Rise of Ruppia in Chesapeake Bay: Climate change-driven turnover of foundation species creates new threats and management opportunities.

Global change has converted many structurally complex and ecologically and economically valuable coastlines to bare substrate. In the structural habitats that remain, climate-tolerant and opportunistic species are increasing in response to environmental extremes and variability. The shifting of dominant foundation species identity with climate change poses a unique conservation challenge because species vary in their responses to environmental stressors and to management. Here, we combine 35 y of watershed modeling and biogeochemical water quality data with species comprehensive aerial surveys to describe causes and consequences of turnover in seagrass foundation species across 26,000 ha of habitat in the Chesapeake Bay. Repeated marine heatwaves have caused 54% retraction of the formerly dominant eelgrass (Zostera marina) since 1991, allowing 171% expansion of the temperature-tolerant widgeongrass (Ruppia maritima) that has likewise benefited from large-scale nutrient reductions. However, this phase shift in dominant seagrass identity now presents two significant shifts for management: Widgeongrass meadows are not only responsible for rapid, extensive recoveries but also for the largest crashes over the last four decades; and, while adapted to high temperatures, are much more susceptible than eelgrass to nutrient pulses driven by springtime runoff. Thus, by selecting for rapid post-disturbance recolonization but low resistance to punctuated freshwater flow disturbance, climate change could threaten the Chesapeake Bay seagrass' ability to provide consistent fishery habitat and sustain functioning over time. We demonstrate that understanding the dynamics of the next generation of foundation species is a critical management priority, because shifts from relatively stable habitat to high interannual variability can have far-reaching consequences across marine and terrestrial ecosystems.

A Pleistocene legacy structures variation in modern seagrass ecosystems.

Distribution of Earth's biomes is structured by the match between climate and plant traits, which in turn shape associated communities and ecosystem processes and services. However, that climate-trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth's environment changes faster than at any time in human history, critical questions are whether and how organismal traits and ecosystems can adjust to altered conditions. We quantified the relative importance of current environmental forcing versus evolutionary history in shaping the growth form (stature and biomass) and associated community of eelgrass (Zostera marina), a widespread foundation plant of marine ecosystems along Northern Hemisphere coastlines, which experienced major shifts in distribution and genetic composition during the Pleistocene. We found that eelgrass stature and biomass retain a legacy of the Pleistocene colonization of the Atlantic from the ancestral Pacific range and of more recent within-basin bottlenecks and genetic differentiation. This evolutionary legacy in turn influences the biomass of associated algae and invertebrates that fuel coastal food webs, with effects comparable to or stronger than effects of current environmental forcing. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems.

Interplay of management and environmental drivers shifts size structure of reef fish communities.

Countries are expanding marine protected area (MPA) networks to mitigate fisheries declines and support marine biodiversity. However, MPA impact evaluations typically assess total fish biomass. Here, we examine how fish biomass disaggregated by adult and juvenile life stages responds to environmental drivers, including sea surface temperature (SST) anomalies and human footprint, and multiple management types at 139 reef sites in the Mesoamerican Reef (MAR) region. We found that total fish biomass generally appears stable across the region from 2006 to 2018, with limited rebuilding of fish stocks in MPAs. However, the metric of total fish biomass masked changes in fish community structure, with lower adult than juvenile fish biomass at northern sites, and adult:juvenile ratios closer to 1:1 at southern sites. These shifts were associated with different responses of juvenile and adult fish to environmental drivers and management. Juvenile fish biomass increased at sites with high larval connectivity and coral cover, whereas adult fish biomass decreased at sites with greater human footprint and SST anomalies. Adult fish biomass decreased primarily in Honduran general use zones, which suggests insufficient protection for adult fish in the southern MAR. There was a north-south gradient in management and environmental drivers, with lower coverage of fully protected areas and higher SST anomalies and coastal development in the south that together may undermine the maintenance of adult fish biomass in the southern MAR. Accounting for the interplay between environmental drivers and management in the design of MPAs is critical for increasing fish biomass across life history stages.

Los países están ampliando las redes de áreas marinas protegidas (AMP) para mitigar la disminución de las pesquerías y apoyar la biodiversidad marina. Sin embargo, las evaluaciones de impacto de las AMP típicamente estudian la biomasa total de peces. Aquí, examinamos cómo la biomasa de peces desagregada por etapas de vida adultas y juveniles responde a factores ambientales como anomalías de la temperatura superficial del mar (SST) e impacto humano, y múltiples tipos de manejo en 139 sitios de arrecifes en el sistema arrecifal mesoamericano (SAM). Encontramos que la biomasa total de peces en general parece estable en toda la región entre 2006 y 2018, con una recuperación limitada de las poblaciones de peces en las AMP. Sin embargo, la métrica de biomasa total de peces enmascaró los cambios en la estructura de la comunidad de peces, con una biomasa de peces adultos más baja que juveniles en los sitios del norte, y proporciones adulto:juvenil más cercana a 1:1 en los sitios del sur. Estos cambios fueron asociados con diferentes respuestas de peces juveniles y adultos a variables ambientales y de manejo. La biomasa de peces juveniles aumentó en sitios con alta conectividad larvaria y cobertura coralina, mientras que la biomasa de peces adultos disminuyó en sitios con mayor impacto humano y anomalías en la SST. La biomasa de peces adultos disminuyó principalmente en las zonas de uso general (GUZ) hondureñas, lo cual sugiere una protección insuficiente para peces adultos en el sur del SAM. Hubo un gradiente norte­sur en el manejo y los factores ambientales, con menor cobertura de áreas totalmente protegidas y mayores anomalías de SST y desarrollo costero en el sur. En conjunto esto puede degradar el mantenimiento de la biomasa de peces adultos en el sur del SAM. La interacción entre factores ambientales y el manejo en el diseño de las AMP es fundamental para aumentar la biomasa de peces en todas las etapas del ciclo de vida.

Climate drives the geography of marine consumption by changing predator communities.

The global distribution of primary production and consumption by humans (fisheries) is well-documented, but we have no map linking the central ecological process of consumption within food webs to temperature and other ecological drivers. Using standardized assays that span 105° of latitude on four continents, we show that rates of bait consumption by generalist predators in shallow marine ecosystems are tightly linked to both temperature and the composition of consumer assemblages. Unexpectedly, rates of consumption peaked at midlatitudes (25 to 35°) in both Northern and Southern Hemispheres across both seagrass and unvegetated sediment habitats. This pattern contrasts with terrestrial systems, where biotic interactions reportedly weaken away from the equator, but it parallels an emerging pattern of a subtropical peak in marine biodiversity. The higher consumption at midlatitudes was closely related to the type of consumers present, which explained rates of consumption better than consumer density, biomass, species diversity, or habitat. Indeed, the apparent effect of temperature on consumption was mostly driven by temperature-associated turnover in consumer community composition. Our findings reinforce the key influence of climate warming on altered species composition and highlight its implications for the functioning of Earth's ecosystems.

Climate affects the outbreaks of a forest defoliator indirectly through its tree hosts.

Although spatial variation in climate can directly affect the survival and reproduction of forest insects and the tree species compositions of forests, little is known about the indirect effects of climate on outbreaks of forest insects through its effects on forest composition. In this study, we use structural equation modeling to examine the direct and indirect effects of climate, water capacity of the soil, host tree density, and non-host density on the spatial extent of Lymantria dispar outbreaks in the Eastern USA over a period of 44 years (1975-2018). Host species were subdivided into four taxonomic and ecologically distinct groups: red oaks (Lobatae), white oaks (Lepidobalanus), other preferred hosts, and intermediate (less preferred) hosts. We found that mean annual temperature had stronger effects than mean annual precipitation on the spatial extent of outbreaks, and that indirect effects of temperature (via its effects on oak density) on defoliation were stronger than direct effects. The density of non-host trees increased with increasing precipitation and, consistent with the 'associational resistance hypothesis', defoliation decreased with increasing density of non-host trees. This study offers quantitative evidence that geographic variation in climate can indirectly affect outbreaks of a forest insect through its effects on tree species composition.

Data synthesis for environmental management: A case study of Chesapeake Bay.

Synthesizing large, complex data sets to inform resource managers towards effective environmental stewardship is a universal challenge. In Chesapeake Bay, a well-studied and intensively monitored estuary in North America, the challenge of synthesizing data on water quality and land use as factors related to a key habitat, submerged aquatic vegetation, was tackled by a team of scientists and resource managers operating at multiple levels of governance (state, federal). The synthesis effort took place over a two-year period (2016-2018), and the results were communicated widely to a) scientists via peer review publications and conference presentations; b) resource managers via web materials and workshop presentations; and c) the public through newspaper articles, radio interviews, and podcasts. The synthesis effort was initiated by resource managers at the United States Environmental Protection Agencys' Chesapeake Bay Program and 16 scientist participants were recruited from a diversity of organizations. Multiple short, immersive workshops were conducted regularly to conceptualize the problem, followed by data analysis and interpretation that supported the preparation of the synthetic products that were communicated widely. Reflections on the process indicate that there are a variety of structural and functional requirements, as well as enabling conditions, that need to be considered to achieve successful outcomes from synthesis efforts.

Long-term nutrient reductions lead to the unprecedented recovery of a temperate coastal region.

Humans strongly impact the dynamics of coastal systems, yet surprisingly few studies mechanistically link management of anthropogenic stressors and successful restoration of nearshore habitats over large spatial and temporal scales. Such examples are sorely needed to ensure the success of ecosystem restoration efforts worldwide. Here, we unite 30 consecutive years of watershed modeling, biogeochemical data, and comprehensive aerial surveys of Chesapeake Bay, United States to quantify the cascading effects of anthropogenic impacts on submersed aquatic vegetation (SAV), an ecologically and economically valuable habitat. We employ structural equation models to link land use change to higher nutrient loads, which in turn reduce SAV cover through multiple, independent pathways. We also show through our models that high biodiversity of SAV consistently promotes cover, an unexpected finding that corroborates emerging evidence from other terrestrial and marine systems. Due to sustained management actions that have reduced nitrogen concentrations in Chesapeake Bay by 23% since 1984, SAV has regained 17,000 ha to achieve its highest cover in almost half a century. Our study empirically demonstrates that nutrient reductions and biodiversity conservation are effective strategies to aid the successful recovery of degraded systems at regional scales, a finding which is highly relevant to the utility of environmental management programs worldwide.

Integrating abundance and functional traits reveals new global hotspots of fish diversity.

Species richness has dominated our view of global biodiversity patterns for centuries. The dominance of this paradigm is reflected in the focus by ecologists and conservation managers on richness and associated occurrence-based measures for understanding drivers of broad-scale diversity patterns and as a biological basis for management. However, this is changing rapidly, as it is now recognized that not only the number of species but the species present, their phenotypes and the number of individuals of each species are critical in determining the nature and strength of the relationships between species diversity and a range of ecological functions (such as biomass production and nutrient cycling). Integrating these measures should provide a more relevant representation of global biodiversity patterns in terms of ecological functions than that provided by simple species counts. Here we provide comparisons of a traditional global biodiversity distribution measure based on richness with metrics that incorporate species abundances and functional traits. We use data from standardized quantitative surveys of 2,473 marine reef fish species at 1,844 sites, spanning 133 degrees of latitude from all ocean basins, to identify new diversity hotspots in some temperate regions and the tropical eastern Pacific Ocean. These relate to high diversity of functional traits amongst individuals in the community (calculated using Rao's Q), and differ from previously reported patterns in functional diversity and richness for terrestrial animals, which emphasize species-rich tropical regions only. There is a global trend for greater evenness in the number of individuals of each species, across the reef fish species observed at sites ('community evenness'), at higher latitudes. This contributes to the distribution of functional diversity hotspots and contrasts with well-known latitudinal gradients in richness. Our findings suggest that the contribution of species diversity to a range of ecosystem functions varies over large scales, and imply that in tropical regions, which have higher numbers of species, each species contributes proportionally less to community-level ecological processes on average than species in temperate regions. Metrics of ecological function usefully complement metrics of species diversity in conservation management, including when identifying planning priorities and when tracking changes to biodiversity values.

Biodiversity enhances reef fish biomass and resistance to climate change.

Fishes are the most diverse group of vertebrates, play key functional roles in aquatic ecosystems, and provide protein for a billion people, especially in the developing world. Those functions are compromised by mounting pressures on marine biodiversity and ecosystems. Because of its economic and food value, fish biomass production provides an unusually direct link from biodiversity to critical ecosystem services. We used the Reef Life Survey's global database of 4,556 standardized fish surveys to test the importance of biodiversity to fish production relative to 25 environmental drivers. Temperature, biodiversity, and human influence together explained 47% of the global variation in reef fish biomass among sites. Fish species richness and functional diversity were among the strongest predictors of fish biomass, particularly for the large-bodied species and carnivores preferred by fishers, and these biodiversity effects were robust to potentially confounding influences of sample abundance, scale, and environmental correlations. Warmer temperatures increased biomass directly, presumably by raising metabolism, and indirectly by increasing diversity, whereas temperature variability reduced biomass. Importantly, diversity and climate interact, with biomass of diverse communities less affected by rising and variable temperatures than species-poor communities. Biodiversity thus buffers global fish biomass from climate change, and conservation of marine biodiversity can stabilize fish production in a changing ocean.

Multiple stressors threaten the imperiled coastal foundation species eelgrass (Zostera marina) in Chesapeake Bay, USA.

Interactions among global change stressors and their effects at large scales are often proposed, but seldom evaluated. This situation is primarily due to lack of comprehensive, sufficiently long-term, and spatially extensive datasets. Seagrasses, which provide nursery habitat, improve water quality, and constitute a globally important carbon sink, are among the most vulnerable habitats on the planet. Here, we unite 31 years of high-resolution aerial monitoring and water quality data to elucidate the patterns and drivers of eelgrass (Zostera marina) abundance in Chesapeake Bay, USA, one of the largest and most valuable estuaries in the world, with an unparalleled history of regulatory efforts. We show that eelgrass area has declined 29% in total since 1991, with wide-ranging and severe ecological and economic consequences. We go on to identify an interaction between decreasing water clarity and warming temperatures as the primary drivers of this trend. Declining clarity has gradually reduced eelgrass cover the past two decades, primarily in deeper beds where light is already limiting. In shallow beds, however, reduced visibility exacerbates the physiological stress of acute warming, leading to recent instances of decline approaching 80%. While degraded water quality has long been known to influence underwater grasses worldwide, we demonstrate a clear and rapidly emerging interaction with climate change. We highlight the urgent need to integrate a broader perspective into local water quality management, in the Chesapeake Bay and in the many other coastal systems facing similar stressors.

Corrigendum: Assessing National Biodiversity Trends for Rocky and Coral Reefs through the Integration of Citizen Science and Scientific Monitoring Programs.

[This corrects the article DOI: 10.1093/biosci/biw180.].

Assessing National Biodiversity Trends for Rocky and Coral Reefs through the Integration of Citizen Science and Scientific Monitoring Programs.

Reporting progress against targets for international biodiversity agreements is hindered by a shortage of suitable biodiversity data. We describe a cost-effective system involving Reef Life Survey citizen scientists in the systematic collection of quantitative data covering multiple phyla that can underpin numerous marine biodiversity indicators at high spatial and temporal resolution. We then summarize the findings of a continental- and decadal-scale State of the Environment assessment for rocky and coral reefs based on indicators of ecosystem state relating to fishing, ocean warming, and invasive species and describing the distribution of threatened species. Fishing impacts are widespread, whereas substantial warming-related change affected some regions between 2005 and 2015. Invasive species are concentrated near harbors in southeastern Australia, and the threatened-species index is highest for the Great Australian Bight and Tasman Sea. Our approach can be applied globally to improve reporting against biodiversity targets and enhance public and policymakers' understanding of marine biodiversity trends.

Biodiversity mediates top-down control in eelgrass ecosystems: a global comparative-experimental approach.

Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom-up and top-down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass (Zostera marina) to quantify how top-down and bottom-up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top-down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross-site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large-scale patterns corresponded strikingly with prior small-scale experiments. Our results link global and local evidence that biodiversity and top-down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.

Multitrophic functional diversity predicts ecosystem functioning in experimental assemblages of estuarine consumers.

The use of functional traits to explain how biodiversity affects ecosystem functioning has attracted intense interest, yet few studies have a priori altered functional diversity, especially in multitrophic communities. Here, we manipulated multivariate functional diversity of estuarine grazers and predators within multiple levels of species richness to test how species richness and functional diversity predicted ecosystem functioning in a multitrophic food web. Community functional diversity was a better predictor than species richness for the majority of ecosystem properties, based on generalized linear mixed-effects models. Combining inferences from eight traits into a single multivariate index increased prediction accuracy of these models relative to any individual trait. Structural equation modeling revealed that functional diversity of both grazers and predators was important in driving final biomass within trophic levels, with stronger effects observed for predators. We also show that different species drove different ecosystem responses, with evidence for both sampling effects and complementarity. Our study extends experimental investigations of functional trait diversity to a multilevel food web, and demonstrates that functional diversity can be more accurate and effective than species richness in predicting community biomass in a food web context.

Physiological effects of diet mixing on consumer fitness: a meta-analysis.

The degree of dietary generalism among consumers has important consequences for population, community, and ecosystem processes, yet the effects on consumer fitness of mixing food types have not been examined comprehensively. We conducted a meta-analysis of 161 peer-reviewed studies reporting 493 experimental manipulations of prey diversity to test whether diet mixing enhances consumer fitness based on the intrinsic nutritional quality of foods and consumer physiology. Averaged across studies, mixed diets conferred significantly higher fitness than the average of single-species diets, but not the best single prey species. More than half of individual experiments, however, showed maximal growth and reproduction on mixed diets, consistent with the predicted benefits of a balanced diet. Mixed diets including chemically defended prey were no better than the average prey type, opposing the prediction that a diverse diet dilutes toxins. Finally, mixed-model analysis showed that the effect of diet mixing was stronger for herbivores than for higher trophic levels. The generally weak evidence for the nutritional benefits of diet mixing in these primarily laboratory experiments suggests that diet generalism is not strongly favored by the inherent physiological benefits of mixing food types, but is more likely driven by ecological and environmental influences on consumer foraging.

Can metabolic traits explain animal community assembly and functioning?

All animals on Earth compete for free energy, which is acquired, assimilated, and ultimately allocated to growth and reproduction. Competition is strongest within communities of sympatric, ecologically similar animals of roughly equal size (i.e. horizontal communities), which are often the focus of traditional community ecology. The replacement of taxonomic identities with functional traits has improved our ability to decipher the ecological dynamics that govern the assembly and functioning of animal communities. Yet, the use of low-resolution and taxonomically idiosyncratic traits in animals may have hampered progress to date. An animal's metabolic rate (MR) determines the costs of basic organismal processes and activities, thus linking major aspects of the multifaceted constructs of ecological niches (where, when, and how energy is obtained) and ecological fitness (how much energy is accumulated and passed on to future generations). We review evidence from organismal physiology to large-scale analyses across the tree of life to propose that MR gives rise to a group of meaningful functional traits - resting metabolic rate (RMR), maximum metabolic rate (MMR), and aerobic scope (AS) - that may permit an improved quantification of the energetic basis of species coexistence and, ultimately, the assembly and functioning of animal communities. Specifically, metabolic traits integrate across a variety of typical trait proxies for energy acquisition and allocation in animals (e.g. body size, diet, mobility, life history, habitat use), to yield a smaller suite of continuous quantities that: (1) can be precisely measured for individuals in a standardized fashion; and (2) apply to all animals regardless of their body plan, habitat, or taxonomic affiliation. While integrating metabolic traits into animal community ecology is neither a panacea to disentangling the nuanced effects of biological differences on animal community structure and functioning, nor without challenges, a small number of studies across different taxa suggest that MR may serve as a useful proxy for the energetic basis of competition in animals. Thus, the application of MR traits for animal communities can lead to a more general understanding of community assembly and functioning, enhance our ability to trace eco-evolutionary dynamics from genotypes to phenotypes (and vice versa), and help predict the responses of animal communities to environmental change. While trait-based ecology has improved our knowledge of animal communities to date, a more explicit energetic lens via the integration of metabolic traits may further strengthen the existing framework.

A wide megafauna gap undermines China's expanding coastal ecosystem conservation.

To fulfill sustainable development goals, many countries are expanding efforts to conserve ecologically and societally critical coastal ecosystems. Although megafauna profoundly affect the functioning of ecosystems, they are neglected as a key component in the conservation scheme for coastal ecosystems in many geographic contexts. We reveal a rich diversity of extant megafauna associated with all major types of coastal ecosystems in China, including 218 species of mammals, birds, reptiles, cephalopods, and fish across terrestrial and marine environments. However, 44% of these species are globally threatened, and 78% have not yet been assessed in China for extinction risk. More worrisome, 73% of these megafauna have not been designated as nationally protected species, and <10% of their most important habitats are protected. Filling this wide "megafauna gap" in China and globally would be a leading step as humanity strives to thrive with coastal ecosystems.

Herbivory limits success of vegetation restoration globally.

Restoring vegetation in degraded ecosystems is an increasingly common practice for promoting biodiversity and ecological function, but successful implementation is hampered by an incomplete understanding of the processes that limit restoration success. By synthesizing terrestrial and aquatic studies globally (2594 experimental tests from 610 articles), we reveal substantial herbivore control of vegetation under restoration. Herbivores at restoration sites reduced vegetation abundance more strongly (by 89%, on average) than those at relatively undegraded sites and suppressed, rather than fostered, plant diversity. These effects were particularly pronounced in regions with higher temperatures and lower precipitation. Excluding targeted herbivores temporarily or introducing their predators improved restoration by magnitudes similar to or greater than those achieved by managing plant competition or facilitation. Thus, managing herbivory is a promising strategy for enhancing vegetation restoration efforts.

Foundational biodiversity effects propagate through coastal food webs via multiple pathways.

Relatively few studies have attempted to resolve the pathways through which the effects of biodiversity on ecosystem functioning cascade from one trophic level to another. Here, we manipulated the richness of habitat-forming seaweeds in a western Atlantic estuary to explore how changes in foundation species diversity affect the structure and functioning of the benthic consumer communities that they support. Structural equation modeling revealed that macroalgal richness enhanced invertebrate abundance, biomass, and diversity, both directly by changing the quality and palatability of the foundational substrate and indirectly by increasing the total biomass of available habitat. Consumer responses were largely driven by a single foundational seaweed, although stronger complementarity among macroalgae was observed for invertebrate richness. These findings with diverse foundational phyla extend earlier inferences from terrestrial grasslands by showing that biodiversity effects can simultaneously propagate through multiple independent pathways to maintain animal foodwebs. Our work also highlights the potential ramifications of human-induced changes in marine ecosystems.