Ocean warming undermines the recovery resilience of New England kelp forests following a fishery-induced trophic cascade.

Ecological theory predicts that kelp forests structured by trophic cascades should experience recovery and persistence of their foundation species when herbivores become rare. Yet, climate change may be altering the outcomes of top-down forcing in kelp forests, especially those located in regions that have rapidly warmed in recent decades, such as the Gulf of Maine. Here, using data collected annually from 30+ sites spanning >350 km of coastline, we explored the dynamics of Maine's kelp forests in the ~20 years after a fishery-induced elimination of sea urchin herbivores. Although forests (Saccharina latissima and Laminaria digitata) had broadly returned to Maine in the late 20th century, we found that forests in northeast Maine have since experienced slow but significant declines in kelp, and forest persistence in the northeast was juxtaposed by a rapid, widespread collapse in the southwest. Forests collapsed in the southwest apparently because ocean warming has-directly and indirectly-made this area inhospitable to kelp. Indeed, when modeling drivers of change using causal techniques from econometrics, we discovered that unusually high summer seawater temperatures the year prior, unusually high spring seawater temperatures, and high sea urchin densities each negatively impacted kelp abundance. Furthermore, the relative power and absolute impact of these drivers varied geographically. Our findings reveal that ocean warming is redefining the outcomes of top-down forcing in this system, whereby herbivore removal no longer predictably leads to a sustained dominance of foundational kelps but instead has led to a waning dominance (northeast) or the rise of a novel phase state defined by "turf" algae (southwest). Such findings indicate that limiting climate change and managing for low herbivore abundances will be essential for preventing further loss of the vast forests that still exist in northeast Maine. They also more broadly highlight that climate change is "rewriting the rules" of nature, and thus that ecological theory and practice must be revised to account for shifting species and processes.

Evidence of elevated heavy metals concentrations in wild and farmed sugar kelp (Saccharina latissima) in New England.

Seaweed farming in the United States is gaining significant financial and political support due to prospects to sustainably expand domestic economies with environmentally friendly products. Several networks are seeking appropriate synthesis of available science to both inform policy and substantiate the sector's sustainability claims. Significant knowledge gaps remain regarding seaweed-specific food hazards and their mitigation; a resource-intensive challenge that can inhibit sustainable policies. This is particularly concerning for rapidly expanding Saccharina latissima (sugar kelp) crops, a brown seaweed that is known to accumulate heavy metals linked to food hazards. Here, we present baseline information about concentrations of arsenic, cadmium, lead, and mercury, in both wild and farmed sugar kelp from the New England region. We interpret our findings based on proximity to potential sources of contamination, location on blade, and available heavy metals standards. Contrary to our expectations, high concentrations were widespread in both wild and farmed populations, regardless of proximity to contamination. We find, like others, that cadmium and arsenic consistently reach levels of regulatory concern, and that dried seaweeds could harbor higher concentrations compared to raw products. We also share unique findings that suggest some toxins concentrate at the base of kelp blades. Our results are one step towards aggregating vital data for the region to expand its seaweed farming footprint.

Clarifying the effect of biodiversity on productivity in natural ecosystems with longitudinal data and methods for causal inference.

Causal effects of biodiversity on ecosystem functions can be estimated using experimental or observational designs - designs that pose a tradeoff between drawing credible causal inferences from correlations and drawing generalizable inferences. Here, we develop a design that reduces this tradeoff and revisits the question of how plant species diversity affects productivity. Our design leverages longitudinal data from 43 grasslands in 11 countries and approaches borrowed from fields outside of ecology to draw causal inferences from observational data. Contrary to many prior studies, we estimate that increases in plot-level species richness caused productivity to decline: a 10% increase in richness decreased productivity by 2.4%, 95% CI [-4.1, -0.74]. This contradiction stems from two sources. First, prior observational studies incompletely control for confounding factors. Second, most experiments plant fewer rare and non-native species than exist in nature. Although increases in native, dominant species increased productivity, increases in rare and non-native species decreased productivity, making the average effect negative in our study. By reducing the tradeoff between experimental and observational designs, our study demonstrates how observational studies can complement prior ecological experiments and inform future ones.

The value of ecosystem services in global marine kelp forests.

While marine kelp forests have provided valuable ecosystem services for millennia, the global ecological and economic value of those services is largely unresolved. Kelp forests are diminishing in many regions worldwide, and efforts to manage these ecosystems are hindered without accurate estimates of the value of the services that kelp forests provide to human societies. Here, we present a global estimate of the ecological and economic potential of three key ecosystem services - fisheries production, nutrient cycling, and carbon removal provided by six major forest forming kelp genera (Ecklonia, Laminaria, Lessonia, Macrocystis, Nereocystis, and Saccharina). Each of these genera creates a potential value of between $64,400 and $147,100/hectare each year. Collectively, they generate between $465 and $562 billion/year worldwide, with an average of $500 billion. These values are primarily driven by fisheries production (mean $29,900, 904 Kg/Ha/year) and nitrogen removal ($73,800, 657 Kg N/Ha/year), though kelp forests are also estimated to sequester 4.91 megatons of carbon from the atmosphere/year highlighting their potential as blue carbon systems for climate change mitigation. These findings highlight the ecological and economic value of kelp forests to society and will facilitate better informed marine management and conservation decisions.

Kelp carbon sink potential decreases with warming due to accelerating decomposition.

Cycling of organic carbon in the ocean has the potential to mitigate or exacerbate global climate change, but major questions remain about the environmental controls on organic carbon flux in the coastal zone. Here, we used a field experiment distributed across 28° of latitude, and the entire range of 2 dominant kelp species in the northern hemisphere, to measure decomposition rates of kelp detritus on the seafloor in relation to local environmental factors. Detritus decomposition in both species were strongly related to ocean temperature and initial carbon content, with higher rates of biomass loss at lower latitudes with warmer temperatures. Our experiment showed slow overall decomposition and turnover of kelp detritus and modeling of coastal residence times at our study sites revealed that a significant portion of this production can remain intact long enough to reach deep marine sinks. The results suggest that decomposition of these kelp species could accelerate with ocean warming and that low-latitude kelp forests could experience the greatest increase in remineralization with a 9% to 42% reduced potential for transport to long-term ocean sinks under short-term (RCP4.5) and long-term (RCP8.5) warming scenarios. However, slow decomposition at high latitudes, where kelp abundance is predicted to expand, indicates potential for increasing kelp-carbon sinks in cooler (northern) regions. Our findings reveal an important latitudinal gradient in coastal ecosystem function that provides an improved capacity to predict the implications of ocean warming on carbon cycling. Broad-scale patterns in organic carbon decomposition revealed here can be used to identify hotspots of carbon sequestration potential and resolve relationships between carbon cycling processes and ocean climate at a global scale.

Automated satellite remote sensing of giant kelp at the Falkland Islands (Islas Malvinas).

Giant kelp populations that support productive and diverse coastal ecosystems at temperate and subpolar latitudes of both hemispheres are vulnerable to changing climate conditions as well as direct human impacts. Observations of giant kelp forests are spatially and temporally uneven, with disproportionate coverage in the northern hemisphere, despite the size and comparable density of southern hemisphere kelp forests. Satellite imagery enables the mapping of existing and historical giant kelp populations in understudied regions, but automating the detection of giant kelp using satellite imagery requires approaches that are robust to the optical complexity of the shallow, nearshore environment. We present and compare two approaches for automating the detection of giant kelp in satellite datasets: one based on crowd sourcing of satellite imagery classifications and another based on a decision tree paired with a spectral unmixing algorithm (automated using Google Earth Engine). Both approaches are applied to satellite imagery (Landsat) of the Falkland Islands or Islas Malvinas (FLK), an archipelago in the southern Atlantic Ocean that supports expansive giant kelp ecosystems. The performance of each method is evaluated by comparing the automated classifications with a subset of expert-annotated imagery (8 images spanning the majority of our continuous timeseries, cumulatively covering over 2,700 km of coastline, and including all relevant sensors). Using the remote sensing approaches evaluated herein, we present the first continuous timeseries of giant kelp observations in the FLK region using Landsat imagery spanning over three decades. We do not detect evidence of long-term change in the FLK region, although we observe a recent decline in total canopy area from 2017-2021. Using a nitrate model based on nearby ocean state measurements obtained from ships and incorporating satellite sea surface temperature products, we find that the area of giant kelp forests in the FLK region is positively correlated with the nitrate content observed during the prior year. Our results indicate that giant kelp classifications using citizen science are approximately consistent with classifications based on a state-of-the-art automated spectral approach. Despite differences in accuracy and sensitivity, both approaches find high interannual variability that impedes the detection of potential long-term changes in giant kelp canopy area, although recent canopy area declines are notable and should continue to be monitored carefully.

Feral hogs control brackish marsh plant communities over time.

Feral hogs modify ecosystems by consuming native species and altering habitat structure. These invasions can generate fundamentally different post-invasion habitats when disturbance changes community structure, ecosystem function, or recovery dynamics. Here, we use multiple three-year exclusion experiments to describe how feral hogs affect hyper-productive brackish marshes over time. We find that infrequent yet consistent hog foraging and trampling suppresses dominant plants by generating a perpetually disturbed habitat that favors competitively inferior species and disallows full vegetative recovery over time. Along borders between plant monocultures, trampling destroys dominant graminoids responsible for most aboveground marsh biomass while competitively inferior plants increase fivefold. Hog activities shift the brackish marsh disturbance regime from pulse to press, which changes the plant community: competitively inferior plants increase coverage, species diversity is doubled, and live cover is lowered by 30% as large plants are unable to take hold in hog-disturbed areas. Release from disturbance does not result in complete recovery (i.e., dominant plant monocultures) because hog consumer control is a combination of both top-down control and broader engineering effects. These results highlight how habitats are susceptible to invasive effects outside of structural destruction alone, especially if large consumers are pervasive over time and change the dynamics that sustain recovery.

A large invasive consumer reduces coastal ecosystem resilience by disabling positive species interactions.

Invasive consumers can cause extensive ecological damage to native communities but effects on ecosystem resilience are less understood. Here, we use drone surveys, manipulative experiments, and mathematical models to show how feral hogs reduce resilience in southeastern US salt marshes by dismantling an essential marsh cordgrass-ribbed mussel mutualism. Mussels usually double plant growth and enhance marsh resilience to extreme drought but, when hogs invade, switch from being essential for plant survival to a liability; hogs selectively forage in mussel-rich areas leading to a 50% reduction in plant biomass and slower post-drought recovery rate. Hogs increase habitat fragmentation across landscapes by maintaining large, disturbed areas through trampling of cordgrass during targeted mussel consumption. Experiments and climate-disturbance recovery models show trampling alone slows marsh recovery by 3x while focused mussel predation creates marshes that may never recover from large-scale disturbances without hog eradication. Our work highlights that an invasive consumer can reshape ecosystems not just via competition and predation, but by disrupting key, positive species interactions that underlie resilience to climatic disturbances.

Grand challenges in biodiversity-ecosystem functioning research in the era of science-policy platforms require explicit consideration of feedbacks.

Feedbacks are an essential feature of resilient socio-economic systems, yet the feedbacks between biodiversity, ecosystem services and human wellbeing are not fully accounted for in global policy efforts that consider future scenarios for human activities and their consequences for nature. Failure to integrate feedbacks in our knowledge frameworks exacerbates uncertainty in future projections and potentially prevents us from realizing the full benefits of actions we can take to enhance sustainability. We identify six scientific research challenges that, if addressed, could allow future policy, conservation and monitoring efforts to quantitatively account for ecosystem and societal consequences of biodiversity change. Placing feedbacks prominently in our frameworks would lead to (i) coordinated observation of biodiversity change, ecosystem functions and human actions, (ii) joint experiment and observation programmes, (iii) more effective use of emerging technologies in biodiversity science and policy, and (iv) a more inclusive and integrated global community of biodiversity observers. To meet these challenges, we outline a five-point action plan for collaboration and connection among scientists and policymakers that emphasizes diversity, inclusion and open access. Efforts to protect biodiversity require the best possible scientific understanding of human activities, biodiversity trends, ecosystem functions and-critically-the feedbacks among them.

General destabilizing effects of eutrophication on grassland productivity at multiple spatial scales.

Eutrophication is a widespread environmental change that usually reduces the stabilizing effect of plant diversity on productivity in local communities. Whether this effect is scale dependent remains to be elucidated. Here, we determine the relationship between plant diversity and temporal stability of productivity for 243 plant communities from 42 grasslands across the globe and quantify the effect of chronic fertilization on these relationships. Unfertilized local communities with more plant species exhibit greater asynchronous dynamics among species in response to natural environmental fluctuations, resulting in greater local stability (alpha stability). Moreover, neighborhood communities that have greater spatial variation in plant species composition within sites (higher beta diversity) have greater spatial asynchrony of productivity among communities, resulting in greater stability at the larger scale (gamma stability). Importantly, fertilization consistently weakens the contribution of plant diversity to both of these stabilizing mechanisms, thus diminishing the positive effect of biodiversity on stability at differing spatial scales. Our findings suggest that preserving grassland functional stability requires conservation of plant diversity within and among ecological communities.

The geography of biodiversity change in marine and terrestrial assemblages.

Human activities are fundamentally altering biodiversity. Projections of declines at the global scale are contrasted by highly variable trends at local scales, suggesting that biodiversity change may be spatially structured. Here, we examined spatial variation in species richness and composition change using more than 50,000 biodiversity time series from 239 studies and found clear geographic variation in biodiversity change. Rapid compositional change is prevalent, with marine biomes exceeding and terrestrial biomes trailing the overall trend. Assemblage richness is not changing on average, although locations exhibiting increasing and decreasing trends of up to about 20% per year were found in some marine studies. At local scales, widespread compositional reorganization is most often decoupled from richness change, and biodiversity change is strongest and most variable in the oceans.

Structure-function analysis of ß-arrestin Kurtz reveals a critical role of receptor interactions in downregulation of GPCR signaling in vivo.

Arrestins control signaling via the G protein coupled receptors (GPCRs), serving as both signal terminators and transducers. Previous studies identified several structural elements in arrestins that contribute to their functions as GPCR regulators. However, the importance of these elements in vivo is unclear, and the developmental roles of arrestins are not well understood. We carried out an in vivo structure-function analysis of Kurtz (Krz), the single ortholog of mammalian ß-arrestins in the Drosophila genome. A combination of Krz mutations affecting the GPCR-phosphosensing and receptor core-binding ("finger loop") functions (Krz-KKVL/A) resulted in a complete loss of Krz activity during development. Endosome recruitment and bioluminescence resonance energy transfer (BRET) assays revealed that the KKVL/A mutations abolished the GPCR-binding ability of Krz. We found that the isolated "finger loop" mutation (Krz-VL/A), while having a negligible effect on GPCR internalization, severely affected Krz function, suggesting that tight receptor interactions are necessary for proper termination of signaling in vivo. Genetic analysis as well as live imaging demonstrated that mutations in Krz led to hyperactivity of the GPCR Mist (also known as Mthl1), which is activated by its ligand Folded gastrulation (Fog) and is responsible for cellular contractility and epithelial morphogenesis. Krz mutations affected two developmental events that are under the control of Fog-Mist signaling: gastrulation and morphogenesis of the wing. Overall, our data reveal the functional importance in vivo of direct ß-arrestin/GPCR binding, which is mediated by the recognition of the phosphorylated receptor tail and receptor core interaction. These Krz-GPCR interactions are critical for setting the correct level of Fog-Mist signaling during epithelial morphogenesis.

Lineage overwhelms environmental conditions in determining rhizosphere bacterial community structure in a cosmopolitan invasive plant.

Plant-microbe interactions play crucial roles in species invasions but are rarely investigated at the intraspecific level. Here, we study these interactions in three lineages of a globally distributed plant, Phragmites australis. We use field surveys and a common garden experiment to analyze bacterial communities in the rhizosphere of P. australis stands from native, introduced, and Gulf lineages to determine lineage-specific controls on rhizosphere bacteria. We show that within-lineage bacterial communities are similar, but are distinct among lineages, which is consistent with our results in a complementary common garden experiment. Introduced P. australis rhizosphere bacterial communities have lower abundances of pathways involved in antimicrobial biosynthesis and degradation, suggesting a lower exposure to enemy attack than native and Gulf lineages. However, lineage and not rhizosphere bacterial communities dictate individual plant growth in the common garden experiment. We conclude that lineage is crucial for determination of both rhizosphere bacterial communities and plant fitness.Environmental factors often outweigh host heritable factors in structuring host-associated microbiomes. Here, Bowen et al. show that host lineage is crucial for determination of rhizosphere bacterial communities in Phragmites australis, a globally distributed invasive plant.

Estimating local biodiversity change: a critique of papers claiming no net loss of local diversity.

Global species extinction rates are orders of magnitude above the background rate documented in the fossil record. However, recent data syntheses have found mixed evidence for patterns of net species loss at local spatial scales. For example, two recent data meta-analyses have found that species richness is decreasing in some locations and is increasing in others. When these trends are combined, these papers argued there has been no net change in species richness, and suggested this pattern is globally representative of biodiversity change at local scales. Here we reanalyze results of these data syntheses and outline why this conclusion is unfounded. First, we show the datasets collated for these syntheses are spatially biased and not representative of the spatial distribution of species richness or the distribution of many primary drivers of biodiversity change. This casts doubt that their results are representative of global patterns. Second, we argue that detecting the trend in local species richness is very difficult with short time series and can lead to biased estimates of change. Reanalyses of the data detected a signal of study duration on biodiversity change, indicating net biodiversity loss is most apparent in studies of longer duration. Third, estimates of species richness change can be biased if species gains during post-disturbance recovery are included without also including species losses that occurred during the disturbance. Net species gains or losses should be assessed with respect to common baselines or reference communities. Ultimately, we need a globally coordinated effort to monitor biodiversity so that we can estimate and attribute human impacts as causes of biodiversity change. A combination of technologies will be needed to produce regularly updated global datasets of local biodiversity change to guide future policy. At this time the conclusion that there is no net change in local species richness is not the consensus state of knowledge.

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.

Marine extinction risk shaped by trait-environment interactions over 500 million years.

Perhaps the most pressing issue in predicting biotic responses to present and future global change is understanding how environmental factors shape the relationship between ecological traits and extinction risk. The fossil record provides millions of years of insight into how extinction selectivity (i.e., differential extinction risk) is shaped by interactions between ecological traits and environmental conditions. Numerous paleontological studies have examined trait-based extinction selectivity; however, the extent to which these patterns are shaped by environmental conditions is poorly understood due to a lack of quantitative synthesis across studies. We conducted a meta-analysis of published studies on fossil marine bivalves and gastropods that span 458 million years to uncover how global environmental and geochemical changes covary with trait-based extinction selectivity. We focused on geographic range size and life habit (i.e., infaunal vs. epifaunal), two of the most important and commonly examined predictors of extinction selectivity. We used geochemical proxies related to global climate, as well as indicators of ocean acidification, to infer average global environmental conditions. Life-habit selectivity is weakly dependent on environmental conditions, with infaunal species relatively buffered from extinction during warmer climate states. In contrast, the odds of taxa with broad geographic ranges surviving an extinction (>2500 km for genera, >500 km for species) are on average three times greater than narrow-ranging taxa (estimate of odds ratio: 2.8, 95% confidence interval = 2.3-3.5), regardless of the prevailing global environmental conditions. The environmental independence of geographic range size extinction selectivity emphasizes the critical role of geographic range size in setting conservation priorities.

Recent Trends in Local-Scale Marine Biodiversity Reflect Community Structure and Human Impacts.

The modern biodiversity crisis reflects global extinctions and local introductions. Human activities have dramatically altered rates and scales of processes that regulate biodiversity at local scales. Reconciling the threat of global biodiversity loss with recent evidence of stability at fine spatial scales is a major challenge and requires a nuanced approach to biodiversity change that integrates ecological understanding. With a new dataset of 471 diversity time series spanning from 1962 to 2015 from marine coastal ecosystems, we tested (1) whether biodiversity changed at local scales in recent decades, and (2) whether we can ignore ecological context (e.g., proximate human impacts, trophic level, spatial scale) and still make informative inferences regarding local change. We detected a predominant signal of increasing species richness in coastal systems since 1962 in our dataset, though net species loss was associated with localized effects of anthropogenic impacts. Our geographically extensive dataset is unlikely to be a random sample of marine coastal habitats; impacted sites (3% of our time series) were underrepresented relative to their global presence. These local-scale patterns do not contradict the prospect of accelerating global extinctions but are consistent with local species loss in areas with direct human impacts and increases in diversity due to invasions and range expansions in lower impact areas. Attempts to detect and understand local biodiversity trends are incomplete without information on local human activities and ecological context.