Protecting the global ocean for biodiversity, food and climate.

The ocean contains unique biodiversity, provides valuable food resources and is a major sink for anthropogenic carbon. Marine protected areas (MPAs) are an effective tool for restoring ocean biodiversity and ecosystem services1,2, but at present only 2.7% of the ocean is highly protected3. This low level of ocean protection is due largely to conflicts with fisheries and other extractive uses. To address this issue, here we developed a conservation planning framework to prioritize highly protected MPAs in places that would result in multiple benefits today and in the future. We find that a substantial increase in ocean protection could have triple benefits, by protecting biodiversity, boosting the yield of fisheries and securing marine carbon stocks that are at risk from human activities. Our results show that most coastal nations contain priority areas that can contribute substantially to achieving these three objectives of biodiversity protection, food provision and carbon storage. A globally coordinated effort could be nearly twice as efficient as uncoordinated, national-level conservation planning. Our flexible prioritization framework could help to inform both national marine spatial plans4 and global targets for marine conservation, food security and climate action.

Environmental variables drive spatial patterns of trophic diversity in mammals.

Understanding environmental drivers of species diversity has become increasingly important under climate change. Different trophic groups (predators, omnivores and herbivores) interact with their environments in fundamentally different ways and may therefore be influenced by different environmental drivers. Using random forest models, we identified drivers of terrestrial mammals' total and proportional species richness within trophic groups at a global scale. Precipitation seasonality was the most important predictor of richness for all trophic groups. Richness peaked at intermediate precipitation seasonality, indicating that moderate levels of environmental heterogeneity promote mammal richness. Gross primary production (GPP) was the most important correlate of the relative contribution of each trophic group to total species richness. The strong relationship with GPP demonstrates that basal-level resource availability influences how diversity is structured among trophic groups. Our findings suggest that environmental characteristics that influence resource temporal variability and abundance are important predictors of terrestrial mammal richness at a global scale.

Herbivory changes soil microbial communities and greenhouse gas fluxes in a high-latitude wetland.

Herbivory can have strong impacts on greenhouse gas fluxes in high-latitude ecosystems. For example, in the Yukon-Kuskokwim (Y-K) Delta in western Alaska, migratory goose grazing affects the magnitude of soil carbon dioxide (CO2) and methane (CH4) fluxes. However, the underlying drivers of this relationship are unclear, as few studies systematically tease apart the processes by which herbivores influences soil biogeochemistry. To examine these mechanisms in detail, we conducted a laboratory incubation experiment to quantify changes in greenhouse gas fluxes in response to three parameters altered by herbivores in situ: temperature, soil moisture content, and nutrient inputs. These treatments were applied to soils collected in grazing lawns and nearby ungrazed habitat, allowing us to assess how variation in microbial community structure influenced observed responses. We found pronounced differences in both fungal and prokaryotic community composition between grazed and ungrazed areas. In the laboratory incubation experiment, CO2 and CH4 fluxes increased with temperature, soil moisture, and goose fecal addition, suggesting that grazing-related changes in the soil abiotic environment may enhance soil C losses. Yet, these abiotic drivers were insufficient to explain variation in fluxes between soils with and without prior grazing. Differences in trace gas fluxes between grazed and ungrazed areas may result both from herbivore-induced shifts in abiotic parameters and grazing-related alterations in microbial community structure. Our findings suggest that relationships among herbivores and soil microbial communities could mediate carbon-climate feedbacks in rapidly changing high-latitude ecosystems.

Metal concentrations in wetland plant tissues influences transfer to terrestrial food webs.

Wetland plants tolerate potentially hazardous metals through a variety of strategies, including exclusion or accumulation. Whether plants sequester metals and where they store them in their tissues is important for understanding the potential role of plants as remediators or vectors of metals to terrestrial food webs. Here we evaluate metal sequestration in Great Salt Lake wetlands for one invasive (Phragmites australis; phragmites) and three native plant species, i.e. threesquare bulrush (Schoenoplectus americanus), hardstem bulrush (Schoenoplectus acutus), alkali bulrush (Bolboschoenus maritimus), and their terrestrial invertebrates. We observed higher concentrations of arsenic and copper than other metals in plant tissues, although high lead concentrations were observed in phragmites. All plants acted as excluders of arsenic and selenium, retaining the bulk of the metal mass in belowground tissues. In contrast, lead, copper, and cadmium were transferred to above ground tissues of hardstem bulrush and phragmites. The aboveground translocation facilitated the movement of these metals into invertebrates, with the highest concentrations in most cases found in predators. Though our results highlight the potential for metal remediation via wetland plant growth and removal, care should be taken to ensure that remediation efforts do not lead to bioaccumulation.

Marine reserves shape seascapes on scales visible from space.

Marine reserves can effectively restore harvested populations, and 'mega-reserves' increasingly protect large tracts of ocean. However, no method exists of monitoring ecological responses at this large scale. Herbivory is a key mechanism structuring ecosystems, and this consumer-resource interaction's strength on coral reefs can indicate ecosystem health. We screened 1372, and measured features of 214, reefs throughout Australia's Great Barrier Reef using high-resolution satellite imagery, combined with remote underwater videography and assays on a subset, to quantify the prevalence, size and potential causes of 'grazing halos'. Halos are known to be seascape-scale footprints of herbivory and other ecological interactions. Here we show that these halo-like footprints are more prevalent in reserves, particularly older ones (approx. 40 years old), resulting in predictable changes to reef habitat at scales visible from space. While the direct mechanisms for this pattern are relatively clear, the indirect mechanisms remain untested. By combining remote sensing and behavioural ecology, our findings demonstrate that reserves can shape large-scale habitat structure by altering herbivores' functional importance, suggesting that reserves may have greater value in restoring ecosystems than previously appreciated. Additionally, our results show that we can now detect macro-patterns in reef species interactions using freely available satellite imagery. Low-cost, ecosystem-level observation tools will be critical as reserves increase in number and scope; further investigation into whether halos may help seems warranted. Significance statement: Marine reserves are a widely used tool to mitigate fishing impacts on marine ecosystems. Predicting reserves' large-scale effects on habitat structure and ecosystem functioning is a major challenge, however, because these effects unfold over longer and larger scales than most ecological studies. We use a unique approach merging remote sensing and behavioural ecology to detect ecosystem change within reserves in Australia's vast Great Barrier Reef. We find evidence of changes in reefs' algal habitat structure occurring over large spatial (thousands of kilometres) and temporal (40+ years) scales, demonstrating that reserves can alter herbivory and habitat structure in predictable ways. This approach demonstrates that we can now detect aspects of reefs' ecological responses to protection even in remote and inaccessible reefs globally.

Landscape heterogeneity strengthens the relationship between ß-diversity and ecosystem function.

Consensus has emerged in the literature that increased biodiversity enhances the capacity of ecosystems to perform multiple functions. However, most biodiversity/ecosystem function studies focus on a single ecosystem, or on landscapes of homogenous ecosystems. Here, we investigate how increased landscape-level environmental dissimilarity may affect the relationship between different metrics of diversity (α, ß, or γ) and ecosystem function. We produced a suite of simulated landscapes, each of which contained four experimental outdoor aquatic mesocosms. Differences in temperature and nutrient conditions of the mesocosms allowed us to simulate landscapes containing a range of within-landscape environmental heterogeneities. We found that the variation in ecosystem functions was primarily controlled by environmental conditions, with diversity metrics accounting for a smaller (but significant) amount of variation in function. When landscapes were more homogeneous, α, ß, and γ diversity was not associated with differences in primary production, and only γ was associated with changes in decomposition. In these homogeneous landscapes, differences in these two ecosystem functions were most strongly related to nutrient and temperature conditions in the ecosystems. However, as landscape-level environmental dissimilarity increased, the relationship between α, ß, or γ and ecosystem functions strengthened, with ß being a greater predictor of variation in decomposition at the highest levels of environmental dissimilarity than α or γ. We propose that when all ecosystems in a landscape have similar environmental conditions, species sorting is likely to generate a single community composition that is well suited to those environmental conditions, ß is low, and the efficiency of diversity-ecosystem function couplings is similar across communities. Under this low ß, the effect of abiotic conditions on ecosystem function will be most apparent. However, when environmental conditions vary among ecosystems, species sorting pressures are different among ecosystems, producing different communities among locations in a landscape. These conditions lead to stronger relationships between ß and the magnitude of ecosystem functions. Our results illustrate that abiotic conditions and the homogeneity of communities influence ecosystem function expressed at the landscape scale.

Ocean acidification alters zooplankton communities and increases top-down pressure of a cubozoan predator.

The composition of local ecological communities is determined by the members of the regional community that are able to survive the abiotic and biotic conditions of a local ecosystem. Anthropogenic activities since the industrial revolution have increased atmospheric CO2 concentrations, which have in turn decreased ocean pH and altered carbonate ion concentrations: so called ocean acidification (OA). Single-species experiments have shown how OA can dramatically affect zooplankton development, physiology and skeletal mineralization status, potentially reducing their defensive function and altering their predatory and antipredatory behaviors. This means that increased OA may indirectly alter the biotic conditions by modifying trophic interactions. We investigated how OA affects the impact of a cubozoan predator on their zooplankton prey, predominantly Copepoda, Pleocyemata, Dendrobranchiata, and Amphipoda. Experimental conditions were set at either current (pCO2 370 µatm) or end-of-the-century OA (pCO2 1,100 µatm) scenarios, crossed in an orthogonal experimental design with the presence/absence of the cubozoan predator Carybdea rastoni. The combined effects of exposure to OA and predation by C. rastoni caused greater shifts in community structure, and greater reductions in the abundance of key taxa than would be predicted from combining the effect of each stressor in isolation. Specifically, we show that in the combined presence of OA and a cubozoan predator, populations of the most abundant member of the zooplankton community (calanoid copepods) were reduced 27% more than it would be predicted based on the effects of these stressors in isolation, suggesting that OA increases the susceptibility of plankton to predation. Our results indicate that the ecological consequences of OA may be greater than predicted from single-species experiments, and highlight the need to understand future marine global change from a community perspective.

Trophic-level dependent effects on CO2 emissions from experimental stream ecosystems.

Concern over accelerating rates of species invasions and losses have initiated investigations into how local and global changes to predator abundance mediate trophic cascades that influence CO2 fluxes of aquatic ecosystems. However, to date, no studies have investigated how species additions or losses at other consumer trophic levels influence the CO2 flux of aquatic ecosystems. In this study, we added a large predatory stonefly, detritivorous stonefly, or grazer tadpole to experimental stream food webs and over a 70-day period quantified their effects on community composition, leaf litter decomposition, chlorophyll-a concentrations, and stream CO2 emissions. In general, streams where the large grazer or large detritivore were added showed no change in total invertebrate biomass, leaf litter loss, chlorophyll-a concentrations, or stream CO2 emissions compared with controls; although we did observe a spike in CO2 emissions in the large grazer treatment following a substantial reduction in chlorophyll-a concentrations on day 28. However, the large grazer and large detritivore altered the community composition of streams by reducing the densities of other grazer and detritivore taxa, respectively, compared with controls. Conversely, the addition of the large predator created trophic cascades that reduced total invertebrate biomass and increased primary producer biomass. The cascading effects of the predator additions on the food web ultimately led to decreased CO2 emissions from stream channels by up to 95%. Our results suggest that stream ecosystem processes were more influenced by changes in large predator abundance than large grazer or detritivore abundance, because of a lack of functionally similar large predators. Our study demonstrates that the presence/absence of species with unique functional roles may have consequences for the exchange of CO2 between the ecosystem and the atmosphere.

Competitive displacement alters top-down effects on carbon dioxide concentrations in a freshwater ecosystem.

Climate change and invasive species have the potential to alter species diversity, creating novel species interactions. Interspecific competition and facilitation between predators may either enhance or dampen trophic cascades, ultimately influencing total predator effects on communities and biogeochemical cycling of ecosystems. However, previous studies have only investigated the effects of a single predator species on CO2 flux of aquatic ecosystems. In this study, we measured and compared the individual and joint effects of predatory damselfly larvae and diving beetles on total prey biomass, leaf litter processing, and dissolved CO2 concentrations of experimental bromeliad ecosystems. Damselfly larvae created strong trophic cascades that reduced CO2 concentrations by ~46% relative to no-predator treatments. Conversely, the effects of diving beetles on prey biomass, leaf litter processing, and dissolved CO2 were not statistically different to no-predator treatments. Relative to multiplicative null models, the presence of damselfly larvae and diving beetles together resulted in antagonistic relations that eliminated trophic cascades and top-down influences on CO2 concentrations. Furthermore, we showed that the antagonistic interactions between predators occurred due to a tactile response that culminated in competitive displacement of damselfly larvae. Our results demonstrate that predator identity and predator-predator interactions can influence CO2 concentrations of an aquatic ecosystem. We suggest that predator effects on CO2 fluxes may depend on the particular predator species removed or added to the ecosystem and their interactions with other predators.

Herbivores at the highest risk of extinction among mammals, birds, and reptiles.

As a result of their extensive home ranges and slow population growth rates, predators have often been perceived to suffer higher risks of extinction than other trophic groups. Our study challenges this extinction-risk paradigm by quantitatively comparing patterns of extinction risk across different trophic groups of mammals, birds, and reptiles. We found that trophic level and body size were significant factors that influenced extinction risk in all taxa. At multiple spatial and temporal scales, herbivores, especially herbivorous reptiles and large-bodied herbivores, consistently have the highest proportions of threatened species. This observed elevated extinction risk for herbivores is ecologically consequential, given the important roles that herbivores are known to play in controlling ecosystem function.

Protecting endangered species in the USA requires both public and private land conservation.

Crucial to the successful conservation of endangered species is the overlap of their ranges with protected areas. We analyzed protected areas in the continental USA to assess the extent to which they covered the ranges of endangered tetrapods. We show that in 80% of ecoregions, protected areas offer equal (25%) or worse (55%) protection for species than if their locations were chosen at random. Additionally, we demonstrate that it is possible to achieve sufficient protection for 100% of the USA's endangered tetrapods through targeted protection of undeveloped public and private lands. Our results highlight that the USA is likely to fall short of its commitments to halting biodiversity loss unless more considerable investments in both public and private land conservation are made.

Extreme rainfall events alter the trophic structure in bromeliad tanks across the Neotropics.

Changes in global and regional precipitation regimes are among the most pervasive components of climate change. Intensification of rainfall cycles, ranging from frequent downpours to severe droughts, could cause widespread, but largely unknown, alterations to trophic structure and ecosystem function. We conducted multi-site coordinated experiments to show how variation in the quantity and evenness of rainfall modulates trophic structure in 210 natural freshwater microcosms (tank bromeliads) across Central and South America (18°N to 29°S). The biomass of smaller organisms (detritivores) was higher under more stable hydrological conditions. Conversely, the biomass of predators was highest when rainfall was uneven, resulting in top-heavy biomass pyramids. These results illustrate how extremes of precipitation, resulting in localized droughts or flooding, can erode the base of freshwater food webs, with negative implications for the stability of trophic dynamics.

Ecological response to altered rainfall differs across the Neotropics.

There is growing recognition that ecosystems may be more impacted by infrequent extreme climatic events than by changes in mean climatic conditions. This has led to calls for experiments that explore the sensitivity of ecosystems over broad ranges of climatic parameter space. However, because such response surface experiments have so far been limited in geographic and biological scope, it is not clear if differences between studies reflect geographic location or the ecosystem component considered. In this study, we manipulated rainfall entering tank bromeliads in seven sites across the Neotropics, and characterized the response of the aquatic ecosystem in terms of invertebrate functional composition, biological stocks (total invertebrate biomass, bacterial density) and ecosystem fluxes (decomposition, carbon, nitrogen). Of these response types, invertebrate functional composition was the most sensitive, even though, in some sites, the species pool had a high proportion of drought-tolerant families. Total invertebrate biomass was universally insensitive to rainfall change because of statistical averaging of divergent responses between functional groups. The response of invertebrate functional composition to rain differed between geographical locations because (1) the effect of rainfall on bromeliad hydrology differed between sites, and invertebrates directly experience hydrology not rainfall and (2) the taxonomic composition of some functional groups differed between sites, and families differed in their response to bromeliad hydrology. These findings suggest that it will be difficult to establish thresholds of "safe ecosystem functioning" when ecosystem components differ in their sensitivity to climatic variables, and such thresholds may not be broadly applicable over geographic space. In particular, ecological forecast horizons for climate change may be spatially restricted in systems where habitat properties mediate climatic impacts, and those, like the tropics, with high spatial turnover in species composition.

Ecosystem Function and Services of Aquatic Predators in the Anthropocene.

Arguments for the need to conserve aquatic predator (AP) populations often focus on the ecological and socioeconomic roles they play. Here, we summarize the diverse ecosystem functions and services connected to APs, including regulating food webs, cycling nutrients, engineering habitats, transmitting diseases/parasites, mediating ecological invasions, affecting climate, supporting fisheries, generating tourism, and providing bioinspiration. In some cases, human-driven declines and increases in AP populations have altered these ecosystem functions and services. We present a social ecological framework for supporting adaptive management decisions involving APs in response to social and environmental change. We also identify outstanding questions to guide future research on the ecological functions and ecosystem services of APs in a changing world.

The future of Blue Carbon science.

The term Blue Carbon (BC) was first coined a decade ago to describe the disproportionately large contribution of coastal vegetated ecosystems to global carbon sequestration. The role of BC in climate change mitigation and adaptation has now reached international prominence. To help prioritise future research, we assembled leading experts in the field to agree upon the top-ten pending questions in BC science. Understanding how climate change affects carbon accumulation in mature BC ecosystems and during their restoration was a high priority. Controversial questions included the role of carbonate and macroalgae in BC cycling, and the degree to which greenhouse gases are released following disturbance of BC ecosystems. Scientists seek improved precision of the extent of BC ecosystems; techniques to determine BC provenance; understanding of the factors that influence sequestration in BC ecosystems, with the corresponding value of BC; and the management actions that are effective in enhancing this value. Overall this overview provides a comprehensive road map for the coming decades on future research in BC science.

Author Correction: The future of Blue Carbon science.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.