Consequences of kelp forest ecosystem shifts and predictors of persistence through multiple stressors.

Ecological communities can be stable over multiple generations, or rapidly shift into structurally and functionally different configurations. In kelp forest ecosystems, overgrazing by sea urchins can abruptly shift forests into alternative states that are void of macroalgae and primarily dominated by actively grazing sea urchins. Beginning in 2014, a sea urchin outbreak along the central coast of California resulted in a patchy mosaic of remnant forests interspersed with sea urchin barrens. In this study, we used a 14-year subtidal monitoring dataset of invertebrates, algae, and fishes to explore changes in community structure associated with the loss of forests. We found that the spatial mosaic of barrens and forests resulted in a region-wide shift in community structure. However, the magnitude of kelp forest loss and taxonomic-level consequences were spatially heterogeneous. Taxonomic diversity declined across the region, but there were no declines in richness for any group, suggesting compositional redistribution. Baseline ecological and environmental conditions, and sea urchin behaviour, explained the persistence of forests through multiple stressors. These results indicate that spatial heterogeneity in preexisting ecological and environmental conditions can explain patterns of community change.

A marine protected area network does not confer community structure resilience to a marine heatwave across coastal ecosystems.

Marine protected areas (MPAs) have gained attention as a conservation tool for enhancing ecosystem resilience to climate change. However, empirical evidence explicitly linking MPAs to enhanced ecological resilience is limited and mixed. To better understand whether MPAs can buffer climate impacts, we tested the resistance and recovery of marine communities to the 2014-2016 Northeast Pacific heatwave in the largest scientifically designed MPA network in the world off the coast of California, United States. The network consists of 124 MPAs (48 no-take state marine reserves, and 76 partial-take or special regulation conservation areas) implemented at different times, with full implementation completed in 2012. We compared fish, benthic invertebrate, and macroalgal community structure inside and outside of 13 no-take MPAs across rocky intertidal, kelp forest, shallow reef, and deep reef nearshore habitats in California's Central Coast region from 2007 to 2020. We also explored whether MPA features, including age, size, depth, proportion rock, historic fishing pressure, habitat diversity and richness, connectivity, and fish biomass response ratios (proxy for ecological performance), conferred climate resilience for kelp forest and rocky intertidal habitats spanning 28 MPAs across the full network. Ecological communities dramatically shifted due to the marine heatwave across all four nearshore habitats, and MPAs did not facilitate habitat-wide resistance or recovery. Only in protected rocky intertidal habitats did community structure significantly resist marine heatwave impacts. Community shifts were associated with a pronounced decline in the relative proportion of cold water species and an increase in warm water species. MPA features did not explain resistance or recovery to the marine heatwave. Collectively, our findings suggest that MPAs have limited ability to mitigate the impacts of marine heatwaves on community structure. Given that mechanisms of resilience to climate perturbations are complex, there is a clear need to expand assessments of ecosystem-wide consequences resulting from acute climate-driven perturbations, and the potential role of regulatory protection in mitigating community structure changes.

Dispersal of a nearshore marine fish connects marine reserves and adjacent fished areas along an open coast.

Marine species with pelagic larvae typically exhibit little population structure, suggesting long-distance dispersal and high gene flow. Directly quantifying dispersal of marine fishes is challenging but important, particularly for the design of marine protected areas (MPAs). Here, we studied kelp rockfish (Sebastes atrovirens) sampled along ~25 km of coastline in a boundary current-dominated ecosystem and used genetic parentage analysis to identify dispersal events and characterize them, because the distance between sedentary parents and their settled offspring is the lifetime dispersal distance. Large sample sizes and intensive sampling are critical for increasing the likelihood of detecting parent-offspring matches in such systems and we sampled more than 6,000 kelp rockfish and analysed them with a powerful set of 96 microhaplotype markers. We identified eight parent-offspring pairs with high confidence, including two juvenile fish that were born inside MPAs and dispersed to areas outside MPAs, and four fish born in MPAs that dispersed to nearby MPAs. Additionally, we identified 25 full-sibling pairs, which occurred throughout the sampling area and included all possible combinations of inferred dispersal trajectories. Intriguingly, these included two pairs of young-of-the-year siblings with one member each sampled in consecutive years. These sibling pairs suggest monogamy, either intentional or accidental, which has not been previously demonstrated in rockfishes. This study provides the first direct observation of larval dispersal events in a current-dominated ecosystem and direct evidence that larvae produced within MPAs are exported both to neighbouring MPAs and to proximate areas where harvest is allowed.

Global patterns of kelp forest change over the past half-century.

Kelp forests (Order Laminariales) form key biogenic habitats in coastal regions of temperate and Arctic seas worldwide, providing ecosystem services valued in the range of billions of dollars annually. Although local evidence suggests that kelp forests are increasingly threatened by a variety of stressors, no comprehensive global analysis of change in kelp abundances currently exists. Here, we build and analyze a global database of kelp time series spanning the past half-century to assess regional and global trends in kelp abundances. We detected a high degree of geographic variation in trends, with regional variability in the direction and magnitude of change far exceeding a small global average decline (instantaneous rate of change = -0.018 y-1). Our analysis identified declines in 38% of ecoregions for which there are data (-0.015 to -0.18 y-1), increases in 27% of ecoregions (0.015 to 0.11 y-1), and no detectable change in 35% of ecoregions. These spatially variable trajectories reflected regional differences in the drivers of change, uncertainty in some regions owing to poor spatial and temporal data coverage, and the dynamic nature of kelp populations. We conclude that although global drivers could be affecting kelp forests at multiple scales, local stressors and regional variation in the effects of these drivers dominate kelp dynamics, in contrast to many other marine and terrestrial foundation species.

Fitting state-space integral projection models to size-structured time series data to estimate unknown parameters.

Integral projection models (IPMs) have a number of advantages over matrix-model approaches for analyzing size-structured population dynamics, because the latter require parameter estimates for each age or stage transition. However, IPMs still require appropriate data. Typically they are parameterized using individual-scale relationships between body size and demographic rates, but these are not always available. We present an alternative approach for estimating demographic parameters from time series of size-structured survey data using a Bayesian state-space IPM (SSIPM). By fitting an IPM in a state-space framework, we estimate unknown parameters and explicitly account for process and measurement error in a dataset to estimate the underlying process model dynamics. We tested our method by fitting SSIPMs to simulated data; the model fit the simulated size distributions well and estimated unknown demographic parameters accurately. We then illustrated our method using nine years of annual surveys of the density and size distribution of two fish species (blue rockfish, Sebastes mystinus, and gopher rockfish, S. carnatus) at seven kelp forest sites in California. The SSIPM produced reasonable fits to the data, and estimated fishing rates for both species that were higher than our Bayesian prior estimates based on coast-wide stock assessment estimates of harvest. That improvement reinforces the value of being able to estimate demographic parameters from local-scale monitoring data. We highlight a number of key decision points in SSIPM development (e.g., open vs. closed demography, number of particles in the state-space filter) so that users can apply the method to their own datasets.

Marine protected area networks in California, USA.

California responded to concerns about overfishing in the 1990s by implementing a network of marine protected areas (MPAs) through two science-based decision-making processes. The first process focused on the Channel Islands, and the second addressed California's entire coastline, pursuant to the state's Marine Life Protection Act (MLPA). We review the interaction between science and policy in both processes, and lessons learned. For the Channel Islands, scientists controversially recommended setting aside 30-50% of coastline to protect marine ecosystems. For the MLPA, MPAs were intended to be ecologically connected in a network, so design guidelines included minimum size and maximum spacing of MPAs (based roughly on fish movement rates), an approach that also implicitly specified a minimum fraction of the coastline to be protected. As MPA science developed during the California processes, spatial population models were constructed to quantify how MPAs were affected by adult fish movement and larval dispersal, i.e., how population persistence within MPA networks depended on fishing outside the MPAs, and how fishery yields could either increase or decrease with MPA implementation, depending on fishery management. These newer quantitative methods added to, but did not supplant, the initial rule-of-thumb guidelines. In the future, similar spatial population models will allow more comprehensive evaluation of the integrated effects of MPAs and conventional fisheries management. By 2011, California had implemented 132 MPAs covering more than 15% of its coastline, and now stands on the threshold of the most challenging step in this effort: monitoring and adaptive management to ensure ecosystem sustainability.

Incorporating biogeography into evaluations of the Channel Islands marine reserve network.

Networks of marine reserves are increasingly a major component of many ecosystem-based management plans designed to conserve biodiversity, protect the structure and function of ecosystems, and rebuild and sustain fisheries. There is a growing need for scientific guidance in the design of network-wide monitoring programs to evaluate the efficacy of reserves at meeting their conservation and management goals. Here, we present an evaluation of the Channel Islands reserve network, which was established in 2003 off the coast of southern California. This reserve network spans a major environmental and biogeographic gradient, making it a challenge to assess network-wide responses of many species. Using fish community structure data from a long-term, large-scale monitoring program, we first identified persistent geographic patterns of community structure and the scale at which sites should be grouped for analysis. Fish communities differed most among islands with densities of individual species varying from 3- to 250-fold. Habitat structure differed among islands but not based on reserve status. Across the network, we found that, after 5 years, species targeted by fishing had higher densities (1.5×) and biomass (1.8×) inside reserves, whereas nontargeted species showed no significant differences. Examining trophic groups, piscivore and carnivore biomass was significantly greater inside reserves (1.8× and 1.3× more, respectively), whereas the biomass of planktivores and herbivores was similar inside and out. A framework for incorporating biogeographic variation into reserve network assessments is critical as we move from the evaluation of single reserves to networks of reserves.

Designing marine reserve networks for both conservation and fisheries management.

Marine protected areas (MPAs) that exclude fishing have been shown repeatedly to enhance the abundance, size, and diversity of species. These benefits, however, mean little to most marine species, because individual protected areas typically are small. To meet the larger-scale conservation challenges facing ocean ecosystems, several nations are expanding the benefits of individual protected areas by building networks of protected areas. Doing so successfully requires a detailed understanding of the ecological and physical characteristics of ocean ecosystems and the responses of humans to spatial closures. There has been enormous scientific interest in these topics, and frameworks for the design of MPA networks for meeting conservation and fishery management goals are emerging. Persistent in the literature is the perception of an inherent tradeoff between achieving conservation and fishery goals. Through a synthetic analysis across these conservation and bioeconomic studies, we construct guidelines for MPA network design that reduce or eliminate this tradeoff. We present size, spacing, location, and configuration guidelines for designing networks that simultaneously can enhance biological conservation and reduce fishery costs or even increase fishery yields and profits. Indeed, in some settings, a well-designed MPA network is critical to the optimal harvest strategy. When reserves benefit fisheries, the optimal area in reserves is moderately large (mode ≈30%). Assessing network design principals is limited currently by the absence of empirical data from large-scale networks. Emerging networks will soon rectify this constraint.

Multistressor global change drivers reduce hatch and viability of Lingcod embryos, a benthic egg layer in the California Current System.

Early life history stages of marine fishes are often more susceptible to environmental stressors than adult stages. This vulnerability is likely exacerbated for species that lay benthic egg masses bound to substrate because the embryos cannot evade locally unfavorable environmental conditions. Lingcod (Ophiodon elongatus), a benthic egg layer, is an ecologically and economically significant predator in the highly-productive California Current System (CCS). We ran a flow-through mesocosm experiment that exposed Lingcod eggs collected from Monterey Bay, CA to conditions we expect to see in the central CCS by the year 2050 and 2100. Exposure to temperature, pH, and dissolved oxygen concentrations projected by the year 2050 halved the successful hatch of Lingcod embryos and significantly reduced the size of day-1 larvae. In the year 2100 treatment, viable hatch plummeted (3% of normal), larvae were undersized (83% of normal), yolk reserves were exhausted (38% of normal), and deformities were widespread (94% of individuals). This experiment is the first to expose marine benthic eggs to future temperature, pH, and dissolved oxygen conditions in concert. Lingcod are a potential indicator species for other benthic egg layers for which global change conditions may significantly diminish recruitment rates.

Large-scale, multidecade monitoring data from kelp forest ecosystems in California and Oregon (USA).

Kelp forests are among the most productive ecosystems on Earth. In combination with their close proximity to the shore, the productivity and biodiversity of these ecosystems generate a wide range of ecosystem services including supporting (e.g., primary production, habitat), regulating (e.g., water flow, coastal erosion), provisioning (e.g., commercial and recreational fisheries), and cultural (e.g., recreational, artisanal) services. For these reasons, kelp forests have long been the target of ecological studies. However, with few exceptions, these studies have been localized and short term (<5 years). In 1999, recognizing the importance of large-scale, long-term studies for understanding the structure, functioning, and dynamics of coastal marine ecosystems, and for informing policy, the Partnership for Interdisciplinary Studies of Coastal Oceans (PISCO) designed and initiated a large-scale, long-term monitoring study of kelp forest ecosystems along 1400 km of coast stretching from southern California to southern Oregon, USA. The purpose of the study has been to characterize the spatial and temporal patterns of kelp forest ecosystem structure and evaluate the relative contributions of biological and environmental variables derived from external sources (e.g., sea otter density, Chl-a concentration, sea surface temperature, wave energy) in explaining observed spatial and temporal patterns. For this purpose, the ecological community (i.e., density, percent cover, or biomass of conspicuous fishes, invertebrates, and macroalgae) and geomorphological attributes (bottom depth, substratum type, and vertical relief) of kelp forest ecosystems have been surveyed annually using SCUBA divers trained in both scientific diving and data collection techniques and the identification of kelp forest species. The study region spans distinct ecological and biogeographic provinces, which enables investigations of how variation in environmental drivers and distinctive species compositions influence community structure, and its response to climate-related environmental change across a portion of the California Current Large Marine Ecosystem. These data have been used to inform fisheries management, design and evaluate California's state-wide network of marine protected areas (MPAs), and assess the ecological consequences of climate change (e.g., marine heatwaves). Over time, the spatial and temporal design of the monitoring program was adapted to fill its role in evaluating the ecological responses to the establishment of MPAs. There are no copyright restrictions; please cite this paper when data are used.

Wave disturbance overwhelms top-down and bottom-up control of primary production in California kelp forests.

We took advantage of regional differences in environmental forcing and consumer abundance to examine the relative importance of nutrient availability (bottom-up), grazing pressure (top-down), and storm waves (disturbance) in determining the standing biomass and net primary production (NPP) of the giant kelp Macrocystis pyrifera in central and southern California. Using a nine-year data set collected from 17 sites we show that, despite high densities of sea urchin grazers and prolonged periods of low nutrient availability in southern California, NPP by giant kelp was twice that of central California where nutrient concentrations were consistently high and sea urchins were nearly absent due to predation by sea otters. Waves associated with winter storms were consistently higher in central California, and the loss of kelp biomass to winter wave disturbance was on average twice that of southern California. These observations suggest that the more intense wave disturbance in central California limited NPP by giant kelp under otherwise favorable conditions. Regional patterns of interannual variation in NPP were similar to those of wave disturbance in that year-to-year variation in disturbance and NPP were both greater in southern California. Our findings provide strong evidence that regional differences in wave disturbance overwhelmed those of nutrient supply and grazing intensity to determine NPP by giant kelp. The important role of disturbance in controlling NPP revealed by our study is likely not unique to giant kelp forests, as vegetation dynamics in many systems are dominated by post-disturbance succession with climax communities being relatively uncommon. The effects of disturbance frequency may be easier to detect in giant kelp because it is fast growing and relatively short lived, with cycles of disturbance and recovery occurring on time scales of years. Much longer data sets (decades to centuries) will likely be needed to properly evaluate the role of disturbance relative to other processes in determining patterns of NPP in other systems.

Large-scale shift in the structure of a kelp forest ecosystem co-occurs with an epizootic and marine heatwave.

Climate change is responsible for increased frequency, intensity, and duration of extreme events, such as marine heatwaves (MHWs). Within eastern boundary current systems, MHWs have profound impacts on temperature-nutrient dynamics that drive primary productivity. Bull kelp (Nereocystis luetkeana) forests, a vital nearshore habitat, experienced unprecedented losses along 350 km of coastline in northern California beginning in 2014 and continuing through 2019. These losses have had devastating consequences to northern California communities, economies, and fisheries. Using a suite of in situ and satellite-derived data, we demonstrate that the abrupt ecosystem shift initiated by a multi-year MHW was preceded by declines in keystone predator population densities. We show strong evidence that northern California kelp forests, while temporally dynamic, were historically resilient to fluctuating environmental conditions, even in the absence of key top predators, but that a series of coupled environmental and biological shifts between 2014 and 2016 resulted in the formation of a persistent, altered ecosystem state with low primary productivity. Based on our findings, we recommend the implementation of ecosystem-based and adaptive management strategies, such as (1) monitoring the status of key ecosystem attributes: kelp distribution and abundance, and densities of sea urchins and their predators, (2) developing management responses to threshold levels of these attributes, and (3) creating quantitative restoration suitability indices for informing kelp restoration efforts.

An ecological framework for informing permitting decisions on scientific activities in protected areas.

There are numerous reasons to conduct scientific research within protected areas, but research activities may also negatively impact organisms and habitats, and thus conflict with a protected area's conservation goals. We developed a quantitative ecological decision-support framework that estimates these potential impacts so managers can weigh costs and benefits of proposed research projects and make informed permitting decisions. The framework generates quantitative estimates of the ecological impacts of the project and the cumulative impacts of the proposed project and all other projects in the protected area, and then compares the estimated cumulative impacts of all projects with policy-based acceptable impact thresholds. We use a series of simplified equations (models) to assess the impacts of proposed research to: a) the population of any targeted species, b) the major ecological assemblages that make up the community, and c) the physical habitat that supports protected area biota. These models consider both targeted and incidental impacts to the ecosystem and include consideration of the vulnerability of targeted species, assemblages, and habitats, based on their recovery time and ecological role. We parameterized the models for a wide variety of potential research activities that regularly occur in the study area using a combination of literature review and expert judgment with a precautionary approach to uncertainty. We also conducted sensitivity analyses to examine the relationships between model input parameters and estimated impacts to understand the dominant drivers of the ecological impact estimates. Although the decision-support framework was designed for and adopted by the California Department of Fish and Wildlife for permitting scientific studies in the state-wide network of marine protected areas (MPAs), the framework can readily be adapted for terrestrial and freshwater protected areas.

Managing small-scale commercial fisheries for adaptive capacity: insights from dynamic social-ecological drivers of change in Monterey Bay.

Globally, small-scale fisheries are influenced by dynamic climate, governance, and market drivers, which present social and ecological challenges and opportunities. It is difficult to manage fisheries adaptively for fluctuating drivers, except to allow participants to shift effort among multiple fisheries. Adapting to changing conditions allows small-scale fishery participants to survive economic and environmental disturbances and benefit from optimal conditions. This study explores the relative influence of large-scale drivers on shifts in effort and outcomes among three closely linked fisheries in Monterey Bay since the Magnuson-Stevens Fisheries Conservation and Management Act of 1976. In this region, Pacific sardine (Sardinops sagax), northern anchovy (Engraulis mordax), and market squid (Loligo opalescens) fisheries comprise a tightly linked system where shifting focus among fisheries is a key element to adaptive capacity and reduced social and ecological vulnerability. Using a cluster analysis of landings, we identify four modes from 1974 to 2012 that are dominated (i.e., a given species accounting for the plurality of landings) by squid, sardine, anchovy, or lack any dominance, and seven points of transition among these periods. This approach enables us to determine which drivers are associated with each mode and each transition. Overall, we show that market and climate drivers are predominantly attributed to dominance transitions. Model selection of external drivers indicates that governance phases, reflected as perceived abundance, dictate long-term outcomes. Our findings suggest that globally, small-scale fishery managers should consider enabling shifts in effort among fisheries and retaining existing flexibility, as adaptive capacity is a critical determinant for social and ecological resilience.

An online database for informing ecological network models: http://kelpforest.ucsc.edu.

Ecological network models and analyses are recognized as valuable tools for understanding the dynamics and resiliency of ecosystems, and for informing ecosystem-based approaches to management. However, few databases exist that can provide the life history, demographic and species interaction information necessary to parameterize ecological network models. Faced with the difficulty of synthesizing the information required to construct models for kelp forest ecosystems along the West Coast of North America, we developed an online database (http://kelpforest.ucsc.edu/) to facilitate the collation and dissemination of such information. Many of the database's attributes are novel yet the structure is applicable and adaptable to other ecosystem modeling efforts. Information for each taxonomic unit includes stage-specific life history, demography, and body-size allometries. Species interactions include trophic, competitive, facilitative, and parasitic forms. Each data entry is temporally and spatially explicit. The online data entry interface allows researchers anywhere to contribute and access information. Quality control is facilitated by attributing each entry to unique contributor identities and source citations. The database has proven useful as an archive of species and ecosystem-specific information in the development of several ecological network models, for informing management actions, and for education purposes (e.g., undergraduate and graduate training). To facilitate adaptation of the database by other researches for other ecosystems, the code and technical details on how to customize this database and apply it to other ecosystems are freely available and located at the following link (https://github.com/kelpforest-cameo/databaseui).

Marine protected area networks: assessing whether the whole is greater than the sum of its parts.

Anthropogenic impacts are increasingly affecting the world's oceans. Networks of marine protected areas (MPAs) provide an option for increasing the ecological and economic benefits often provided by single MPAs. It is vital to empirically assess the effects of MPA networks and to prioritize the monitoring data necessary to explain those effects. We summarize the types of MPA networks based on their intended management outcomes and illustrate a framework for evaluating whether a connectivity network is providing an outcome greater than the sum of individual MPA effects. We use an analysis of an MPA network in Hawai'i to compare networked MPAs to non-networked MPAs to demonstrate results consistent with a network effect. We assert that planning processes for MPA networks should identify their intended outcomes while also employing coupled field monitoring-simulation modeling approaches, a powerful way to prioritize the most relevant monitoring data for empirically assessing MPA network performance.

Biodiversity, population regulation, and the stability of coral-reef fish communities.

Unprecedented population declines and extinctions because of human activities, combined with a growing recognition that such losses affect the stability of ecosystems, underscore the need to better understand how populations persist naturally. We provide field experimental evidence that high biodiversity-in particular, the combined effects of predators and competitors-acts in a way that regulates the size of local fish populations within their coral-reef community. These results indicate that complex interactions among multiple species are necessary for the stability of a highly diverse community, and so forewarn that overexploiting such species may have cascading negative consequences for the entire system.