Oyster reef restoration fails to recoup global historic ecosystem losses despite substantial biodiversity gain.

Human activities have led to degradation of ecosystems globally. The lost ecosystem functions and services accumulate from the time of disturbance to the full recovery of the ecosystem and can be quantified as a "recovery debt," providing a valuable tool to develop better restoration practices that accelerate recovery and limit losses. Here, we quantified the recovery of faunal biodiversity and abundance toward a predisturbed state following structural restoration of oyster habitats globally. We found that while restoration initiates a rapid increase in biodiversity and abundance of reef-associated species within 2 years, recovery rate then decreases substantially, leaving a global shortfall in recovery of 35% below a predisturbed state. While efficient restoration methods boost recovery and minimize recovery shortfalls, the time to full recovery is yet to be quantified. Therefore, potential future coastal development should weigh up not only the instantaneous damage to ecosystem functions but also the potential for generational loss of services.

Persistence in a tropical transition zone? Sargassum forests alternate seasonal growth forms to maintain productivity in warming waters at the expense of annual biomass production.

Macroalgal forests provide productivity and biomass that underpins the function of many coastal ecosystems globally. The phenology of forests is seasonally driven by environmental conditions, with the environment-productivity relationship understood for most coastlines of the world. Climatic transition zones, however, have characteristics of temperate and tropical regions, creating large fluctuations in environmental conditions, and potentially limiting productivity and the persistence of macroalgal forests. The response of a forest-forming, dimorphic seaweed (Sargassum hemiphyllum) to seasonal temperature and light conditions in a rapidly warming tropical-temperate transitional zone (Hong Kong) was quantified by measuring in situ growth, net primary productivity (NPP), respiration, and photosynthetic potential. These physiological responses of S. hemiphyllum were then experimentally tested in response to changing temperatures (16.5-27 °C) and irradiances (20, 110, and 300 µmol m-2 s-1) in laboratory mesocosms. In contrast to predictions, S. hemiphyllum demonstrated asynchronous NPP and growth patterns, with growth maximized in cooler conditions but, counter-intuitively, highest photosynthetic rates in summer after annual senescence and dormancy were established. This discrepancy between peak photosynthetic rates and growth may provide regional populations of S. hemiphyllum the ability to survive higher temperatures in the near future, resisting the predicted range shifts under ocean warming. In contrast, warming is likely to drive a shorter growth season, longer dormancy, and reduced annual biomass production in bi-phasic seaweeds inhabiting climatic transition zones, potentially reducing system-wide productivity of these algal forests.

Live-fast-die-young: Carryover effects of heatwave-exposed adult urchins on the development of the next generation.

With rising ocean temperatures, extreme weather events such as marine heatwaves (MHWs) are increasing in frequency and duration, pushing marine life beyond their physiological limits. The potential to respond to extreme conditions through physiological acclimatization, and pass on resistance to the next generation, fundamentally depends on the capacity of an organism to cope within their thermal tolerance limits. To elucidate whether heat conditioning of parents could benefit offspring development, we exposed adult sea urchins (Heliocidaris erythrogramma) to ambient summer (23°C), moderate (25°C) or strong (26°C) MHW conditions for 10 days. Offspring were then reared at constant temperature along a thermal gradient (22-28°C) and development was tracked to the 14-day juvenile stage. Progeny from the MHW-conditioned adults developed through to metamorphosis faster than those of ambient conditioned parents, with most individuals from the moderate and strong heatwaves developing to the larval stage across all temperatures. In contrast, the majority of offspring from the control summer temperature died before metamorphosis at temperatures above 25°C (moderate MHW). Juveniles produced from the strong MHW-conditioned adults were also larger across all temperatures, with the largest juveniles in the 26°C treatment. In contrast, the smallest juveniles were from control (current-day summer) parents (and reared at 22 and 25°C). Surprisingly, initial survival was higher in the progeny of MHW exposed parents, even at temperatures hotter than predicted MHWs (28°C). Importantly, however, there was substantial mortality of juveniles from the strong MHW parents by day 14. Therefore, while carryover effects of parental conditioning to MHWs resulted in faster growing, larger progeny, this benefit will only persist beyond the more sensitive juvenile stage and enhance survival if conditions return promptly to normal seasonal temperatures within current thermal tolerance limits.

Predicting responses to marine heatwaves using functional traits.

Marine heatwaves (MHWs), discrete but prolonged periods of anomalously warm seawater, can fundamentally restructure marine communities and ecosystems. Although our understanding of these events has improved in recent years, key knowledge gaps hinder our ability to predict how MHWs will affect patterns of biodiversity. Here, we outline a functional trait approach that enables a better understanding of which species and communities will be most vulnerable to MHWs, and how the distribution of species and composition of communities are likely to shift through time. Our perspective allows progress toward unifying extreme events and longer term environmental trends as co-drivers of ecological change, with the incorporation of species traits into our predictions allowing for a greater capacity to make management decisions.

Capacity of an ecologically key urchin to recover from extreme events: Physiological impacts of heatwaves and the road to recovery.

Heatwaves are increasing in frequency and intensity, with substantial impacts on ecosystems and species which maintain their function. Whether or not species are harmed by heatwave conditions by being pushed beyond their physiological bounds can depend on whether energy replacement is sufficient to enable recovery from acute stress. We exposed an ecologically important sea urchin, Heliocidaris erythrogramma, to experimental marine heatwave scenarios in context with recent summer heat anomalies in moderate (25 °C), and strong heatwave (26 °C) conditions for 10 days, followed by a 10-day recovery period at normal summer temperature (23 °C). Greater heatwave intensity drove higher metabolic rates which were not matched with a concurrent increase in food consumption or faecal production. However, food consumption increased during the post-heatwave recovery period, likely to replenish an energy deficit. Despite this, mortality increased into the recovery period and seemed to be caused by latent effects, manifesting as a decline in health index as individuals progressed from spine and pedicellariae loss, through to loss of tube foot rigor, bald patch disease, culminating in mortality. We show for the first time that the acute thermal stress of heatwaves can have latent physiological effects that cause mortality even when conditions return to normal. Our results show that the negative effects of heatwaves can manifest after relief from stressful conditions and highlight the importance of understanding the latent effects on physiology and health. This understanding will offer insights into the long-term potential for stress recovery following seemingly sublethal effects and whether the restoration of ambient conditions post-heatwave is sufficient to ensure population stability.

Long-term thermal acclimation drives adaptive physiological adjustments of a marine gastropod to reduce sensitivity to climate change.

Ocean warming is predicted to challenge the persistence of a variety of marine organisms, especially when combined with ocean acidification. While temperature affects virtually all physiological processes, the extent to which thermal history mediates the adaptive capacity of marine organisms to climate change has been largely overlooked. Using populations of a marine gastropod (Turbo undulatus) with different thermal histories (cool vs. warm), we compared their physiological adjustments following exposure (8-week) to ocean acidification and warming. Compared to cool-acclimated counterparts, we found that warm-acclimated individuals had a higher thermal threshold (i.e. increased CTmax by 2 °C), which was unaffected by the exposure to ocean acidification and warming. Thermal history also strongly mediated physiological effects, where warm-acclimated individuals adjusted to warming by conserving energy, suggested by lower respiration and ingestion rates, energy budget (i.e. scope for growth) and O:N ratio. After exposure to warming, warm-acclimated individuals had higher metabolic rates and greater energy budget due to boosted ingestion rates, but such compensatory feeding disappeared when combined with ocean acidification. Overall, we suggest that thermal history can be a critical mediator of physiological performance under future climatic conditions. Given the relatively gradual rate of global warming, marine organisms may be better able to adaptively adjust their physiology to future climate than what short-term experiments currently convey.

Survived but not safe: Marine heatwave hinders metabolism in two gastropod survivors.

Marine heatwaves (MHWs) are an emerging threat to marine organisms that have increased in frequency and magnitude in the past decade. These extreme heating events can have differential impacts on organisms with some experiencing mortality while others survive. Here, we experimentally exposed two species of subtidal gastropod (Trochus sacellum and Astralium haematragum) to two realistic intensities of MHW to test the ability of different species to physiologically cope with extreme heating events. Extreme MHW conditions caused 100% mortality in both species within five days. While both species survived under moderate MHW conditions they showed evidence of nonadaptive metabolic depression. Both species demonstrated an inability to upregulate their metabolic rates at the higher temperatures following exposure to a MHW (i.e. reduced temperature of maximum metabolic rate; TMMR), suggesting a lack of molecular protective responses and ongoing physiological damage. Therefore, the physiological damage endured by heatwave survivors may lessen their ability to cope with subsequent stress until fully recovered. Repairing this damage may have serious repercussions for the rate of recovery of these normally resilient species and their ability to maintain their ecological functions post MHW, especially under the predicted increasing frequency, duration and magnitude of MHWs.

Ocean Acidification and Human Health.

The ocean provides resources key to human health and well-being, including food, oxygen, livelihoods, blue spaces, and medicines. The global threat to these resources posed by accelerating ocean acidification is becoming increasingly evident as the world's oceans absorb carbon dioxide emissions. While ocean acidification was initially perceived as a threat only to the marine realm, here we argue that it is also an emerging human health issue. Specifically, we explore how ocean acidification affects the quantity and quality of resources key to human health and well-being in the context of: (1) malnutrition and poisoning, (2) respiratory issues, (3) mental health impacts, and (4) development of medical resources. We explore mitigation and adaptation management strategies that can be implemented to strengthen the capacity of acidifying oceans to continue providing human health benefits. Importantly, we emphasize that the cost of such actions will be dependent upon the socioeconomic context; specifically, costs will likely be greater for socioeconomically disadvantaged populations, exacerbating the current inequitable distribution of environmental and human health challenges. Given the scale of ocean acidification impacts on human health and well-being, recognizing and researching these complexities may allow the adaptation of management such that not only are the harms to human health reduced but the benefits enhanced.

Linking energy budget to physiological adaptation: How a calcifying gastropod adjusts or succumbs to ocean acidification and warming.

Accelerating CO2 emissions have driven physico-chemical changes in the world's oceans, such as ocean acidification and warming. How marine organisms adjust or succumb to such environmental changes may be determined by their ability to balance energy intake against expenditure (i.e. energy budget) as energy supports physiological functions, including those with adaptive value. Here, we examined whether energy budget is a driver of physiological adaptability of marine calcifiers to the near-future ocean acidification and warming; i.e. how physiological energetics (respiration rate, feeding rate, energy assimilation and energy budget) relates to adjustments in shell growth and shell properties of a calcifying gastropod (Austrocochlea concamerata). We found that ocean warming boosted the energy budget of gastropods due to increased feeding rate, resulting in faster shell growth and greater shell strength (i.e. more mechanically resilient). When combined with ocean acidification, however, the gastropods had a substantial decrease in energy budget due to reduced feeding rate and energy assimilation, leading to the reduction in shell growth and shell strength. By linking energy budget to the adjustability of shell building, we revealed that energy availability can be critical to determine the physiological adaptability of marine calcifiers to the changing oceanic climate.

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.

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.

The duality of ocean acidification as a resource and a stressor.

Ecologically dominant species often define ecosystem states, but as human disturbances intensify, their subordinate counterparts increasingly displace them. We consider the duality of disturbance by examining how environmental drivers can simultaneously act as a stressor to dominant species and as a resource to subordinates. Using a model ecosystem, we demonstrate that CO2 -driven interactions between species can account for such reversals in dominance; i.e., the displacement of dominants (kelp forests) by subordinates (turf algae). We established that CO2 enrichment had a direct positive effect on productivity of turfs, but a negligible effect on kelp. CO2 enrichment further suppressed the abundance and feeding rate of the primary grazer of turfs (sea urchins), but had an opposite effect on the minor grazer (gastropods). Thus, boosted production of subordinate producers, exacerbated by a net reduction in its consumption by primary grazers, accounts for community change (i.e., turf displacing kelp). Ecosystem collapse, therefore, is more likely when resource enrichment alters competitive dominance of producers, and consumers fail to compensate. By recognizing such duality in the responses of interacting species to disturbance, which may stabilize or exacerbate change, we can begin to understand how intensifying human disturbances determine whether or not ecosystems undergo phase shifts.

Boosted nutritional quality of food by CO2 enrichment fails to offset energy demand of herbivores under ocean warming, causing energy depletion and mortality.

The CO2-boosted trophic transfer from primary producers to herbivores has been increasingly discovered at natural CO2 vents and in laboratory experiments. Despite the emerging knowledge of this boosting effect, we do not know the extent to which it may be enhanced or dampened by ocean warming. We investigated whether ocean acidification and warming enhance the nutritional quality (C:N ratio) and energy content of turf algae, which is speculated to drive higher feeding rate, greater energy budget and eventually faster growth of herbivores. This proposal was tested by observing the physiological (feeding rate, respiration rate and energy budget) and demographic responses (growth and survival) of a common grazing gastropod (Phasianella australis) to ocean acidification and warming in a 6-month mesocosm experiment. Whilst we observed the boosting effect of ocean acidification and warming in isolation on the energy budget of herbivores by either increasing feeding rate on the more nutritious algae or increasing energy gain per feeding effort, their growth and survival were reduced by the sublethal thermal stress under ocean warming, especially when both climate change stressors were combined. This reduced growth and survival occurred as a consequence of depleted energy reserves, suggesting that the boosting effect via trophic transfer might not sufficiently compensate for the increased energy demand imposed by ocean warming. In circumstances where ocean acidification and warming create an energy demand on herbivores that outweighs the energy enhancement of their food (i.e. primary producers), the performance of herbivores to control their blooming resources likely deteriorates and thus runaway primary production ensues.

Heatwaves diminish the survival of a subtidal gastropod through reduction in energy budget and depletion of energy reserves.

Extreme climatic events, such as heatwaves, are predicted to be more prevalent in future due to global climate change. The devastating impacts of heatwaves on the survival of marine organisms may be further intensified by ocean acidification. Here, we tested the hypothesis that prolonged exposure to heatwave temperatures (24 °C, +3 °C summer seawater temperature) would diminish energy budget, body condition and ultimately survival of a subtidal gastropod (Thalotia conica) by pushing close to its critical thermal maximum (CTmax). We also tested whether ocean acidification (pCO2: 1000 ppm) affects energy budget, CTmax and hence survival of this gastropod. Following the 8-week experimental period, mortality was markedly higher at 24 °C irrespective of pCO2 level, probably attributed to energy deficit (negative scope for growth) and concomitant depletion of energy reserves (reduced organ weight to flesh weight ratio). CTmax of T. conica appeared at 27 °C and was unaffected by ocean acidification. Our findings imply that prolonged exposure to heatwaves can compromise the survival of marine organisms below CTmax via disruption in energy homeostasis, which possibly explains their mass mortality in the past heatwave events. Therefore, heatwaves would have more profound effects than ocean acidification on future marine ecosystems.

Impacts of Near-Future Ocean Acidification and Warming on the Shell Mechanical and Geochemical Properties of Gastropods from Intertidal to Subtidal Zones.

Many marine organisms produce calcareous shells as the key structure for defense, but the functionality of shells may be compromised by ocean acidification and warming. Nevertheless, calcifying organisms may adaptively modify their shell properties in response to these impacts. Here, we examined how reduced pH and elevated temperature affect shell mechanical and geochemical properties of common grazing gastropods from intertidal to subtidal zones. Given the greater environmental fluctuations in the intertidal zone, we hypothesized that intertidal gastropods would exhibit more plastic responses in shell properties than subtidal gastropods. Overall, three out of five subtidal gastropods produced softer shells at elevated temperature, while intertidal gastropods maintained their shell hardness at both elevated pCO2 (i.e., reduced pH) and temperature. Regardless of pH and temperature, degree of crystallization was maintained (except one subtidal gastropod) and carbonate polymorph remained unchanged in all tested species. One intertidal gastropod produced less soluble shells (e.g., higher calcite/aragonite) in response to reduced pH. In contrast, subtidal gastropods produced only aragonite which has higher solubility than calcite. Overall, subtidal gastropods are expected to be more susceptible than intertidal gastropods to shell dissolution and physical damage under future seawater conditions. The increased vulnerability to shell dissolution and predation could have serious repercussions for their survival and ecological contributions in the future subtidal environment.

Ecological performance of construction materials subject to ocean climate change.

Artificial structures will be increasingly utilized to protect coastal infrastructure from sea-level rise and storms associated with climate change. Although it is well documented that the materials comprising artificial structures influence the composition of organisms that use them as habitat, little is known about how these materials may chemically react with changing seawater conditions, and what effects this will have on associated biota. We investigated the effects of ocean warming, acidification, and type of coastal infrastructure material on algal turfs. Seawater acidification resulted in greater covers of turf, though this effect was counteracted by elevated temperatures. Concrete supported a greater cover of turf than granite or high-density polyethylene (HDPE) under all temperature and pH treatments, with the greatest covers occurring under simulated ocean acidification. Furthermore, photosynthetic efficiency under acidification was greater on concrete substratum compared to all other materials and treatment combinations. These results demonstrate the capacity to maximise ecological benefits whilst still meeting local management objectives when engineering coastal defense structures by selecting materials that are appropriate in an ocean change context. Therefore, mitigation efforts to offset impacts from sea-level rise and storms can also be engineered to alter, or even reduce, the effects of climatic change on biological assemblages.

Conceptualizing ecosystem tipping points within a physiological framework.

Connecting the nonlinear and often counterintuitive physiological effects of multiple environmental drivers to the emergent impacts on ecosystems is a fundamental challenge. Unfortunately, the disconnect between the way "stressors" (e.g., warming) is considered in organismal (physiological) and ecological (community) contexts continues to hamper progress. Environmental drivers typically elicit biphasic physiological responses, where performance declines at levels above and below some optimum. It is also well understood that species exhibit highly variable response surfaces to these changes so that the optimum level of any environmental driver can vary among interacting species. Thus, species interactions are unlikely to go unaltered under environmental change. However, while these nonlinear, species-specific physiological relationships between environment and performance appear to be general, rarely are they incorporated into predictions of ecological tipping points. Instead, most ecosystem-level studies focus on varying levels of "stress" and frequently assume that any deviation from "normal" environmental conditions has similar effects, albeit with different magnitudes, on all of the species within a community. We consider a framework that realigns the positive and negative physiological effects of changes in climatic and nonclimatic drivers with indirect ecological responses. Using a series of simple models based on direct physiological responses to temperature and ocean pCO 2, we explore how variation in environment-performance relationships among primary producers and consumers translates into community-level effects via trophic interactions. These models show that even in the absence of direct mortality, mismatched responses resulting from often subtle changes in the physical environment can lead to substantial ecosystem-level change.

Species Interactions Drive Fish Biodiversity Loss in a High-CO2 World.

Accelerating climate change is eroding the functioning and stability of ecosystems by weakening the interactions among species that stabilize biological communities against change [1]. A key challenge to forecasting the future of ecosystems centers on how to extrapolate results from short-term, single-species studies to community-level responses that are mediated by key mechanisms such as competition, resource availability (bottom-up control), and predation (top-down control) [2]. We used CO2 vents as potential analogs of ocean acidification combined with in situ experiments to test current predictions of fish biodiversity loss and community change due to elevated CO2 [3] and to elucidate the potential mechanisms that drive such change. We show that high risk-taking behavior and competitive strength, combined with resource enrichment and collapse of predator populations, fostered already common species, enabling them to double their populations under acidified conditions. However, the release of these competitive dominants from predator control led to suppression of less common and subordinate competitors that did not benefit from resource enrichment and reduced predation. As a result, local biodiversity was lost and novel fish community compositions were created under elevated CO2. Our study identifies the species interactions most affected by ocean acidification, revealing potential sources of natural selection. We also reveal how diminished predator abundances can have cascading effects on local species diversity, mediated by complex species interactions. Reduced overfishing of predators could therefore act as a key action to stall diversity loss and ecosystem change in a high-CO2 world. VIDEO ABSTRACT.

Testing for thresholds of ecosystem collapse in seagrass meadows.

Although the public desire for healthy environments is clear-cut, the science and management of ecosystem health has not been as simple. Ecological systems can be dynamic and can shift abruptly from one ecosystem state to another. Such unpredictable shifts result when ecological thresholds are crossed; that is, small cumulative increases in an environmental stressor drive a much greater change than could be predicted from linear effects, suggesting an unforeseen tipping point is crossed. In coastal waters, broad-scale seagrass loss often occurs as a sudden event associated with human-driven nutrient enrichment (eutrophication). We tested whether the response of seagrass ecosystems to coastal nutrient enrichment is subject to a threshold effect. We exposed seagrass plots to different levels of nutrient enrichment (dissolved inorganic nitrogen) for 10 months and measured net production. Seagrass response exhibited a threshold pattern when nutrient enrichment exceeded moderate levels: there was an abrupt and large shift from positive to negative net leaf production (from approximately 0.04 leaf production to 0.02 leaf loss per day). Epiphyte load also increased as nutrient enrichment increased, which may have driven the shift in leaf production. Inadvertently crossing such thresholds, as can occur through ineffective management of land-derived inputs such as wastewater and stormwater runoff along urbanized coasts, may account for the widely observed sudden loss of seagrass meadows. Identification of tipping points may improve not only adaptive-management monitoring that seeks to avoid threshold effects, but also restoration approaches in systems that have crossed them.