after restoration of baseline conditions.

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.

Testing effects of bottom-up factors, grazing, and competition on New Zealand rocky intertidal algal communities.

Top-down and bottom-up factors and their interaction highlight the interdependence of resources and consumer impacts on food webs and ecosystems. Variation in the strength of upwelling-mediated ecological controls (i.e., light availability and herbivory) between early and late succession stages is less well understood from the standpoint of influencing algal functional group composition. We experimentally tested the effect of light, grazing, and disturbance on rocky intertidal turf-forming algal communities. Studies were conducted on the South Island of New Zealand at Raramai on the east coast (a persistent downwelling region) and Twelve Mile Beach on the west coast (an intermittent upwelling region). Herbivory, light availability, and algal cover were manipulated and percent cover of major macroalgal functional groups and sessile invertebrates were measured monthly from October 2017 to March 2018. By distinguishing between algal functional groups and including different starting conditions in our design, we found that the mosaic-like pattern of bare rock intermingled with diverse turf-forming algae at Twelve Mile Beach was driven by a complex array of species interactions, including grazing, predation, preemptive competition and interference competition, colonization rates, and these interactions were modulated by light availability and other environmental conditions. Raramai results contrasted with those at Twelve Mile Beach in showing stronger effects of grazing and relatively weak effects of other interactions, low colonization rates of invertebrates, and light effects limited to crustose algae. Our study highlights the potential importance of an upwelling-mediated 3-way interaction among herbivory, light availability, and preemption in structuring contrasting low rocky intertidal macroalgal communities.

Community theory: Testing environmental stress models.

Intensifying climate change and an increasing need for understanding its impacts on ecological communities places new emphasis on testing environmental stress models (ESMs). Using a prior literature search plus references from a more recent search, I evaluated empirical support for ESMs, focusing on whether consumer pressure on prey decreased (consumer stress model; CSM) or increased (prey stress model; PSM) with increasing environmental stress. Applying the criterion that testing ESMs requires conducting research at multiple sites along environmental stress gradients, the analysis found that CSMs were most frequent, with 'No Effect' and PSMs occurring at low but similar frequencies. This result contrasts to a prior survey in which 'No Effect' studies were most frequent, thus suggesting that consumers are generally more suppressed by stress than prey. Thus, increased climate change-induced environmental stress seems likely to reduce, not increase impacts of consumers on prey more often than the reverse.

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.

Biogeography of ocean acidification: Differential field performance of transplanted mussels to upwelling-driven variation in carbonate chemistry.

Ocean acidification (OA) represents a serious challenge to marine ecosystems. Laboratory studies addressing OA indicate broadly negative effects for marine organisms, particularly those relying on calcification processes. Growing evidence also suggests OA combined with other environmental stressors may be even more deleterious. Scaling these laboratory studies to ecological performance in the field, where environmental heterogeneity may mediate responses, is a critical next step toward understanding OA impacts on natural communities. We leveraged an upwelling-driven pH mosaic along the California Current System to deconstruct the relative influences of pH, ocean temperature, and food availability on seasonal growth, condition and shell thickness of the ecologically dominant intertidal mussel Mytilus californianus. In 2011 and 2012, ecological performance of adult mussels from local and commonly sourced populations was measured at 8 rocky intertidal sites between central Oregon and southern California. Sites coincided with a large-scale network of intertidal pH sensors, allowing comparisons among pH and other environmental stressors. Adult California mussel growth and size varied latitudinally among sites and inter-annually, and mean shell thickness index and shell weight growth were reduced with low pH. Surprisingly, shell length growth and the ratio of tissue to shell weight were enhanced, not diminished as expected, by low pH. In contrast, and as expected, shell weight growth and shell thickness were both diminished by low pH, consistent with the idea that OA exposure can compromise shell-dependent defenses against predators or wave forces. We also found that adult mussel shell weight growth and relative tissue mass were negatively associated with increased pH variability. Including local pH conditions with previously documented influences of ocean temperature, food availability, aerial exposure, and origin site enhanced the explanatory power of models describing observed performance differences. Responses of local mussel populations differed from those of a common source population suggesting mussel performance partially depended on genetic or persistent phenotypic differences. In light of prior research showing deleterious effects of low pH on larval mussels, our results suggest a life history transition leading to greater resilience in at least some performance metrics to ocean acidification by adult California mussels. Our data also demonstrate "hot" (more extreme) and "cold" (less extreme) spots in both mussel responses and environmental conditions, a pattern that may enable mitigation approaches in response to future changes in climate.

Remote sensing: generation of long-term kelp bed data sets for evaluation of impacts of climatic variation.

A critical tool in assessing ecosystem change is the analysis of long-term data sets, yet such information is generally sparse and often unavailable for many habitats. Kelp forests are an example of rapidly changing ecosystems that are in most cases data poor. Because kelp forests are highly dynamic and have high intrinsic interannual variability, understanding how regional-scale drivers are driving kelp populations-and particularly how kelp populations are responding to climate change-requires long-term data sets. However, much of the work on kelp responses to climate change has focused on just a few, relatively long-lived, perennial, canopy-forming species. To understand how kelp populations with different life history traits are responding to climate-related variability, we leverage 35 yr of Landsat satellite imagery to track the population size of an annual, ruderal kelp, Nereocystis luetkeana, across Oregon. We found high levels of interannual variability in Nereocystis canopy area and varying population trajectories over the last 35 yr. Surprisingly, Oregon Nereocystis population sizes were unresponsive to a 2014 marine heat wave accompanied by increases in urchin densities that decimated northern California Nereocystis populations. Some Oregon Nereocystis populations have even increased in area relative to pre-2014 levels. Analysis of environmental drivers found that Nereocystis population size was negatively correlated with estimated nitrate levels and positively correlated with winter wave height. This pattern is the inverse of the predicted relationship based on extensive prior work on the perennial kelp Macrocystis pyrifera and may be related to the annual life cycle of Nereocystis. This article demonstrates (1) the value of novel remote sensing tools to create long-term data sets that may challenge our understanding of nearshore marine species and (2) the need to incorporate life history traits into our theory of how climate change will shape the ocean of the future.

Regional processes are stronger determinants of rocky intertidal community dynamics than local biotic interactions.

Understanding the relative roles of species interactions and environmental factors in structuring communities has historically focused on local scales where manipulative experiments are possible. However, recent interest in predicting the effects of climate change and species invasions has spurred increasing attention to processes occurring at larger spatial and temporal scales. The "meta-ecosystem" approach is an ideal framework for integrating processes operating at multiple scales as it explicitly considers the influence of local biotic interactions and regional flows of energy, materials, and organisms on community structure. Using a comparative-experimental design, we asked (1) what is the relative importance of local biotic interactions and oceanic processes in determining rocky intertidal community structure in the low zone within the Northern California Current System, and (2) what factors are most important in regulating this structure and why? We focused on functional group interactions between macrophytes and sessile invertebrates and their consumers (grazers, predators), how these varied across spatial scales, and with ocean-driven conditions (upwelling, temperature) and ecological subsidies (nutrients, phytoplankton, sessile invertebrate recruits). Experiments were conducted at 13 sites divided across four capes in Oregon and northern California. Results showed that biotic interactions were variable in space and time but overall, sessile invertebrates had no effect on macrophytes while macrophytes had weakly negative effects on sessile invertebrates. Consumers, particularly predators, also had weakly negative effects on both functional groups. Overall, we found that 40-49% of the variance in community structure at the local scale was explained by external factors (e.g., spatial scale, time, upwelling, temperature, ecological subsidies) vs. 19-39% explained by functional group interactions. When individual functional group interaction strengths were used, only 2-3% of the variation was explained by any one functional group while 28-54% of the variation was explained by external factors. We conclude that community structure in the low intertidal zone is driven primarily by external factors at the regional scale with local biotic interactions playing a secondary role.

Generality in multispecies responses to ocean acidification revealed through multiple hypothesis testing.

Decades of research have demonstrated that many calcifying species are negatively affected by ocean acidification, a major anthropogenic threat in marine ecosystems. However, even closely related species may exhibit different responses to ocean acidification and less is known about the drivers that shape such variation in different species. Here, we examine the drivers of physiological performance under ocean acidification in a group of five species of turf-forming coralline algae. Specifically, quantitating the relative weight of evidence for each of ten hypotheses, we show that variation in coralline calcification and photosynthesis was best explained by allometric traits. Across ocean acidification conditions, larger individuals (measured as noncalcified mass) had higher net calcification and photosynthesis rates. Importantly, our approach was able to not only identify the aspect of size that drove the performance of coralline algae, but also determined that responses to ocean acidification were not dependent on species identity, evolutionary relatedness, habitat, shape, or structural composition. In fact, we found that failure to test multiple, alternative hypotheses would underestimate the generality of physiological performances, leading to the conclusion that each species had different baseline performance under ocean acidification. Testing among alternative hypotheses is an essential step toward determining the generalizability of experiments across taxa and identifying common drivers of species responses to global change.

Fundamental contradictions among observational and experimental estimates of non-trophic species interactions.

The difficulty of experimentally quantifying non-trophic species interactions has long troubled ecologists. Increasingly, a new application of the classic "checkerboard distribution" approach is used to infer interactions by examining the pairwise frequency at which species are found to spatially co-occur. However, the link between spatial associations, as estimated from observational co-occurrence, and species interactions has not been tested. Here we used nine common statistical methods to estimate associations from surveys of rocky intertidal communities in the Northeast Pacific Ocean. We compared those inferred associations with a new data set of experimentally determined net and direct species interactions. Although association methods generated networks with aggregate structure similar to previously published interaction networks, each method detected a different set of species associations from the same data set. Moreover, although association methods generally performed better than a random model, associations rarely matched empirical net or direct species interactions, with high rates of false positives and true positives, and many false negatives. Our findings cast doubt on studies that equate species co-occurrences to species interactions and highlight a persistent, unanswered question: how do we interpret spatial patterns in communities? We suggest future research directions to unify the observational and experimental study of species interactions, and discuss the need for community standards and best practices in association analysis.

Incorporating Context Dependency of Species Interactions in Species Distribution Models.

SYNOPSIS: Species distribution models typically use correlative approaches that characterize the species-environment relationship using occurrence or abundance data for a single species. However, species distributions are determined by both abiotic conditions and biotic interactions with other species in the community. Therefore, climate change is expected to impact species through direct effects on their physiology and indirect effects propagated through their resources, predators, competitors, or mutualists. Furthermore, the sign and strength of species interactions can change according to abiotic conditions, resulting in context-dependent species interactions that may change across space or with climate change. Here, we incorporated the context dependency of species interactions into a dynamic species distribution model. We developed a multi-species model that uses a time-series of observational survey data to evaluate how abiotic conditions and species interactions affect the dynamics of three rocky intertidal species. The model further distinguishes between the direct effects of abiotic conditions on abundance and the indirect effects propagated through interactions with other species. We apply the model to keystone predation by the sea star Pisaster ochraceus on the mussel Mytilus californianus and the barnacle Balanus glandula in the rocky intertidal zone of the Pacific coast, USA. Our method indicated that biotic interactions between P. ochraceus and B. glandula affected B. glandula dynamics across >1000 km of coastline. Consistent with patterns from keystone predation, the growth rate of B. glandula varied according to the abundance of P. ochraceus in the previous year. The data and the model did not indicate that the strength of keystone predation by P. ochraceus varied with a mean annual upwelling index. Balanus glandula cover increased following years with high phytoplankton abundance measured as mean annual chlorophyll-a. M. californianus exhibited the same pattern to a lesser degree, although this pattern was not significant. This work bridges the disciplines of biogeography and community ecology to develop tools to better understand the direct and indirect effects of abiotic conditions on ecological communities.

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.

Long-term declines in an intertidal foundation species parallel shifts in community composition.

The earth is in the midst of a biodiversity crisis, and projections indicate continuing and accelerating rates of global changes. Future alterations in communities and ecosystems may be precipitated by changes in the abundance of strongly interacting species, whose disappearance can lead to profound changes in abundance of other species, including an increase in extinction rate for some. Nearshore coastal communities are often dependent on the habitat and food resources provided by foundational plant (e.g., kelp) and animal (e.g., shellfish) species. We quantified changes in the abundance of the blue mussel (Mytilus edulis), a foundation species known to influence diversity and productivity of intertidal habitats, over the past 40 years in the Gulf of Maine, USA, one of the fastest warming regions in the global ocean. Using consistent survey methods, we compared contemporary population sizes to historical data from sites spanning >400 km. The results of these comparisons showed that blue mussels have declined in the Gulf of Maine by >60% (range: 29-100%) at the site level since the earliest benchmarks in the 1970s. At the same time as mussels declined, community composition shifted: at the four sites with historical community data, the sessile community became increasingly algal dominated. Contemporary (2013-2014) surveys across 20 sites showed that sessile species richness was positively correlated to mussel abundance in mid to high intertidal zones. These results suggest that declines in a critical foundation species may have already impacted the intertidal community. To inform future conservation efforts, we provide a database of historical and contemporary baselines of mussel population abundance and dynamics in the Gulf of Maine. Our results underscore the importance of anticipating not only changes in diversity but also changes in the abundance and identity of component species, as strong interactors like foundation species have the potential to drive cascading community shifts.

A keystone ecologist: Robert Treat Paine, 1933-2016.

Robert T. Paine, who passed away on 13 June 2016, is among the most influential people in the history of ecology. Paine was an experimentalist, a theoretician, a practitioner, and proponent of the "ecology of place," and a deep believer in the importance of natural history to ecological understanding. His scientific legacy grew from the discovery of a link between top-down forcing and species diversity, a breakthrough that led to the ideas of both keystone species and trophic cascades, and to our early understanding of the mosaic nature of biological communities, causes of zonation across physical gradients, and the intermediate-disturbance hypothesis of species diversity. Paine's influence as a mentor was equally important to the growth of ecological thinking, natural resource conservation, and policy. He served ecology as an Ecological Society of America president, an editor of the Society's journals, a member of and contributor to the National Academy of Sciences and the National Research Council, and an in-demand advisor to various state and federal agencies. Paine's broad interests, enthusiasm, charisma, and humor deeply affected our lives and the lives of so many others.

Long-term, high frequency in situ measurements of intertidal mussel bed temperatures using biomimetic sensors.

At a proximal level, the physiological impacts of global climate change on ectothermic organisms are manifest as changes in body temperatures. Especially for plants and animals exposed to direct solar radiation, body temperatures can be substantially different from air temperatures. We deployed biomimetic sensors that approximate the thermal characteristics of intertidal mussels at 71 sites worldwide, from 1998-present. Loggers recorded temperatures at 10-30 min intervals nearly continuously at multiple intertidal elevations. Comparisons against direct measurements of mussel tissue temperature indicated errors of ~2.0-2.5 °C, during daily fluctuations that often exceeded 15°-20 °C. Geographic patterns in thermal stress based on biomimetic logger measurements were generally far more complex than anticipated based only on 'habitat-level' measurements of air or sea surface temperature. This unique data set provides an opportunity to link physiological measurements with spatially- and temporally-explicit field observations of body temperature.

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.

Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability.

Although theory suggests geographic variation in species' performance is determined by multiple niche parameters, little consideration has been given to the spatial structure of interacting stressors that may shape local and regional vulnerability to global change. Here, we use spatially explicit mosaics of carbonate chemistry, food availability and temperature spanning 1280 km of coastline to test whether persistent, overlapping environmental mosaics mediate the growth and predation vulnerability of a critical foundation species, the mussel Mytilus californianus. We find growth was highest and predation vulnerability was lowest in dynamic environments with frequent exposure to low pH seawater and consistent food. In contrast, growth was lowest and predation vulnerability highest when exposure to low pH seawater was decoupled from high food availability, or in exceptionally warm locations. These results illustrate how interactions among multiple drivers can cause unexpected, yet persistent geographic mosaics of species performance, interactions and vulnerability to environmental change.

Are large macroalgal blooms necessarily bad? Nutrient impacts on seagrass in upwelling-influenced estuaries.

Knowledge of nutrient pathways and their resulting ecological interactions can alleviate numerous environmental problems associated with nutrient increases in both natural and managed systems. Although not unique, coastal systems are particularly prone to complex ecological interactions resulting from nutrient inputs from both the land and sea. Nutrient inputs to coastal systems often spur ulvoid macroalgal blooms, with negative consequences for seagrasses, primarily through shading, as well as through changes in local biogeochemistry. We conducted complementary field and mesocosm experiments in an upwelling-influenced estuary, where marine-derived nutrients dominate, to understand the direct and indirect effects of nutrients on the macroalgal-eelgrass (Zostera marina L.) interaction. In the field experiment, we found weak evidence that nutrients and/or macroalgal treatments had a negative effect on eelgrass. However, in the mesocosm experiment, we found that a combination of nutrient and macroalgal treatments led to strongly negative eelgrass responses, primarily via indirect effects associated with macroalgal additions. Together, increased total light attenuation and decreased sediment oxygen levels were associated with larger effects on eelgrass than shading alone, which was evaluated using mimic algae treatments that did not alter sediment redox potential. Nutrient addition in the mesocosms directly affected seagrass density; biomass, and morphology, but not as strongly as macroalgae. We hypothesize that the contrary results from these parallel experiments are a consequence of differences in the hydrodynamics between field and mesocosm settings. We suggest that the high rates of water movement and tidal submersion of our intertidal field experiments alleviated the light reduction and negative biogeochemical changes in the sediment associated with macroalgal canopies, as well as the nutrient effects observed in the mesocosm experiments. Furthermore, adaptation of ulvoids and eelgrass to high, but variable, background nutrient concentrations in upwelling-influenced estuaries may partly explain the venue-specific results reported here. In order to manage critical seagrass habitats, nutrient criteria and macroalgal indicators must consider variability in marine-based nutrient delivery and local physical conditions among estuaries.