Spatial covariation in nutrient enrichment and fishing of herbivores in an oceanic coral reef ecosystem.

Both natural and anthropogenic stressors are increasing on coral reefs, resulting in large-scale loss of coral and potential shifts from coral- to macroalgae-dominated community states. Two factors implicated in shifts to macroalgae are nutrient enrichment and fishing of reef herbivores. Although either of these factors alone could facilitate establishment of macroalgae, reefs may be particularly vulnerable to coral-to-algae phase shifts in which strong bottom-up forcing from nutrient enrichment is accompanied by a weakening of herbivore control of macroalgae via intense fishing. We explored spatial heterogeneity and covariance in these drivers on reefs in the lagoons of Moorea, French Polynesia, where the local fishery heavily targets herbivorous fishes and there are spatially variable inputs of nutrients from agricultural fertilizers and wastewater systems. Spatial patterns of fishing and nutrient enrichment were not correlated at the two landscape scales we examined: among the 11 interconnected lagoons around the island or among major habitats (fringing reef, mid-lagoon, back reef) within a lagoon. This decoupling at the landscape scale resulted from patterns of covariation between enrichment and fishing that differed qualitatively between cross-shore and long-shore directions. At the cross-shore scale, nutrient enrichment declined but fishing increased from shore to the crest of the barrier reef. By contrast, nutrient enrichment and fishing were positively correlated in the long-shore direction, with both increasing with proximity to a pass in the barrier reef. Contrary to widespread assumptions in the scientific literature that human coastal population density correlates with impact on marine ecosystems and that fishing effort declines linearly with distance from the shore, these local stressors produced a complex spatial mosaic of reef vulnerabilities. Our findings support spatially explicit management involving the control of anthropogenic nutrients and strategic reductions in fishing pressure on herbivores by highlighting specific areas to target for management actions.

Improving the ability of a BACI design to detect impacts within a kelp-forest community.

Distinguishing between human impacts and natural variation in abundance remains difficult because most species exhibit complex patterns of variation in space and time. When ecological monitoring data are available, a before-after-control-impact (BACI) analysis can control natural spatial and temporal variation to better identify an impact and estimate its magnitude. However, populations with limited distributions and confounding spatial-temporal dynamics can violate core assumptions of BACI-type designs. In this study, we assessed how such properties affect the potential to identify impacts. Specifically, we quantified the conditions under which BACI analyses correctly (or incorrectly) identified simulated anthropogenic impacts in a spatially and temporally replicated data set of fish, macroalgal, and invertebrate species found on nearshore subtidal reefs in southern California, USA. We found BACI failed to assess very localized impacts, and had low power but high precision when assessing region-wide impacts. Power was highest for severe impacts of moderate spatial scale, and impacts were most easily detected in species with stable, widely distributed populations. Serial autocorrelation in the data greatly inflated false impact detection rates, and could be partly controlled for statistically, while spatial synchrony in dynamics had no consistent effect on power or false detection rates. Unfortunately, species that offer high power to detect real impacts were also more likely to detect impacts where none had occurred. However, considering power and false detection rates together can identify promising indicator species, and collectively analyzing data for similar species improved the net ability to assess impacts. These insights set expectations for the sizes and severities of impacts that BACI analyses can detect in real systems, point to the importance of serial autocorrelation (but not of spatial synchrony), and indicate how to choose the species, and groups of species, that can best identify impacts.

Caribbean reefs of the Anthropocene: Variance in ecosystem metrics indicates bright spots on coral depauperate reefs.

Dramatic coral loss has significantly altered many Caribbean reefs, with potentially important consequences for the ecological functions and ecosystem services provided by reef systems. Many studies examine coral loss and its causes-and often presume a universal decline of ecosystem services with coral loss-rather than evaluating the range of possible outcomes for a diversity of ecosystem functions and services at reefs varying in coral cover. We evaluate 10 key ecosystem metrics, relating to a variety of different reef ecosystem functions and services, on 328 Caribbean reefs varying in coral cover. We focus on the range and variability of these metrics rather than on mean responses. In contrast to a prevailing paradigm, we document high variability for a variety of metrics, and for many the range of outcomes is not related to coral cover. We find numerous "bright spots," where herbivorous fish biomass, density of large fishes, fishery value, and/or fish species richness are high, despite low coral cover. Although it remains critical to protect and restore corals, understanding variability in ecosystem metrics among low-coral reefs can facilitate the maintenance of reefs with sustained functions and services as we work to restore degraded systems. This framework can be applied to other ecosystems in the Anthropocene to better understand variance in ecosystem service outcomes and identify where and why bright spots exist.

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.

Giant kelp, Macrocystis pyrifera, increases faunal diversity through physical engineering.

Foundation species define the ecosystems they live in, but ecologists have often characterized dominant plants as foundational without supporting evidence. Giant kelp has long been considered a marine foundation species due to its complex structure and high productivity; however, there is little quantitative evidence to evaluate this. Here, we apply structural equation modelling to a 15-year time series of reef community data to evaluate how giant kelp affects the reef community. Although species richness was positively associated with giant kelp biomass, most direct paths did not involve giant kelp. Instead, the foundational qualities of giant kelp were driven mostly by indirect effects attributed to its dominant physical structure and associated engineering influence on the ecosystem, rather than by its use as food by invertebrates and fishes. Giant kelp structure has indirect effects because it shades out understorey algae that compete with sessile invertebrates. When released from competition, sessile species in turn increase the diversity of mobile predators. Sea urchin grazing effects could have been misinterpreted as kelp effects, because sea urchins can overgraze giant kelp, understorey algae and sessile invertebrates alike. Our results confirm the high diversity and biomass associated with kelp forests, but highlight how species interactions and habitat attributes can be misconstrued as direct consequences of a foundation species like giant kelp.

Improved estimates of net primary production, growth, and standing crop of Macrocystis pyrifera in Southern California.

The giant kelp Macrocystis pyrifera forms subtidal forests on shallow reefs in temperate regions of the world. It is one of the fastest-growing multicellular autotrophs on Earth and its high productivity supports diverse marine food webs. In 2008, we published a method for estimating biomass and net primary production (NPP) of giant kelp along with five years of data, to provide a more integrated measure of NPP than those yielded by previous methods. Our method combines monthly field measurements of standing crop and loss rates with a model of kelp biomass dynamics to estimate instantaneous mass-specific growth rates and NPP for each season of each year. We have since improved our approach to account for several previously unresolved sources of biomass loss. These improvements have led to a near doubling of our prior estimates of growth and NPP. At our site with the most persistent stand of giant kelp, NPP averages ~5.2 kg dry mass·m-2 ·yr-1 and results from the rapid growth (~3.5% per d) of a relatively small standing biomass (~0.4 kg dry mass/m2 on average) that turns over ~12 times annually. Here we provide revised estimates of seasonal biomass, growth, and NPP for the five years covered by our previous publication (2002-2006), along with more than a decade of additional data (2007-2017). We also present updated relationships for predicting giant kelp biomass and NPP from much more easily obtained measurements of frond density. These data can be used to understand the mechanisms that drive variation in giant kelp NPP at a wide range of temporal scales. No copyright or proprietary restrictions are associated with the use of this data set other than citation of this Data Paper.

Scale-specific drivers of kelp forest communities.

Identifying spatial scales of variation in natural communities and the processes driving them is critical for obtaining a predictive understanding of biodiversity. In this study, we focused on diverse communities inhabiting productive kelp forests on shallow subtidal rocky reefs in southern California, USA. We combined long-term community surveys from 86 sites with detailed environmental data to determine what structures assemblages of fishes, invertebrates and algae at multiple spatial scales. We identified the spatial scales of variation in species composition using a hierarchical analysis based on eigenfunctions, and assessed how sea surface temperature (SST), water column chlorophyll, giant kelp biomass, wave exposure and potential propagule delivery strength contributed to community variation at each scale. Spatial effects occurring at multiple scales explained 60% of the variation in fish assemblages and 52% of the variation in the assemblages of invertebrates and algae. Most variation occurred over broad spatial scales (> 200 km) consistent with spatial heterogeneity in SST and potential propagule delivery strength, while the latter also explained community variation at medium scales (65-200 km). Small scale (1-65 km) community variation was substantial but not linked to any of the measured drivers. Conclusions were consistent for both reef fishes and benthic invertebrates and algae, despite sharp differences in their adult mobility. Our results demonstrate the scale dependence of environmental drivers on kelp forest communities, showing that most species were strongly sorted along oceanographic conditions over various spatial scales. Such spatial effects must be integrated into models assessing the response of marine ecosystems to climate change.

Marine protected areas and the value of spatially optimized fishery management.

There is a growing focus around the world on marine spatial planning, including spatial fisheries management. Some spatial management approaches are quite blunt, as when marine protected areas (MPAs) are established to restrict fishing in specific locations. Other management tools, such as zoning or spatial user rights, will affect the distribution of fishing effort in a more nuanced manner. Considerable research has focused on the ability of MPAs to increase fishery returns, but the potential for the broader class of spatial management approaches to outperform MPAs has received far less attention. We use bioeconomic models of seven nearshore fisheries in Southern California to explore the value of optimized spatial management in which the distribution of fishing is chosen to maximize profits. We show that fully optimized spatial management can substantially increase fishery profits relative to optimal nonspatial management but that the magnitude of this increase depends on characteristics of the fishing fleet and target species. Strategically placed MPAs can also increase profits substantially compared with nonspatial management, particularly if fishing costs are low, although profit increases available through optimal MPA-based management are roughly half those from fully optimized spatial management. However, if the same total area is protected by randomly placing MPAs, starkly contrasting results emerge: most random MPA designs reduce expected profits. The high value of spatial management estimated here supports continued interest in spatially explicit fisheries regulations but emphasizes that predicted increases in profits can only be achieved if the fishery is well understood and the regulations are strategically designed.

Integrating scientific guidance into marine spatial planning.

Marine spatial planning (MSP), whereby areas of the ocean are zoned for different uses, has great potential to reduce or eliminate conflicts between competing management goals, but only if strategically applied. The recent literature overwhelmingly agrees that including stakeholders in these planning processes is critical to success; but, given the countless alternative ways even simple spatial regulations can be configured, how likely is it that a stakeholder-driven process will generate plans that deliver on the promise of MSP? Here, we use a spatially explicit, dynamic bioeconomic model to show that stakeholder-generated plans are doomed to fail in the absence of strong scientific guidance. While strategically placed spatial regulations can improve outcomes remarkably, the vast majority of possible plans fail to achieve this potential. Surprisingly, existing scientific rules of thumb do little to improve outcomes. Here, we develop an alternative approach in which models are used to identify efficient plans, which are then modified by stakeholders. Even if stakeholders alter these initial proposals considerably, results hugely outperform plans guided by scientific rules of thumb. Our results underscore the importance of spatially explicit dynamic models for the management of marine resources and illustrate how such models can be harmoniously integrated into a stakeholder-driven MSP process.

The importance of progressive senescence in the biomass dynam of giant kelp (Macrocystis pyrifera).

Temporal variation in primary producer biomass has profound effects on the structure and function of the surrounding ecological community. The giant kelp (Macrocystis pyrifera) exhibits strong intra-annual variation in biomass density, which is better explained by the demographic rates of fronds than by those of whole plants. To better understand the processes controlling the dynamics of giant kelp fronds we collected monthly time-series data of frond initiation and survival. These data were used to determine how frond loss and frond initiation rates were predicted by factors thought to affect the growth and survival of Macrocystis, including external environmental factors (i.e., wave height, day length, temperature, nutrient concentration, and neighborhood density) and intrinsic biological characteristics (i.e., frond age, plant size, and nutritional status). Our results revealed that frond dynamics were better explained by intrinsic biological processes rather than external environmental factors. A metric of frond age structure that incorporated progressive senescence was the best predictor of frond loss rate, accounting for 58% of the explained variation in frond loss. A similar analysis revealed that frond age structure was also the single best predictor of frond initiation rate, accounting for 46% of the explained variation. To further examine the importance of senescence in biomass dynamics, we used frond age-dependent mortality and frond initiation rates to predict biomass in subsequent months and found that the model explained 73% of the observed variation in biomass at our sites. Vegetation dynamics of many species including giant kelp are often considered largely in the context of external controls on resource availability and physical disturbance. Our results indicate that investigations of the processes controlling vegetation dynamics may benefit greatly from the inclusion of intrinsic biological factors such as age-dependent mortality and growth, which can outweigh the effects of external forcing in accounting for fluctuations in vegetation biomass.

The value of spatial information in MPA network design.

The science of spatial fisheries management, which combines ecology, oceanography, and economics, has matured significantly. As a result, there have been recent advances in exploiting spatially explicit data to develop spatially explicit management policies, such as networks of marine protected areas (MPAs). However, when data are sparse, spatially explicit policies become less viable, and we must instead rely on blunt policies such as total allowable catches or imprecisely configured networks of MPAs. Therefore, spatial information has the potential to change management approaches and thus has value. We develop a general framework within which to analyze the value of information for spatial fisheries management and apply that framework to several US Pacific coast fisheries. We find that improved spatial information can increase fishery value significantly (>10% in our simulations), and that it changes dramatically the efficient management approach-switching from diffuse effort everywhere to a strategy where fishing is spatially targeted, with some areas under intensive harvest and others closed to fishing. Using all available information, even when incomplete, is essential to management success and may as much as double fishery value relative to using (admittedly incorrect) assumptions commonly invoked.

Long-term ecological research and the COVID-19 anthropause: A window to understanding social-ecological disturbance.

The period of disrupted human activity caused by the COVID-19 pandemic, coined the "anthropause," altered the nature of interactions between humans and ecosystems. It is uncertain how the anthropause has changed ecosystem states, functions, and feedback to human systems through shifts in ecosystem services. Here, we used an existing disturbance framework to propose new investigation pathways for coordinated studies of distributed, long-term social-ecological research to capture effects of the anthropause. Although it is still too early to comprehensively evaluate effects due to pandemic-related delays in data availability and ecological response lags, we detail three case studies that show how long-term data can be used to document and interpret changes in air and water quality and wildlife populations and behavior coinciding with the anthropause. These early findings may guide interpretations of effects of the anthropause as it interacts with other ongoing environmental changes in the future, particularly highlighting the importance of long-term data in separating disturbance impacts from natural variation and long-term trends. Effects of this global disturbance have local to global effects on ecosystems with feedback to social systems that may be detectable at spatial scales captured by nationally to globally distributed research networks.

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.

Triggers and maintenance of multiple shifts in the state of a natural community.

Ecological communities can undergo sudden and dramatic shifts between alternative persistent community states. Both ecological prediction and natural resource management rely on understanding the mechanisms that trigger such shifts and maintain each state. Differentiating between potential mechanisms is difficult, however, because shifts are often recognized only in hindsight and many occur on such large spatial scales that manipulative experiments to test their causes are difficult or impossible. Here we use an approach that focuses first on identifying changes in environmental factors that could have triggered a given state change, and second on examining whether these changes were sustained (and thus potentially maintained the new state) or transitory (explaining the shift but not its persistence). We use this approach to evaluate a community shift in which a benthic marine species of filter feeding sea cucumber (Pachythyone rubra) suddenly came to dominate subtidal rocky reefs that had previously supported high abundances of macroalgae, persisted for more than a decade, then abruptly declined. We found that a sustained period without large wave events coincided with the shift to sea cucumber dominance, but that the sea cucumbers persisted even after the end of this low wave period, indicating that different mechanisms maintained the new community. Additionally, the period of sea cucumber dominance occurred when their predators were rare, and increases in the abundance of these predators coincided with the end of sea cucumber dominance. These results underscore the complex nature of regime shifts and illustrate that focusing separately on the causes and maintenance of state change can be a productive first step for analyzing these shifts in a range of systems.

Perceptions and responses of Pacific Island fishers to changing coral reefs.

The transformation of coral reefs has profound implications for millions of people. However, the interactive effects of changing reefs and fishing remain poorly resolved. We combine underwater surveys (271 000 fishes), catch data (18 000 fishes), and household surveys (351 households) to evaluate how reef fishes and fishers in Moorea, French Polynesia responded to a landscape-scale loss of coral caused by sequential disturbances (a crown-of-thorns sea star outbreak followed by a category 4 cyclone). Although local communities were aware of the disturbances, less than 20% of households reported altering what fishes they caught or ate. This contrasts with substantial changes in the taxonomic composition in the catch data that mirrored changes in fish communities observed on the reef. Our findings highlight that resource users and scientists may have very different interpretations of what constitutes 'change' in these highly dynamic social-ecological systems, with broad implications for successful co-management of coral reef fisheries.

Biomass rather than growth rate determines variation in net primary production by giant kelp.

Net primary production (NPP) is influenced by disturbance-driven fluctuations in foliar standing crop (FSC) and resource-driven fluctuations in rates of recruitment and growth, yet most studies of NPP have focused primarily on factors influencing growth. We quantified NPP, FSC, recruitment, and growth rate for the giant kelp, Macrocystis pyrifera, at three kelp forests in southern California, U.S.A., over a 54-month period and determined the relative roles of FSC, recruitment, and growth rate in contributing to variation in annual NPP. Net primary production averaged between 0.42 and 2.38 kg dry mass x m(-2) x yr(-1) at the three sites. The initial FSC present at the beginning of the growth year and the recruitment of new plants during the year explained 63% and 21% of the interannual variation observed in NPP, respectively. The previous year's NPP and disturbance from waves collectively accounted for 80% of the interannual variation in initial FSC. No correlation was found between annual growth rate (i.e., the amount of new kelp mass produced per unit of existing kelp mass) and annual NPP (i.e., the amount of new kelp mass produced per unit area of ocean bottom), largely because annual growth rate was consistent compared to initial FSC and recruitment, which fluctuated greatly among years and sites. Although growth rate was a poor predictor of variation in annual NPP, it was principally responsible for the high mean values observed for NPP by Macrocystis. These high mean values reflected rapid growth (average of approximately 2% per day) of a relatively small standing crop (maximum annual mean = 444 g dry mass/m2) that replaced itself approximately seven times per year. Disturbance-driven variability in FSC may be generally important in explaining variation in NPP, yet it is rarely examined because cycles of disturbance and recovery occur over timescales of decades or more in many systems. Considerable insight into how variation in FSC drives variation in NPP may be gained by studying systems such as giant kelp forests that are characterized by frequent disturbance and rapid rates of growth and recruitment.

Net primary production, growth, and standing crop of Macrocystis pyrifera in Southern California.

Marine macroalgae are believed to be among the most productive autotrophs in the world. However, relatively little information exists about spatial and temporal variation in net primary production (NPP) by these organisms. The data presented here are being collected to investigate patterns and causes of variation in NPP by the giant kelp, Macrocystis pyrifera, which is believed to be one of the fastest growing autotrophs on earth. The standing crop and loss rates of M. pyrifera have been measured monthly in permanent plots at three sites in the Santa Barbara Channel, USA. Collection of these data began in June 2002 and is ongoing. Seasonal estimates of NPP and growth rate are made by combining the field data with a model of kelp dynamics. The purpose of this Data Paper is to make available a time series of M. pyrifera NPP, growth, and standing crop that is appropriate for examining seasonal and interannual patterns across multiple sites. Data on plant density in each plot and censuses of fronds on tagged plants at each site are also made available here. NPP, mass-specific growth rate, and standing crop are presented in four different metrics (wet mass, dry mass, carbon mass, and nitrogen mass) to facilitate comparisons with previous studies of M. pyrifera and with NPP measured in other ecosystems. Analyses of these data reveal seasonal cycles in growth and standing crop as well as substantial differences in M. pyrifera NPP among sites and years.

The effects of landscape structure on space competition and alternative stable states.

Many species that compete for space live on heterogeneous landscapes and interact at local scales. The quality, amount, and structure of landscapes may have considerable impact on the ability of species to compete or coexist, yet basic models of space competition do not include that level of detail. We model space competition between two species with positive feedback through recruitment facilitation, which creates the potential for alternative stable states to occur. We compare the predictions of a spatially implicit model with a simulation model that includes explicit space and landscape structure. We create structured landscapes in which we specify the amount of habitat and degree of fragmentation and ask how landscape structure, dispersal strategy, and scale affect the presence of alternative stable states, or bistability. We find that structured landscapes can reduce the range of parameter values that lead to bistability in our model, but they do not eliminate bistability. The type of landscape and the dispersal distance for each species also influence the amount of environmental change needed for abrupt community shifts to occur. Coexistence of the two competitors is possible under certain conditions when connectivity is low. Consequently, landscape structure may lead to considerable disparity between the predictions of simple models and actual dynamics on complex landscapes during environmental change.

Extreme warming challenges sentinel status of kelp forests as indicators of climate change.

The desire to use sentinel species as early warning indicators of impending climate change effects on entire ecosystems is attractive, but we need to verify that such approaches have sound biological foundations. A recent large-scale warming event in the North Pacific Ocean of unprecedented magnitude and duration allowed us to evaluate the sentinel status of giant kelp, a coastal foundation species that thrives in cold, nutrient-rich waters and is considered sensitive to warming. Here, we show that giant kelp and the majority of species that associate with it did not presage ecosystem effects of extreme warming off southern California despite giant kelp's expected vulnerability. Our results challenge the general perception that kelp-dominated systems are highly vulnerable to extreme warming events and expose the more general risk of relying on supposed sentinel species that are assumed to be very sensitive to climate change.