Taxa-dependent temporal trends in the abundance and size of sea urchins in subtropical eastern Australia.

Subtropical reefs host a dynamic mix of tropical, subtropical, and temperate species that is changing due to shifts in the abundance and distribution of species in response to ocean warming. In these transitional communities, biogeographic affinity is expected to predict changes in species composition, with projected increases of tropical species and declines in cool-affinity temperate species. Understanding population dynamics of species along biogeographic transition zones is critical, especially for habitat engineers such as sea urchins that can facilitate ecosystem shifts through grazing. We investigated the population dynamics of sea urchins on coral-associated subtropical reefs at 7 sites in eastern Australia (28.196° S to 30.95° S) over 9 years (2010-2019), a period impacted by warming and heatwaves. Specifically, we investigated the density and population size structure of taxa with temperate (Centrostephanus rodgersii, Phyllacanthus parvispinus), subtropical (Tripneustes australiae) and tropical (Diadema spp.) affinities. Counter to expectation, biogeographic affinity did not explain shifts in species abundances in this region. Although we expected the abundance of tropical species to increase at their cold range boundaries, tropical Diadema species declined across all sites. The subtropical T. australiae also showed declines, while populations of the temperate C. rodgersii were remarkably stable throughout our study period. Our results show that temporal patterns of sea urchin populations in this region cannot be predicted by bio-geographic affinity alone and contribute critical information about the population dynamics of these important herbivores along this biogeographic transition zone.

Decadal demographic shifts and size-dependent disturbance responses of corals in a subtropical warming hotspot.

Long-term demographic studies at biogeographic transition zones can elucidate how body size mediates disturbance responses. Focusing on subtropical reefs in eastern Australia, we examine trends in the size-structure of corals with contrasting life-histories and zoogeographies surrounding the 2016 coral bleaching event (2010-2019) to determine their resilience and recovery capacity. We document demographic shifts, with disproportionate declines in the number of small corals and long-term persistence of larger corals. The incidence of bleaching (Pocillopora, Turbinaria) and partial mortality (Acropora, Pocillopora) increased with coral size, and bleached corals had greater risk of partial mortality. While endemic Pocillopora experienced marked declines, decadal stability of Turbinaria despite bleaching, coupled with abundance increase and bleaching resistance in Acropora indicate remarkable resilience of these taxa in the subtropics. Declines in the number of small corals and variable associations with environmental drivers indicate bottlenecks to recovery mediated by inhibitory effects of thermal extremes for Pocillopora (heat stress) and Acropora (heat and cold stress), and stimulatory effects of chlorophyll-a for Turbinaria. Although our study reveals signs of resilience, it foreshadows the vulnerability of subtropical corals to changing disturbance regimes that include marine heatwaves. Disparity in population dynamics suggest that subtropical reefs are ecologically distinct from tropical coral reefs.

The role of microbial biofilms in range shifts of marine habitat-forming organisms.

Marine species, such as corals and kelp, are responding to climate change by altering their distributions. Microbial biofilms underpin key processes that affect the establishment, maintenance, and function of these dominant habitat-formers. Climate-mediated changes to microbial biofilms can therefore strongly influence species' range shifts. Here, we review emerging research on the interactions between benthic biofilms and habitat-formers and identify two key areas of interaction where climate change can impact this dynamic: (i) via direct effects on biofilm composition, and (ii) via impacts on the complex feedback loops which exist between the biofilm microbes and habitat-forming organisms. We propose that these key interactions will be fundamental in driving the speed and extent of tropicalisation of coastal ecosystems under climate change.

Coral assemblages at higher latitudes favor short-term potential over long-term performance.

The persistent exposure of coral assemblages to more variable abiotic regimes is assumed to augment their resilience to future climatic variability. Yet, while the determinants of coral population resilience across species remain unknown, we are unable to predict the winners and losers across reef ecosystems exposed to increasingly variable conditions. Using annual surveys of 3171 coral individuals across Australia and Japan (2016-2019), we explore spatial variation across the short- and long-term dynamics of competitive, stress-tolerant, and weedy assemblages to evaluate how abiotic variability mediates the structural composition of coral assemblages. We illustrate how, by promoting short-term potential over long-term performance, coral assemblages can reduce their vulnerability to stochastic environments. However, compared to stress-tolerant, and weedy assemblages, competitive coral taxa display a reduced capacity for elevating their short-term potential. Accordingly, future climatic shifts threaten the structural complexity of coral assemblages in variable environments, emulating the degradation expected across global tropical reefs.

Regional and global climate risks for reef corals: Incorporating species-specific vulnerability and exposure to climate hazards.

Climate change is driving rapid and widespread erosion of the environmental conditions that formerly supported species persistence. Existing projections of climate change typically focus on forecasts of acute environmental anomalies and global extinction risks. The current projections also frequently consider all species within a broad taxonomic group together without differentiating species-specific patterns. Consequently, we still know little about the explicit dimensions of climate risk (i.e., species-specific vulnerability, exposure and hazard) that are vital for predicting future biodiversity responses (e.g., adaptation, migration) and developing management and conservation strategies. Here, we use reef corals as model organisms (n = 741 species) to project the extent of regional and global climate risks of marine organisms into the future. We characterise species-specific vulnerability based on the global geographic range and historical environmental conditions (1900-1994) of each coral species within their ranges, and quantify the projected exposure to climate hazard beyond the historical conditions as climate risk. We show that many coral species will experience a complete loss of pre-modern climate analogs at the regional scale and across their entire distributional ranges, and such exposure to hazardous conditions are predicted to pose substantial regional and global climate risks to reef corals. Although high-latitude regions may provide climate refugia for some tropical corals until the mid-21st century, they will not become a universal haven for all corals. Notably, high-latitude specialists and species with small geographic ranges remain particularly vulnerable as they tend to possess limited capacities to avoid climate risks (e.g., via adaptive and migratory responses). Predicted climate risks are amplified substantially under the SSP5-8.5 compared with the SSP1-2.6 scenario, highlighting the need for stringent emission controls. Our projections of both regional and global climate risks offer unique opportunities to facilitate climate action at spatial scales relevant to conservation and management.

Corals at the edge of environmental limits: A new conceptual framework to re-define marginal and extreme coral communities.

The worldwide decline of coral reefs has renewed interest in coral communities at the edge of environmental limits because they have the potential to serve as resilience hotspots and climate change refugia, and can provide insights into how coral reefs might function in future ocean conditions. These coral communities are often referred to as marginal or extreme but few definitions exist and usage of these terms has therefore been inconsistent. This creates significant challenges for categorising these often poorly studied communities and synthesising data across locations. Furthermore, this impedes our understanding of how coral communities can persist at the edge of their environmental limits and the lessons they provide for future coral reef survival. Here, we propose that marginal and extreme coral communities are related but distinct and provide a novel conceptual framework to redefine them. Specifically, we define coral reef extremeness solely based on environmental conditions (i.e., large deviations from optimal conditions in terms of mean and/or variance) and marginality solely based on ecological criteria (i.e., altered community composition and/or ecosystem functioning). This joint but independent assessment of environmental and ecological criteria is critical to avoid common pitfalls where coral communities existing outside the presumed optimal conditions for coral reef development are automatically considered inferior to coral reefs in more traditional settings. We further evaluate the differential potential of marginal and extreme coral communities to serve as natural laboratories, resilience hotspots and climate change refugia, and discuss strategies for their conservation and management as well as priorities for future research. Our new classification framework provides an important tool to improve our understanding of how corals can persist at the edge of their environmental limits and how we can leverage this knowledge to optimise strategies for coral reef conservation, restoration and management in a rapidly changing ocean.

No apparent trade-offs associated with heat tolerance in a reef-building coral.

As marine species adapt to climate change, their heat tolerance will likely be under strong selection. Yet trade-offs between heat tolerance and other life history traits could compromise natural adaptation or assisted evolution. This is particularly important for ecosystem engineers, such as reef-building corals, which support biodiversity yet are vulnerable to heatwave-induced mass bleaching and mortality. Here, we exposed 70 colonies of the reef-building coral Acropora digitifera to a long-term marine heatwave emulation experiment. We tested for trade-offs between heat tolerance and three traits measured from the colonies in situ - colony growth, fecundity, and symbiont community composition. Despite observing remarkable within-population variability in heat tolerance, all colonies were dominated by Cladocopium C40 symbionts. We found no evidence for trade-offs between heat tolerance and fecundity or growth. Contrary to expectations, positive associations emerged with growth, such that faster-growing colonies tended to bleach and die at higher levels of heat stress. Collectively, our results suggest that these corals exist on an energetic continuum where some high-performing individuals excel across multiple traits. Within populations, trade-offs between heat tolerance and growth or fecundity may not be major barriers to natural adaptation or the success of assisted evolution interventions.

Temperate functional niche availability not resident-invader competition shapes tropicalisation in reef fishes.

Temperate reefs are at the forefront of warming-induced community alterations resulting from poleward range shifts. This tropicalisation is exemplified and amplified by tropical species' invasions of temperate herbivory functions. However, whether other temperate ecosystem functions are similarly invaded by tropical species, and by what drivers, remains unclear. We examine tropicalisation footprints in nine reef fish functional groups using trait-based analyses and biomass of 550 fish species across tropical to temperate gradients in Japan and Australia. We discover that functional niches in transitional communities are asynchronously invaded by tropical species, but with congruent invasion schedules for functional groups across the two hemispheres. These differences in functional group tropicalisation point to habitat availability as a key determinant of multi-species range shifts, as in the majority of functional groups tropical and temperate species share functional niche space in suitable habitat. Competition among species from different thermal guilds played little part in limiting tropicalisation, rather available functional space occupied by temperate species indicates that tropical species can invade. Characterising these drivers of reef tropicalisation is pivotal to understanding, predicting, and managing marine community transformation.

Macroalgae exhibit diverse responses to human disturbances on coral reefs.

Scientists and managers rely on indicator taxa such as coral and macroalgal cover to evaluate the effects of human disturbance on coral reefs, often assuming a universally positive relationship between local human disturbance and macroalgae. Despite evidence that macroalgae respond to local stressors in diverse ways, there have been few efforts to evaluate relationships between specific macroalgae taxa and local human-driven disturbance. Using genus-level monitoring data from 1205 sites in the Indian and Pacific Oceans, we assess whether macroalgae percent cover correlates with local human disturbance while accounting for factors that could obscure or confound relationships. Assessing macroalgae at genus level revealed that no genera were positively correlated with all human disturbance metrics. Instead, we found relationships between the division or genera of algae and specific human disturbances that were not detectable when pooling taxa into a single functional category, which is common to many analyses. The convention to use percent cover of macroalgae as an indication of local human disturbance therefore likely obscures signatures of local anthropogenic threats to reefs. Our limited understanding of relationships between human disturbance, macroalgae taxa, and their responses to human disturbances impedes the ability to diagnose and respond appropriately to these threats.

SizeExtractR: A workflow for rapid reproducible extraction of object size metrics from scaled images.

Size is a biological characteristic that drives ecological processes from microscopic to geographic spatial scales, influencing cellular energetics, species fitness, population dynamics, and ecological interactions. Methods to measure size from images (e.g., proxies of body size, leaf area, and cell area) occur along a gradient from manual approaches to fully automated technologies (e.g., machine learning). These methods differ in terms of time investment, expertise required, and data or resource availability. While manual methods can improve accuracy through human recognition, they can be labor intensive, highlighting the need for semi-automated, and user-friendly software or workflows to increase the efficiency of manual techniques.Here, we present SizeExtractR, an open-source workflow that enables faster extraction of size metrics from scaled images (e.g., each image includes a ruler) using semi-automated protocols. It comprises a set of ImageJ macros to speed up size extraction and annotation, and an R-package for the quality control of annotations, data collation, calibration, and visualization.SizeExtractR extracts seven common size dimensions, including planar area, min/max diameter, and perimeter. Users can record additional categorical variables relating to their own study, for example species ID, by simply adding alphanumeric annotations to individual objects when prompted. Using a population size structure case study for hard corals as an example, we show how SizeExtractR was used to quantify the impact of mass coral bleaching on coral population dynamics. Lastly, the time saving benefit of using SizeExtractR was quantified during a series of timed image analyses, revealing up to a 49% reduction in image analysis time compared to a fully manual approach.SizeExtractR automatically archives results, allowing re-analysis of size extraction and promoting quality control and reproducibility. It has already been employed in marine and terrestrial sciences to assess population dynamics and demography, energy investment in eggs, and growth of nursery reared corals, with potential to be applied to a wide range of other research fields.

Photogrammetry as a tool to improve ecosystem restoration.

Ecosystem restoration has been practiced for over a century and is increasingly supported by the emergent applied science of restoration ecology. A prerequisite for successful ecosystem restoration is determining meaningful and measurable goals. This requires tools to monitor success in a standardized way. Photogrammetry uses images to reconstruct landscapes and organisms in three dimensions, enabling non-invasive measurement of key success indicators with unprecedented accuracy. We propose photogrammetry can improve restoration success by: (i) facilitating measurable goals; (ii) innovating and standardizing indicators of success; and (iii) standardizing monitoring. While the case we present is specific to coral reefs, photogrammetry has enormous potential to improve restoration practice in a wide range of ecosystems.

The projected degradation of subtropical coral assemblages by recurrent thermal stress.

Subtropical coral assemblages are threatened by similar extreme thermal stress events to their tropical counterparts. Yet, the mid- and long-term thermal stress responses of corals in subtropical environments remain largely unquantified, limiting our capacity to predict their future viability. The annual survival, growth and recruitment of 311 individual corals within the Solitary Islands Marine Park (Australia) was recorded over a 3-year period (2016-2018), including the 2015/2016 thermal stress event. These data were used to parameterise integral projection models quantifying the effect of thermal stress within a subtropical coral assemblage. Stochastic simulations were also applied to evaluate the implications of recurrent thermal stress scenarios predicted by four different Representative Concentration Pathways. We report differential shifts in population growth rates (λ) among coral populations during both stress and non-stress periods, confirming contrasting bleaching responses among taxa. However, even during non-stress periods, the observed dynamics for all taxa were unable to maintain current community composition, highlighting the need for external recruitment sources to support the community structure. Across all coral taxa, projected stochastic growth rates (λs ) were found to be lowest under higher emissions scenarios. Correspondingly, predicted increases in recurrent thermal stress regimes may accelerate the loss of coral coverage, species diversity and structural complexity within subtropical regions. We suggest that these trends are primarily due to the susceptibility of subtropical specialists and endemic species, such as Pocillopora aliciae, to thermal stress. Similarly, the viability of many tropical coral populations at higher latitudes is highly dependent on the persistence of up-current tropical systems. As such, the inherent dynamics of subtropical coral populations appear unable to support their future persistence under unprecedented thermal disturbance scenarios.

Refugia under threat: Mass bleaching of coral assemblages in high-latitude eastern Australia.

Environmental anomalies that trigger adverse physiological responses and mortality are occurring with increasing frequency due to climate change. At species' range peripheries, environmental anomalies are particularly concerning because species often exist at their environmental tolerance limits and may not be able to migrate to escape unfavourable conditions. Here, we investigated the bleaching response and mortality of 14 coral genera across high-latitude eastern Australia during a global heat stress event in 2016. We evaluated whether the severity of assemblage-scale and genus-level bleaching responses was associated with cumulative heat stress and/or local environmental history, including long-term mean temperatures during the hottest month of each year (SSTLTMAX ), and annual fluctuations in water temperature (SSTVAR ) and solar irradiance (PARZVAR ). The most severely-bleached genera included species that were either endemic to the region (Pocillopora aliciae) or rare in the tropics (e.g. Porites heronensis). Pocillopora spp., in particular, showed high rates of immediate mortality. Bleaching severity of Pocillopora was high where SSTLTMAX was low or PARZVAR was high, whereas bleaching severity of Porites was directly associated with cumulative heat stress. While many tropical Acropora species are extremely vulnerable to bleaching, the Acropora species common at high latitudes, such as A. glauca and A. solitaryensis, showed little incidence of bleaching and immediate mortality. Two other regionally-abundant genera, Goniastrea and Turbinaria, were also largely unaffected by the thermal anomaly. The severity of assemblage-scale bleaching responses was poorly explained by the environmental parameters we examined. Instead, the severity of assemblage-scale bleaching was associated with local differences in species abundance and taxon-specific bleaching responses. The marked taxonomic disparity in bleaching severity, coupled with high mortality of high-latitude endemics, point to climate-driven simplification of assemblage structures and progressive homogenisation of reef functions at these high-latitude locations.

Decommissioning of offshore oil and gas structures - Environmental opportunities and challenges.

Thousands of offshore oil and gas structures are approaching the end of their operating life globally, yet our understanding of the environmental effects of different decommissioning strategies is incomplete. Past focus on a narrow set of criteria has limited evaluation of decommissioning effects, restricting decommissioning options in most regions. We broadly review the environmental effects of decommissioning, analyse case studies, and outline analytical approaches that can advance our understanding of ecological dynamics on oil and gas structures. We find that ecosystem functions and services increase with the age of the structure and vary with geographical setting, such that decommissioning decisions need to take an ecosystem approach that considers their broader habitat and biodiversity values. Alignment of decommissioning assessment priorities among regulators and how they are evaluated, will reduce the likelihood of variable and sub-optimal decommissioning decisions. Ultimately, the range of allowable decommissioning options must be expanded to optimise the environmental outcomes of decommissioning across the broad range of ecosystems in which platforms are located.

Local and regional controls of phylogenetic structure at the high-latitude range limits of corals.

Understanding how range-edge populations will respond to climate change is an urgent research priority. Here, we used a phylogenetic community ecology approach to examine how ecological and evolutionary processes shape biodiversity patterns of scleractinian corals at their high-latitude range limits in eastern Australia. We estimated phylogenetic signal in seven ecologically important functional traits and conducted tests of phylogenetic structure at local and regional scales using the net relatedness (NRI) and nearest taxon indices (NTI) for the presence/absence and abundance data. Regional tests showed light phylogenetic clustering, indicating that coral species found in this subtropical-to-temperate transition zone are more closely related to each other than are species on the nearby, more northerly Great Barrier Reef. Local tests revealed variable patterns of phylogenetic clustering and overdispersion and higher than expected phylogenetic turnover among sites. In combination, these results are broadly consistent with the hierarchical filtering model, whereby species pass through a regional climatic filter based on their tolerances for marginal conditions and subsequently segregate into local assemblages according to the relative strength of habitat filtering and species interactions. Conservatism of tested traits suggests that corals will likely track their niches with climate change. Nevertheless, high turnover of lineages among sites indicates that range shifts will probably vary among species and highlights the vulnerability and conservation significance of high-latitude reefs.

Global warming and recurrent mass bleaching of corals.

During 2015-2016, record temperatures triggered a pan-tropical episode of coral bleaching, the third global-scale event since mass bleaching was first documented in the 1980s. Here we examine how and why the severity of recurrent major bleaching events has varied at multiple scales, using aerial and underwater surveys of Australian reefs combined with satellite-derived sea surface temperatures. The distinctive geographic footprints of recurrent bleaching on the Great Barrier Reef in 1998, 2002 and 2016 were determined by the spatial pattern of sea temperatures in each year. Water quality and fishing pressure had minimal effect on the unprecedented bleaching in 2016, suggesting that local protection of reefs affords little or no resistance to extreme heat. Similarly, past exposure to bleaching in 1998 and 2002 did not lessen the severity of bleaching in 2016. Consequently, immediate global action to curb future warming is essential to secure a future for coral reefs.

Trait-mediated environmental filtering drives assembly at biogeographic transition zones.

Abiotic filtering is a major driver of gradients in the structure and functioning of ecosystems from the tropics to the poles. It is thus likely that environmental filtering is an important assembly process at the transition of biogeographical zones where many species occur at their range limits. Shifts in species abundances and association patterns along environmental gradients can be indicative of environmental filtering, which is predicted to be stronger in areas of high abiotic stress and to promote increased similarity of ecological characteristics among co-occurring species. Here we test these hypotheses for scleractinian corals along a broad latitudinal gradient in high-latitude eastern Australia, where corals occur at the margins of their ranges and environmental tolerances. We quantify variation in taxonomic, zoogeographic, and functional patterns combined with null model approaches and demonstrate systematic spatial variation in community structure and significant covariance of species abundance distributions and functional characteristics along the latitudinal gradient. We describe a strong biogeographic transition zone, consistent with patterns expected under abiotic filtering, whereby species are sorted along the latitudinal gradient according to their tolerances for marginal reef conditions. High-latitude coastal reefs are typified by widely distributed, generalist, stress-tolerant coral species with massive and horizontally spreading morphologies and by diminishing influence of tropical taxa at higher latitudes and closer to the mainland. Higher degree of ecological similarity among co-occurring species than expected by chance supports the environmental filtering hypothesis. Among individual traits, the structural traits corallite size and colony morphology were filtered most strongly, suggesting that characteristics linked to energy acquisition and physical stability may be particularly important for coral survival in high-latitude environments. These findings highlight interspecific differences and species interactions with the environment as key drivers of community organization in biogeographic transition zones and support the hypothesis that environmental filters play a stronger role than biotic interactions in structuring ecological communities in areas of high abiotic stress.