Continent-wide declines in shallow reef life over a decade of ocean warming.

Human society is dependent on nature1,2, but whether our ecological foundations are at risk remains unknown in the absence of systematic monitoring of species' populations3. Knowledge of species fluctuations is particularly inadequate in the marine realm4. Here we assess the population trends of 1,057 common shallow reef species from multiple phyla at 1,636 sites around Australia over the past decade. Most populations decreased over this period, including many tropical fishes, temperate invertebrates (particularly echinoderms) and southwestern Australian macroalgae, whereas coral populations remained relatively stable. Population declines typically followed heatwave years, when local water temperatures were more than 0.5 °C above temperatures in 2008. Following heatwaves5,6, species abundances generally tended to decline near warm range edges, and increase near cool range edges. More than 30% of shallow invertebrate species in cool latitudes exhibited high extinction risk, with rapidly declining populations trapped by deep ocean barriers, preventing poleward retreat as temperatures rise. Greater conservation effort is needed to safeguard temperate marine ecosystems, which are disproportionately threatened and include species with deep evolutionary roots. Fundamental among such efforts, and broader societal needs to efficiently adapt to interacting anthropogenic and natural pressures, is greatly expanded monitoring of species' population trends7,8.

Research priorities for natural ecosystems in a changing global climate.

Climate change poses significant emerging risks to biodiversity, ecosystem function and associated socioecological systems. Adaptation responses must be initiated in parallel with mitigation efforts, but resources are limited. As climate risks are not distributed equally across taxa, ecosystems and processes, strategic prioritization of research that addresses stakeholder-relevant knowledge gaps will accelerate effective uptake into adaptation policy and management action. After a decade of climate change adaptation research within the Australian National Climate Change Adaptation Research Facility, we synthesize the National Adaptation Research Plans for marine, terrestrial and freshwater ecosystems. We identify the key, globally relevant priorities for ongoing research relevant to informing adaptation policy and environmental management aimed at maximizing the resilience of natural ecosystems to climate change. Informed by both global literature and an extensive stakeholder consultation across all ecosystems, sectors and regions in Australia, involving thousands of participants, we suggest 18 priority research topics based on their significance, urgency, technical and economic feasibility, existing knowledge gaps and potential for cobenefits across multiple sectors. These research priorities provide a unified guide for policymakers, funding organizations and researchers to strategically direct resources, maximize stakeholder uptake of resulting knowledge and minimize the impacts of climate change on natural ecosystems. Given the pace of climate change, it is imperative that we inform and accelerate adaptation progress in all regions around the world.

Global patterns of kelp forest change over the past half-century.

Kelp forests (Order Laminariales) form key biogenic habitats in coastal regions of temperate and Arctic seas worldwide, providing ecosystem services valued in the range of billions of dollars annually. Although local evidence suggests that kelp forests are increasingly threatened by a variety of stressors, no comprehensive global analysis of change in kelp abundances currently exists. Here, we build and analyze a global database of kelp time series spanning the past half-century to assess regional and global trends in kelp abundances. We detected a high degree of geographic variation in trends, with regional variability in the direction and magnitude of change far exceeding a small global average decline (instantaneous rate of change = -0.018 y-1). Our analysis identified declines in 38% of ecoregions for which there are data (-0.015 to -0.18 y-1), increases in 27% of ecoregions (0.015 to 0.11 y-1), and no detectable change in 35% of ecoregions. These spatially variable trajectories reflected regional differences in the drivers of change, uncertainty in some regions owing to poor spatial and temporal data coverage, and the dynamic nature of kelp populations. We conclude that although global drivers could be affecting kelp forests at multiple scales, local stressors and regional variation in the effects of these drivers dominate kelp dynamics, in contrast to many other marine and terrestrial foundation species.

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.

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.].

Climate-driven invasion and incipient warnings of kelp ecosystem collapse.

Climate change is progressively redistributing species towards the Earth's poles, indicating widespread potential for ecosystem collapse. Detecting early-warning-signals and enacting adaptation measures is therefore a key imperative for humanity. However, detecting early-warning signals has remained elusive and has focused on exceptionally high-frequency and/ or long-term time-series, which are generally unattainable for most ecosystems that are under-sampled and already impacted by warming. Here, we show that a catastrophic phase-shift in kelp ecosystems, caused by range-extension of an overgrazing sea urchin, also propagates poleward. Critically, we show that incipient spatial-pattern-formations of kelp overgrazing are detectable well-in-advance of collapse along temperate reefs in the ocean warming hotspot of south-eastern Australia. Demonstrating poleward progression of collapse over 15 years, these early-warning 'incipient barrens' are now widespread along 500 km of coast with projections indicating that half of all kelp beds within this range-extension region will collapse by ~2030. Overgrazing was positively associated with deep boulder-reefs, yet negatively associated with predatory lobsters and subordinate abalone competitors, which have both been intensively fished. Climate-driven collapse of ecosystems is occurring; however, by looking equatorward, space-for-time substitutions can enable practical detection of early-warning spatial-pattern-formations, allowing local climate adaptation measures to be enacted in advance.

Bio-physical determinants of sediment accumulation on an offshore coral reef: A snapshot study.

Sediments are found on all coral reefs around the globe. However, the amount of sediment in different reservoirs, and the rates at which sediments move between reservoirs, can shape the biological functioning of coral reefs. Unfortunately, relatively few studies have examined reef sediment dynamics, and associated bio-physical drivers, simultaneously over matching spatial and temporal scales. This has led to a partial understanding of how sediments and living reef systems are connected, especially on clear-water offshore reefs. To address this problem, four sediment reservoirs/sedimentary processes and three bio-physical drivers were quantified across seven different reef habitats/depths at Lizard Island, an exposed mid-shelf reef on the Great Barrier Reef. Even in this clear-water reef location a substantial load of suspended sediment passed over the reef; a load theoretically capable of replacing the entire standing stock of on-reef turf sediments in just 8 h. However, quantification of actual sediment deposition suggested that just 2 % of this passing sediment settled on the reef. The data also revealed marked spatial incongruence in sediment deposition (sediment trap data) and accumulation (TurfPod data) across the reef profile, with the flat and back reef emerging as key areas of both deposition and accumulation. By contrast, the shallow windward reef crest was an area of deposition but had a limited capacity for sediment accumulation. These cross-reef patterns related to wave energy and reef geomorphology, with low sediment accumulation on the ecologically important reef crest aligning with substantial wave energy. These findings reveal a disconnect between patterns of sediment deposition and accumulation on the benthos, with the 'post-settlement' fate of sediments dependent on local hydrodynamic conditions. From an ecological perspective, the data suggests key contextual constraints (wave energy and reef geomorphology) may predispose some reefs or reef areas to high-load turf sediment regimes.

Poleward bound: adapting to climate-driven species redistribution.

One of the most pronounced effects of climate change on the world's oceans is the (generally) poleward movement of species and fishery stocks in response to increasing water temperatures. In some regions, such redistributions are already causing dramatic shifts in marine socioecological systems, profoundly altering ecosystem structure and function, challenging domestic and international fisheries, and impacting on human communities. Such effects are expected to become increasingly widespread as waters continue to warm and species ranges continue to shift. Actions taken over the coming decade (2021-2030) can help us adapt to species redistributions and minimise negative impacts on ecosystems and human communities, achieving a more sustainable future in the face of ecosystem change. We describe key drivers related to climate-driven species redistributions that are likely to have a high impact and influence on whether a sustainable future is achievable by 2030. We posit two different futures-a 'business as usual' future and a technically achievable and more sustainable future, aligned with the Sustainable Development Goals. We then identify concrete actions that provide a pathway towards the more sustainable 2030 and that acknowledge and include Indigenous perspectives. Achieving this sustainable future will depend on improved monitoring and detection, and on adaptive, cooperative management to proactively respond to the challenge of species redistribution. We synthesise examples of such actions as the basis of a strategic approach to tackle this global-scale challenge for the benefit of humanity and ecosystems. Supplementary Information: The online version contains supplementary material available at 10.1007/s11160-021-09641-3.

Tracking widespread climate-driven change on temperate and tropical reefs.

Warming seas, marine heatwaves, and habitat degradation are increasingly widespread phenomena affecting marine biodiversity, yet our understanding of their broader impacts is largely derived from collective insights from independent localized studies. Insufficient systematic broadscale monitoring limits our understanding of the true extent of these impacts and our capacity to track these at scales relevant to national policies and international agreements. Using an extensive time series of co-located reef fish community structure and habitat data spanning 12 years and the entire Australian continent, we found that reef fish community responses to changing temperatures and habitats are dynamic and widespread but regionally patchy. Shifts in composition and abundance of the fish community often occurred within 2 years of environmental or habitat change, although the relative importance of these two mechanisms of climate impact tended to differ between tropical and temperate zones. The clearest of these changes on temperate and subtropical reefs were temperature related, with responses measured by the reef fish thermal index indicating reshuffling according to the thermal affinities of species present. On low latitude coral reefs, the community generalization index indicated shifting dominance of habitat generalist fishes through time, concurrent with changing coral cover. Our results emphasize the importance of maintaining local ecological detail when scaling up datasets to inform national policies and global biodiversity targets. Scaled-up ecological monitoring is needed to discriminate among increasingly diverse drivers of large-scale biodiversity change and better connect presently disjointed systems of biodiversity observation, indicator research, and governance.

Species richness and identity both determine the biomass of global reef fish communities.

Changing biodiversity alters ecosystem functioning in nature, but the degree to which this relationship depends on the taxonomic identities rather than the number of species remains untested at broad scales. Here, we partition the effects of declining species richness and changing community composition on fish community biomass across >3000 coral and rocky reef sites globally. We find that high biodiversity is 5.7x more important in maximizing biomass than the remaining influence of other ecological and environmental factors. Differences in fish community biomass across space are equally driven by both reductions in the total number of species and the disproportionate loss of larger-than-average species, which is exacerbated at sites impacted by humans. Our results confirm that sustaining biomass and associated ecosystem functions requires protecting diversity, most importantly of multiple large-bodied species in areas subject to strong human influences.

Knowledge Gaps in the Biology, Ecology, and Management of the Pacific Crown-of-Thorns Sea Star Acanthaster sp. on Australia's Great Barrier Reef.

AbstractCrown-of-thorns sea stars (Acanthaster sp.) are among the most studied coral reef organisms, owing to their propensity to undergo major population irruptions, which contribute to significant coral loss and reef degradation throughout the Indo-Pacific. However, there are still important knowledge gaps pertaining to the biology, ecology, and management of Acanthaster sp. Renewed efforts to advance understanding and management of Pacific crown-of-thorns sea stars (Acanthaster sp.) on Australia's Great Barrier Reef require explicit consideration of relevant and tractable knowledge gaps. Drawing on established horizon scanning methodologies, this study identified contemporary knowledge gaps by asking active and/or established crown-of-thorns sea star researchers to pose critical research questions that they believe should be addressed to improve the understanding and management of crown-of-thorns sea stars on the Great Barrier Reef. A total of 38 participants proposed 246 independent research questions, organized into 7 themes: feeding ecology, demography, distribution and abundance, predation, settlement, management, and environmental change. Questions were further assigned to 48 specific topics nested within the 7 themes. During this process, redundant questions were removed, which reduced the total number of distinct research questions to 172. Research questions posed were mostly related to themes of demography (46 questions) and management (48 questions). The dominant topics, meanwhile, were the incidence of population irruptions (16 questions), feeding ecology of larval sea stars (15 questions), effects of elevated water temperature on crown-of-thorns sea stars (13 questions), and predation on juveniles (12 questions). While the breadth of questions suggests that there is considerable research needed to improve understanding and management of crown-of-thorns sea stars on the Great Barrier Reef, the predominance of certain themes and topics suggests a major focus for new research while also providing a roadmap to guide future research efforts.

Genetic structure of a recent climate change-driven range extension.

The life-history strategies of some species make them strong candidates for rapid exploitation of novel habitat under new climate regimes. Some early-responding species may be considered invasive, and negatively impact on 'naïve' ecosystems. The barrens-forming sea urchin Centrostephanus rodgersii is one such species, having a high dispersal capability and a high-latitude range margin limited only by a developmental temperature threshold. Within this species' range in eastern Australian waters, sea temperatures have increased at greater than double the global average rate. The coinciding poleward range extension of C. rodgersii has caused major ecological changes, threatening reef biodiversity and fisheries productivity. We investigated microsatellite diversity and population structure associated with range expansion by this species. Generalized linear model analyses revealed no reduction in genetic diversity in the newly colonized region. A 'seascape genetics' analysis of genetic distances found no spatial genetic structure associated with the range extension. The distinctive genetic characteristic of the extension zone populations was reduced population-specific F(ST), consistent with very rapid population expansion. Demographic and genetic simulations support our inference of high connectivity between pre- and post-extension zones. Thus, the range shift appears to be a poleward extension of the highly-connected rangewide population of C. rodgersii. This is consistent with advection of larvae by the intensified warm water East Australian current, which has also increased Tasmanian Sea temperatures above the species' lower developmental threshold. Thus, ocean circulation changes have improved the climatic suitability of novel habitat for C. rodgersii and provided the supply of recruits necessary for colonization.

Remnant kelp bed refugia and future phase-shifts under ocean acidification.

Ocean warming, ocean acidification and overfishing are major threats to the structure and function of marine ecosystems. Driven by increasing anthropogenic emissions of CO2, ocean warming is leading to global redistribution of marine biota and altered ecosystem dynamics, while ocean acidification threatens the ability of calcifying marine organisms to form skeletons due to decline in saturation state of carbonate Ω and pH. In Tasmania, the interaction between overfishing of sea urchin predators and rapid ocean warming has caused a phase-shift from productive kelp beds to overgrazed sea urchin barren grounds, however potential impacts of ocean acidification on this system have not been considered despite this threat for marine ecosystems globally. Here we use automated loggers and point measures of pH, spanning kelp beds and barren grounds, to reveal that kelp beds have the capacity to locally ameliorate effects of ocean acidification, via photosynthetic drawdown of CO2, compared to unvegetated barren grounds. Based on meta-analysis of anticipated declines in physiological performance of grazing urchins to decreasing pH and assumptions of nil adaptation, future projection of OA across kelp-barrens transition zones reveals that kelp beds could act as important pH refugia, with urchins potentially becoming increasingly challenged at distances >40 m from kelp beds. Using spatially explicit simulation of physicochemical feedbacks between grazing urchins and their kelp prey, we show a stable mosaicked expression of kelp patches to emerge on barren grounds. Depending on the adaptative capacity of sea urchins, future declines in pH appear poised to further alter phase-shift dynamics for reef communities; thus, assessing change in spatial-patterning of reef-scapes may indicate cascading ecological impacts of ocean acidification.

Relationships between invertebrate benthos, environmental drivers and pollutants at a subcontinental scale.

Marine ecosystems are structured by an array of natural and anthropogenic drivers, their diverse influences varying between different community types and across space. We assessed consistency in variation in composition and richness for three communities (macro- and meio-faunal communities associated with macroalgae, and soft-sediment infaunal communities) across natural and pollution gradients at the subcontinental scale of southeastern Australia. Community structure varied with natural environmental factors (temperature, wave exposure) and, to a lesser extent, pollutant loads (catchment effects, heavy metals, hydrocarbons and nutrients) across 43 sites spanning 2700 km. The community types showed differing sensitivities to pollutants: algal macrofauna was most strongly associated with hydrocarbon pollution and nutrient loading; algal meiofauna with heavy metals and nutrients; and infauna with catchment effects and nutrients. Different taxonomic resolutions were needed to detect significant pollution relationships for the three community types, indicating that monitoring programmes are most effective if pollutant- and fauna-specific.

Understanding interactions between plasticity, adaptation and range shifts in response to marine environmental change.

Climate change is leading to shifts in species geographical distributions, but populations are also probably adapting to environmental change at different rates across their range. Owing to a lack of natural and empirical data on the influence of phenotypic adaptation on range shifts of marine species, we provide a general conceptual model for understanding population responses to climate change that incorporates plasticity and adaptation to environmental change in marine ecosystems. We use this conceptual model to help inform where within the geographical range each mechanism will probably operate most strongly and explore the supporting evidence in species. We then expand the discussion from a single-species perspective to community-level responses and use the conceptual model to visualize and guide research into the important yet poorly understood processes of plasticity and adaptation. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.

Body size and substrate type modulate movement by the western Pacific crown-of-thorns starfish, Acanthaster solaris.

The movement capacity of the crown-of-thorns starfishes (Acanthaster spp.) is a primary determinant of both their distribution and impact on coral assemblages. We quantified individual movement rates for the Pacific crown-of-thorns starfish (Acanthaster solaris) ranging in size from 75-480 mm total diameter, across three different substrates (sand, flat consolidated pavement, and coral rubble) on the northern Great Barrier Reef. The mean (±SE) rate of movement for smaller (<150 mm total diameter) A. solaris was 23.99 ± 1.02 cm/ min and 33.41 ± 1.49 cm/ min for individuals >350 mm total diameter. Mean (±SE) rates of movement varied with substrate type, being much higher on sand (36.53 ± 1.31 cm/ min) compared to consolidated pavement (28.04 ± 1.15 cm/ min) and slowest across coral rubble (17.25 ± 0.63 cm/ min). If average rates of movement measured here can be sustained, in combination with strong directionality, displacement distances of adult A. solaris could range from 250-520 m/ day, depending on the prevailing substrate. Sustained movement of A. solaris is, however, likely to be highly constrained by habitat heterogeneity, energetic constraints, resource availability, and diurnal patterns of activity, thereby limiting their capacity to move between reefs or habitats.

Phase-Shift Dynamics of Sea Urchin Overgrazing on Nutrified Reefs.

Shifts from productive kelp beds to impoverished sea urchin barrens occur globally and represent a wholesale change to the ecology of sub-tidal temperate reefs. Although the theory of shifts between alternative stable states is well advanced, there are few field studies detailing the dynamics of these kinds of transitions. In this study, sea urchin herbivory (a 'top-down' driver of ecosystems) was manipulated over 12 months to estimate (1) the sea urchin density at which kelp beds collapse to sea urchin barrens, and (2) the minimum sea urchin density required to maintain urchin barrens on experimental reefs in the urbanised Port Phillip Bay, Australia. In parallel, the role of one of the 'bottom-up' drivers of ecosystem structure was examined by (3) manipulating local nutrient levels and thus attempting to alter primary production on the experimental reefs. It was found that densities of 8 or more urchins m-2 (≥ 427 g m-2 biomass) lead to complete overgrazing of kelp beds while kelp bed recovery occurred when densities were reduced to ≤ 4 urchins m-2 (≤ 213 g m-2 biomass). This experiment provided further insight into the dynamics of transition between urchin barrens and kelp beds by exploring possible tipping-points which in this system can be found between 4 and 8 urchins m-2 (213 and 427 g m-2 respectively). Local enhancement of nutrient loading did not change the urchin density required for overgrazing or kelp bed recovery, as algal growth was not affected by nutrient enhancement.