Life goes on: Spatial heterogeneity promotes biodiversity in an urbanized coastal marine ecosystem.

Both human populations and marine biodiversity are concentrated along coastlines, with growing conservation interest in how these ecosystems can survive intense anthropogenic impacts. Tropical urban centres provide valuable research opportunities because these megacities are often adjacent to mega-diverse coral reef systems. The Pearl River Delta is a prime exemplar, as it encompasses one of the most densely populated and impacted regions in the world and is located just northwest of the Coral Triangle. However, the spatial and taxonomic complexity of this biodiversity, most of which is small, cryptic in habitat and poorly known, make comparative analyses challenging. We deployed standardized settlement structures at seven sites differing in the intensity of human impacts and used COI metabarcoding to characterize benthic biodiversity, with a focus on metazoans. We found a total of 7184 OTUs, with an average of 665 OTUs per sampling unit; these numbers exceed those observed in many previous studies using comparable methods, despite the location of our study in an urbanized environment. Beta diversity was also high, with 52% of the OTUs found at just one site. As expected, we found that the sites close to point sources of pollution had substantially lower diversity (44% less) relative to sites bathed in less polluted oceanic waters. However, the polluted sites contributed substantially to the total animal diversity of the region, with 25% of all OTUs occurring only within polluted sites. Further analysis of Arthropoda, Annelida and Mollusca showed that phylogenetic clustering within a site was common, suggesting that environmental filtering reduced biodiversity to a subset of lineages present within the region, a pattern that was most pronounced in polluted sites and for the Arthropoda. The water quality gradients surrounding the PRD highlight the unique role of in situ studies for understanding the impacts of complex urbanization pressures on biodiversity.

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.

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.

Climate-driven disparities among ecological interactions threaten kelp forest persistence.

The combination of ocean warming and acidification brings an uncertain future to kelp forests that occupy the warmest parts of their range. These forests are not only subject to the direct negative effects of ocean climate change, but also to a combination of unknown indirect effects associated with changing ecological landscapes. Here, we used mesocosm experiments to test the direct effects of ocean warming and acidification on kelp biomass and photosynthetic health, as well as climate-driven disparities in indirect effects involving key consumers (urchins and rock lobsters) and competitors (algal turf). Elevated water temperature directly reduced kelp biomass, while their turf-forming competitors expanded in response to ocean acidification and declining kelp canopy. Elevated temperatures also increased growth of urchins and, concurrently, the rate at which they thinned kelp canopy. Rock lobsters, which are renowned for keeping urchin populations in check, indirectly intensified negative pressures on kelp by reducing their consumption of urchins in response to elevated temperature. Overall, these results suggest that kelp forests situated towards the low-latitude margins of their distribution will need to adapt to ocean warming in order to persist in the future. What is less certain is how such adaptation in kelps can occur in the face of intensifying consumptive (via ocean warming) and competitive (via ocean acidification) pressures that affect key ecological interactions associated with their persistence. If such indirect effects counter adaptation to changing climate, they may erode the stability of kelp forests and increase the probability of regime shifts from complex habitat-forming species to more simple habitats dominated by algal turfs.

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.

Mineralogical Plasticity Acts as a Compensatory Mechanism to the Impacts of Ocean Acidification.

Calcifying organisms are considered particularly susceptible to the future impacts of ocean acidification (OA), but recent evidence suggests that they may be able to maintain calcification and overall fitness. The underlying mechanism remains unclear but may be attributed to mineralogical plasticity, which modifies the energetic cost of calcification. To test the hypothesis that mineralogical plasticity enables the maintenance of shell growth and functionality under OA conditions, we assessed the biological performance of a gastropod (respiration rate, feeding rate, somatic growth, and shell growth of Austrocochlea constricta) and analyzed its shell mechanical and geochemical properties (shell hardness, elastic modulus, amorphous calcium carbonate, calcite to aragonite ratio, and magnesium to calcium ratio). Despite minor metabolic depression and no increase in feeding rate, shell growth was faster under OA conditions, probably due to increased precipitation of calcite and trade-offs against inner shell density. In addition, the resulting shell was functionally suitable for increasingly "corrosive" oceans, i.e., harder and less soluble shells. We conclude that mineralogical plasticity may act as a compensatory mechanism to maintain overall performance of calcifying organisms under OA conditions and could be a cornerstone of calcifying organisms to acclimate to and maintain their ecological functions in acidifying oceans.

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.

Ocean acidification: Linking science to management solutions using the Great Barrier Reef as a case study.

Coral reefs are one of the most vulnerable ecosystems to ocean acidification. While our understanding of the potential impacts of ocean acidification on coral reef ecosystems is growing, gaps remain that limit our ability to translate scientific knowledge into management action. To guide solution-based research, we review the current knowledge of ocean acidification impacts on coral reefs alongside management needs and priorities. We use the world's largest continuous reef system, Australia's Great Barrier Reef (GBR), as a case study. We integrate scientific knowledge gained from a variety of approaches (e.g., laboratory studies, field observations, and ecosystem modelling) and scales (e.g., cell, organism, ecosystem) that underpin a systems-level understanding of how ocean acidification is likely to impact the GBR and associated goods and services. We then discuss local and regional management options that may be effective to help mitigate the effects of ocean acidification on the GBR, with likely application to other coral reef systems. We develop a research framework for linking solution-based ocean acidification research to practical management options. The framework assists in identifying effective and cost-efficient options for supporting ecosystem resilience. The framework enables on-the-ground OA management to be the focus, while not losing sight of CO2 mitigation as the ultimate solution.

Trophic compensation reinforces resistance: herbivory absorbs the increasing effects of multiple disturbances.

Disturbance often results in small changes in community structure, but the probability of transitioning to contrasting states increases when multiple disturbances combine. Nevertheless, we have limited insights into the mechanisms that stabilise communities, particularly how perturbations can be absorbed without restructuring (i.e. resistance). Here, we expand the concept of compensatory dynamics to include countervailing mechanisms that absorb disturbances through trophic interactions. By definition, 'compensation' occurs if a specific disturbance stimulates a proportional countervailing response that eliminates its otherwise unchecked effect. We show that the compounding effects of disturbances from local to global scales (i.e. local canopy-loss, eutrophication, ocean acidification) increasingly promote the expansion of weedy species, but that this response is countered by a proportional increase in grazing. Finally, we explore the relatively unrecognised role of compensatory effects, which are likely to maintain the resistance of communities to disturbance more deeply than current thinking allows.

Ocean acidification through the lens of ecological theory.

Ocean acidification, chemical changes to the carbonate system of seawater, is emerging as a key environmental challenge accompanying global warming and other human-induced perturbations. Considerable research seeks to define the scope and character of potential outcomes from this phenomenon, but a crucial impediment persists. Ecological theory, despite its power and utility, has been only peripherally applied to the problem. Here we sketch in broad strokes several areas where fundamental principles of ecology have the capacity to generate insight into ocean acidification's consequences. We focus on conceptual models that, when considered in the context of acidification, yield explicit predictions regarding a spectrum of population- and community-level effects, from narrowing of species ranges and shifts in patterns of demographic connectivity, to modified consumer-resource relationships, to ascendance of weedy taxa and loss of species diversity. Although our coverage represents only a small fraction of the breadth of possible insights achievable from the application of theory, our hope is that this initial foray will spur expanded efforts to blend experiments with theoretical approaches. The result promises to be a deeper and more nuanced understanding of ocean acidification'and the ecological changes it portends.

Escaping herbivory: ocean warming as a refuge for primary producers where consumer metabolism and consumption cannot pursue.

Ocean warming is anticipated to strengthen the persistence of turf-forming habitat, yet the concomitant elevation of grazer metabolic rates may accelerate per capita rates of consumption to counter turf predominance. Whilst this possibility of strong top-down control is supported by the metabolic theory of ecology (MTE), it assumes that consumer metabolism and consumption keep pace with increasing production. This assumption was tested by quantifying the metabolic rates of turfs and herbivorous gastropods under a series of elevated temperatures in which the ensuing production and consumption were observed. We discovered that as temperature increases towards near-future levels (year 2100), consumption rates of gastropods peak earlier than the rate of growth of producers. Hence, turfs have greater capacity to persist under near-future temperatures than the capacity for herbivores to counter their growth. These results suggest that whilst MTE predicts stronger top-down control, understanding whether consumer-producer responses are synchronous is key to assessing the future strength of top-down control.

Discovery of the mineral brucite (magnesium hydroxide) in the tropical calcifying alga Polystrata dura (Peyssonneliales, Rhodophyta).

Red algae of the family Peyssonneliaceae typically form thin crusts impregnated with aragonite. Here, we report the first discovery of brucite in a thick red algal crust (~1 cm) formed by the peyssonnelioid species Polystrata dura from Papua New Guinea. Cells of P. dura were found to be infilled by the magnesium-rich mineral brucite [Mg(OH)2 ]; minor amounts of magnesite and calcite were also detected. We propose that cell infill may be associated with the development of thick (> ~5 mm) calcified red algal crusts, integral components of tropical biotic reefs. If brucite infill within the P. dura crust enhances resistance to dissolution similarly to crustose coralline algae that infill with dolomite, then these crusts would be more resilient to future ocean acidification than crusts without infill.

Seagrass response to CO2 contingent on epiphytic algae: indirect effects can overwhelm direct effects.

Increased availability of dissolved CO2 in the ocean can enhance the productivity and growth of marine plants such as seagrasses and algae, but realised benefits may be contingent on additional conditions (e.g. light) that modify biotic interactions between these plant groups. The combined effects of future CO2 and differing light on the growth of seagrass and their algal epiphytes were tested by maintaining juvenile seagrasses Amphibolis antarctica under three different CO2 concentrations representing ambient, moderate future and high future forecasts (i.e. 390, 650 vs. 900 µl l(-1)) and two light levels representing low and high PAR (i.e. 43 vs. 167 µmol m(-2) s(-1)). Aboveground and belowground biomass, leaf growth, epiphyte cover, tissue chemistry and photosynthetic parameters of seagrasses were measured. At low light, there was a neutral to positive effect of elevated CO2 on seagrass biomass and growth; at high light, this effect of CO2 switched toward negative, as growth and biomass decreased at the highest CO2 level. These opposing responses to CO2 appeared to be closely linked to the overgrowth of seagrass by filamentous algal epiphytes when high light and CO2 were combined. Importantly, all seagrass plants maintained positive leaf growth throughout the experiment, indicating that growth was inhibited by some experimental conditions but not arrested entirely. Therefore, while greater light or elevated CO2 provided direct physiological benefits for seagrasses, such benefits were likely negated by overgrowth of epiphytic algae when greater light and CO2 were combined. This result demonstrates how indirect ecological effects from epiphytes can modify independent physiological predictions for seagrass associated with global change.

Population dynamics can be more important than physiological limits for determining range shifts under climate change.

Evidence is accumulating that species' responses to climate changes are best predicted by modelling the interaction of physiological limits, biotic processes and the effects of dispersal-limitation. Using commercially harvested blacklip (Haliotis rubra) and greenlip abalone (Haliotis laevigata) as case studies, we determine the relative importance of accounting for interactions among physiology, metapopulation dynamics and exploitation in predictions of range (geographical occupancy) and abundance (spatially explicit density) under various climate change scenarios. Traditional correlative ecological niche models (ENM) predict that climate change will benefit the commercial exploitation of abalone by promoting increased abundances without any reduction in range size. However, models that account simultaneously for demographic processes and physiological responses to climate-related factors result in future (and present) estimates of area of occupancy (AOO) and abundance that differ from those generated by ENMs alone. Range expansion and population growth are unlikely for blacklip abalone because of important interactions between climate-dependent mortality and metapopulation processes; in contrast, greenlip abalone should increase in abundance despite a contraction in AOO. The strongly non-linear relationship between abalone population size and AOO has important ramifications for the use of ENM predictions that rely on metrics describing change in habitat area as proxies for extinction risk. These results show that predicting species' responses to climate change often require physiological information to understand climatic range determinants, and a metapopulation model that can make full use of this data to more realistically account for processes such as local extirpation, demographic rescue, source-sink dynamics and dispersal-limitation.

Contrasting resource limitations of marine primary producers: implications for competitive interactions under enriched CO2 and nutrient regimes.

Primary producers rarely exist under their ideal conditions, with key processes often limited by resource availability. As human activities modify environmental conditions, and therefore resource availability, some species may be released from these limitations while others are not, potentially disrupting community structure. In order to examine the limitations experienced by algal functional groups that characterise alternate community structures (i.e. turf-forming algae and canopy-forming kelp), we exposed these groups to contemporary and enriched levels of carbon dioxide (CO2) and nutrients. Turfs responded to the individual enrichment of both CO2 and nutrients, with the greatest shift in the biomass and carbon:nitrogen (C:N) ratios observed under their combined enrichment. In contrast, kelp responded to enriched nutrients, but not enriched CO2. We hypothesise that the differing limitations reflect the contrasting physiologies of these functional groups, specifically their methods of C acquisition, such as the possession and/or efficiency of a carbon concentrating mechanism (CCM). Importantly, our results reveal that these functional groups, whose interactions structure entire communities, experience distinct resource limitations, with some potentially limited by a single type of resource (i.e. kelp by nutrients), while others may be co-limited (i.e. turf by CO2 and nutrients). Consequently, the identification of how alternate conditions modify resource availability and limitations may facilitate anticipation of the future sustainability of major ecosystem components and the communities they support.

Temperate and tropical brown macroalgae thrive, despite decalcification, along natural CO2 gradients.

Predicting the impacts of ocean acidification on coastal ecosystems requires an understanding of the effects on macroalgae and their grazers, as these underpin the ecology of rocky shores. Whilst calcified coralline algae (Rhodophyta) appear to be especially vulnerable to ocean acidification, there is a lack of information concerning calcified brown algae (Phaeophyta), which are not obligate calcifiers but are still important producers of calcium carbonate and organic matter in shallow coastal waters. Here, we compare ecological shifts in subtidal rocky shore systems along CO2 gradients created by volcanic seeps in the Mediterranean and Papua New Guinea, focussing on abundant macroalgae and grazing sea urchins. In both the temperate and tropical systems the abundances of grazing sea urchins declined dramatically along CO2 gradients. Temperate and tropical species of the calcifying macroalgal genus Padina (Dictyoaceae, Phaeophyta) showed reductions in CaCO3 content with CO2 enrichment. In contrast to other studies of calcified macroalgae, however, we observed an increase in the abundance of Padina spp. in acidified conditions. Reduced sea urchin grazing pressure and significant increases in photosynthetic rates may explain the unexpected success of decalcified Padina spp. at elevated levels of CO2 . This is the first study to provide a comparison of ecological changes along CO2 gradients between temperate and tropical rocky shores. The similarities we found in the responses of Padina spp. and sea urchin abundance at several vent systems increases confidence in predictions of the ecological impacts of ocean acidification over a large geographical range.

Predicting ecosystem shifts requires new approaches that integrate the effects of climate change across entire systems.

Most studies that forecast the ecological consequences of climate change target a single species and a single life stage. Depending on climatic impacts on other life stages and on interacting species, however, the results from simple experiments may not translate into accurate predictions of future ecological change. Research needs to move beyond simple experimental studies and environmental envelope projections for single species towards identifying where ecosystem change is likely to occur and the drivers for this change. For this to happen, we advocate research directions that (i) identify the critical species within the target ecosystem, and the life stage(s) most susceptible to changing conditions and (ii) the key interactions between these species and components of their broader ecosystem. A combined approach using macroecology, experimentally derived data and modelling that incorporates energy budgets in life cycle models may identify critical abiotic conditions that disproportionately alter important ecological processes under forecasted climates.

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.

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.

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.