Current extent and future opportunities for living shorelines in Australia.

Living shorelines aim to enhance the resilience of coastlines to hazards while simultaneously delivering co-benefits such as carbon sequestration. Despite the potential ecological and socio-economic benefits of living shorelines over conventional engineered coastal protection structures, application is limited globally. Australia has a long and diverse coastline that provides prime opportunities for living shorelines using beaches and dunes, vegetation, and biogenic reefs, which may be either natural ('soft' approach) or with an engineered structural component ('hybrid' approach). Published scientific studies, however, have indicated limited use of living shorelines for coastal protection in Australia. In response, we combined a national survey and interviews of coastal practitioners and a grey and peer-reviewed literature search to (1) identify barriers to living shoreline implementation; and (2) create a database of living shoreline projects in Australia based on sources other than scientific literature. Projects included were those that had either a primary or secondary goal of protection of coastal assets from erosion and/or flooding. We identified 138 living shoreline projects in Australia through the means sampled starting in 1970; with the number of projects increasing through time particularly since 2000. Over half of the total projects (59 %) were considered to be successful according to their initial stated objective (i.e., reducing hazard risk) and 18 % of projects could not be assessed for their success based on the information available. Seventy percent of projects received formal or informal monitoring. Even in the absence of peer-reviewed support for living shoreline construction in Australia, we discovered local and regional increases in their use. This suggests that coastal practitioners are learning on-the-ground, however more generally it was stated that few examples of living shorelines are being made available, suggesting a barrier in information sharing among agencies at a broader scale. A database of living shoreline projects can increase knowledge among practitioners globally to develop best practice that informs technical guidelines for different approaches and helps focus attention on areas for further research.

The cycle of seagrass life: From flowers to new meadows.

Understanding sexual reproduction and recruitment in seagrasses is crucial to their conservation and restoration. Flowering, seed production, seed recruitment, and seedling establishment data for the seagrass Posidonia australis was collected annually between 2013 and 2018 in meadows at six locations around Rottnest Island, Western Australia. Variable annual rates of flowering and seed production were observed among meadows between northern and southern sides of the island and among years. Meadows on the northern shore consistently flowered more intensely and produced more seeds across the years of the survey. Inter-site variation in clonal diversity and size of clones, seed production, wind and surface currents during pollen and seed release, and the large, but variable, impact of seed predation are likely the principal drivers of successful recruitment into established meadows and in colonizing unvegetated sands. The prolific but variable annual reproductive investment increases the probability of low levels of continuous recruitment from seed in this seagrass, despite high rates of abiotic and biotic disturbance at seedling, shoot, and patch scales. This strategy also imparts a level of ecological resilience to this long-lived and persistent species.

Marine heatwave and reduced light scenarios cause species-specific metabolomic changes in seagrasses under ocean warming.

Climate change and extreme climatic events, such as marine heatwaves (MHWs), are threatening seagrass ecosystems. Metabolomics can be used to gain insight into early stress responses in seagrasses and help to develop targeted management and conservation measures. We used metabolomics to understand the temporal and mechanistic response of leaf metabolism in seagrasses to climate change. Two species, temperate Posidonia australis and tropical Halodule uninervis, were exposed to a combination of future warming, simulated MHW with subsequent recovery period, and light deprivation in a mesocosm experiment. The leaf metabolome of P. australis was altered under MHW exposure at ambient light while H. uninervis was unaffected. Light deprivation impacted both seagrasses, with combined effects of heat and low light causing greater alterations in leaf metabolism. There was no MHW recovery in P. australis. Conversely, the heat-resistant leaf metabolome of H. uninervis showed recovery of sugars and intermediates of the tricarboxylic acid cycle under combined heat and low light exposure, suggesting adaptive strategies to long-term light deprivation. Overall, this research highlights how metabolomics can be used to study the metabolic pathways of seagrasses, identifies early indicators of environmental stress and analyses the effects of environmental factors on plant metabolism and health.

Back to the wild: movements of a juvenile tiger shark released from a public aquarium.

Sharks are an important attraction for aquaria; however, larger species can rarely be kept indefinitely. To date, there has been little work tracking shark movements post-release to the wild. The authors used high-resolution biologgers to monitor a sub-adult tiger shark's pre- and post-release fine-scale movements following 2 years of captivity in an aquarium. They also compared its movement with that of a wild shark tagged nearby. Despite the differences in movement between the two sharks, with vertical oscillations notably absent and greater levels of turning seen from the released shark, the captive shark survived the release. These biologgers improve insight into post-release movements of captive sharks.

Sulfide intrusion in a habitat forming seagrass can be predicted from relative abundance of sulfur cycling genes in sediments.

Sulfide intrusion from sediments is an increasingly recognized contributor to seagrass declines globally, yet the relationship between sediment microorganisms and sulfide intrusion has received little attention. Here, we use metagenomic sequencing and stable isotope (34S) analysis to examine this relationship in Cockburn Sound, Australia, a seagrass-dominated embayment with a gradient of sulfide stress and seagrass declines. There was a significant positive relationship between sulfide intrusion into seagrasses and sulfate reduction genes in sediment microbial communities, which was greatest at sites with long term seagrass declines. This is the first demonstration of a significant link between sulfur cycling genes present in seagrass sediments and sulfide intrusion in a habitat-forming seagrass that is experiencing long-term shoot density decline. Given that microorganisms respond rapidly to environmental change, the quantitative links established in this study can be used as a potential management tool to enable the prediction of sulfide stress on large habitat forming seagrasses; a global issue expected to worsen with climate change.

Cable bacteria at oxygen-releasing roots of aquatic plants: a widespread and diverse plant-microbe association.

Cable bacteria are sulfide-oxidising, filamentous bacteria that reduce toxic sulfide levels, suppress methane emissions and drive nutrient and carbon cycling in sediments. Recently, cable bacteria have been found associated with roots of aquatic plants and rice (Oryza sativa). However, the extent to which cable bacteria are associated with aquatic plants in nature remains unexplored. Using newly generated and public 16S rRNA gene sequence datasets combined with fluorescence in situ hybridisation, we investigated the distribution of cable bacteria around the roots of aquatic plants, encompassing seagrass (including seagrass seedlings), rice, freshwater and saltmarsh plants. Diverse cable bacteria were found associated with roots of 16 out of 28 plant species and at 36 out of 55 investigated sites, across four continents. Plant-associated cable bacteria were confirmed across a variety of ecosystems, including marine coastal environments, estuaries, freshwater streams, isolated pristine lakes and intensive agricultural systems. This pattern indicates that this plant-microbe relationship is globally widespread and neither obligate nor species specific. The occurrence of cable bacteria in plant rhizospheres may be of general importance to vegetation vitality, primary productivity, coastal restoration practices and greenhouse gas balance of rice fields and wetlands.

Cutting out the middle clam: lucinid endosymbiotic bacteria are also associated with seagrass roots worldwide.

Seagrasses and lucinid bivalves inhabit highly reduced sediments with elevated sulphide concentrations. Lucinids house symbiotic bacteria (Ca. Thiodiazotropha) capable of oxidising sediment sulphide, and their presence in sediments has been proposed to promote seagrass growth by decreasing otherwise phytotoxic sulphide levels. However, vast and productive seagrass meadows are present in ecosystems where lucinids do not occur. Hence, we hypothesised that seagrasses themselves host these sulphur-oxidising Ca. Thiodiazotropha that could aid their survival when lucinids are absent. We analysed newly generated and publicly available 16S rRNA gene sequences from seagrass roots and sediments across 14 seagrass species and 10 countries and found that persistent and colonising seagrasses across the world harbour sulphur-oxidising Ca. Thiodiazotropha, regardless of the presence of lucinids. We used fluorescence in situ hybridisation to visually confirm the presence of Ca. Thiodiazotropha on roots of Halophila ovalis, a colonising seagrass species with wide geographical, water depth range, and sedimentary sulphide concentrations. We provide the first evidence that Ca. Thiodiazotropha are commonly present on seagrass roots, providing another mechanism for seagrasses to alleviate sulphide stress globally.

Too hot to handle: Unprecedented seagrass death driven by marine heatwave in a World Heritage Area.

The increased occurrence of extreme climate events, such as marine heatwaves (MHWs), has resulted in substantial ecological impacts worldwide. To date, metrics of thermal stress within marine systems have focussed on coral communities, and less is known about measuring stress relevant to other primary producers, such as seagrasses. An extreme MHW occurred across the Western Australian coastline in the austral summer of 2010-2011, exposing marine communities to summer seawater temperatures 2-5°C warmer than average. Using a combination of satellite imagery and in situ assessments, we provide detailed maps of seagrass coverage across the entire Shark Bay World Heritage Area (ca. 13,000 km2 ) before (2002 and 2010) and after the MHW (2014 and 2016). Our temporal analysis of these maps documents the single largest loss in dense seagrass extent globally (1,310 km2 ) following an acute disturbance. Total change in seagrass extent was spatially heterogeneous, with the most extensive declines occurring in the Western Gulf, Wooramel Bank and Faure Sill. Spatial variation in seagrass loss was best explained by a model that included an interaction between two heat stress metrics, the most substantial loss occurring when degree heating weeks (DHWm) was ≥10 and the number of days exposed to extreme sea surface temperature during the MHW (DaysOver) was ≥94. Ground truthing at 622 points indicated that change in seagrass cover was predominantly due to loss of Amphibolis antarctica rather than Posidonia australis, the other prominent seagrass at Shark Bay. As seawater temperatures continue to rise and the incidence of MHWs increase globally, this work will provide a basis for identifying areas of meadow degradation, or stability and recovery, and potential areas of resilience.

Root microbiomes as indicators of seagrass health.

The development of early warning indicators that identify ecosystem stress is a priority for improving ecosystem management. As microbial communities respond rapidly to environmental disturbance, monitoring their composition could prove one such early indicator of environmental stress. We combined 16S rRNA gene sequencing of the seagrass root microbiome of Halophila ovalis with seagrass health metrics (biomass, productivity and Fsulphide) to develop microbial indicators for seagrass condition across the Swan-Canning Estuary and the Leschenault Estuary (south-west Western Australia); the former had experienced an unseasonal rainfall event leading to declines in seagrass health. Microbial indicators detected sites of potential stress that other seagrass health metrics failed to detect. Genera that were more abundant in 'healthy' seagrasses included putative methylotrophic bacteria (e.g. Methylotenera and Methylophaga), iron cycling bacteria (e.g. Deferrisoma and Geothermobacter) and N2 fixing bacteria (e.g. Rhizobium). Conversely, genera that were more abundant in 'stressed' seagrasses were dominated by putative sulphur-cycling bacteria, both sulphide-oxidising (e.g. Candidatus Thiodiazotropha and Candidatus Electrothrix) and sulphate-reducing (e.g. SEEP-SRB1, Desulfomonile and Desulfonema). The sensitivity of the microbial indicators developed here highlights their potential to be further developed for use in adaptive seagrass management, and emphasises their capacity to be effective early warning indicators of stress.

Salinity stress drives herbivory rates and selective grazing in subtidal seagrass communities.

The role of environmental-stress gradients in driving trophic processes like grazing, has potential to shape ecosystem responses to environmental change. In subtidal seagrass systems, however, the variation in top-down processes along stress gradients are poorly understood. We deployed herbivory assays using the five most common seagrass species of Shark Bay, to determine whether herbivory pressure changed across a salinity-stress gradient from oceanic (38 PSU) to hyper-saline (51 PSU) conditions. Seagrass tissue removed from herbivory assays by fishes decreased as environmental stress increased, and herbivores consumed greater amounts of tropical seagrass species compared to the temperate species that dominate seagrass cover in Shark Bay. This heightened consumption was correlated with enriched seagrass nutrient concentrations. Our work suggests there's a fundamental relationship between trophic interactions and environmental conditions within complex marine settings. Abiotic stressors like salinity directly impact seagrass communities physiologically; however we show that salinity stressors also shift biotic interactions, indirectly influencing grazing rates and thus having a greater effect on seagrasses than physiological impacts alone. In Shark Bay where restoration efforts are being employed to address large scale loss of seagrasses, the relationship between herbivory pressure and salinity-stress could therefore prove crucial to restoration success.

Metagenomic Evidence of Microbial Community Responsiveness to Phosphorus and Salinity Gradients in Seagrass Sediments.

Sediment microorganisms can have profound influence on productivity and functioning of marine ecosystems through their critical roles in regulating biogeochemical processes. However, the identity of sediment microorganisms that mediate organic matter turnover and nutrient cycling in seagrass sediments is only poorly understood. Here, we used metagenomic sequencing to investigate shifts in the structure and functioning of the microbial community of seagrass sediments across a salinity and phosphorus (P) availability gradient in Shark Bay, WA, Australia. This iconic ecosystem is oligotrophic and hypersaline with abundant seagrass meadows that directly contribute Shark Bay's status as a World Heritage Site. We show that sediment phosphonate metabolism genes as well as enzyme activities increase in hypersaline conditions with lower soluble reactive phosphate in the water column. Given that sediment organic P content is also highest where P concentrations in the water column are low, we suggest that microbial processing of organic P can contribute to the P requirements of seagrasses at particularly oligotrophic sites. Seagrass meadows are often highly productive in oligotrophic waters, and our findings suggest that an increase in the functional capacity of microbial communities in seagrass sediments to break down organic P may contribute to the high productivity of seagrass meadows under oligotrophic conditions. When compared to soil and sediment metagenomes from other aquatic and terrestrial ecosystems, we also show microbial communities in seagrass sediments have a disproportionately high abundance of putative phosphorus and sulfur metabolism genes, which may have played an important evolutionary role in allowing these angiosperms to recolonize the marine environment and prosper under oligotrophic conditions.

Belowground stressors and long-term seagrass declines in a historically degraded seagrass ecosystem after improved water quality.

Continued seagrass declines in ecosystems with improved water quality may be driven by sediment stressors. One of the most cited examples of a seagrass ecosystem with declines is Cockburn Sound, Western Australia, where 75% of seagrasses (2169 ha) were lost in the 1960s-1980s due to poor water quality. Water quality has subsequently improved in Cockburn Sound, yet shoot density declines continue in some areas. Here, we investigated if sediment stressors (sulfide intrusion and heavy metals) contributed to declining Posidonia sinuosa shoot densities in Cockburn Sound. Seagrass δ34S were depleted at sites with a history of seagrass declines, indicating seagrasses at these sites were under sulfide stress. Heavy metals (Fe, Zn, Mn, Cr, Cu and Cd) in sediments and seagrasses did not show clear patterns with shoot density or biomass, and largely decreased from similar measurements in the late 1970s. However, seagrass cadmium concentrations were negatively correlated to seagrass biomass and shoot density. High cadmium concentrations interfere with sulfur metabolism in terrestrial plants, but impacts on seagrasses remain to be explored. Given that sulfide intrusion can prevent recolonization and drive seagrass declines, management plans in degraded seagrass ecosystems should include management of sediment stressors and water quality to provide comprehensive management.

Coastal connectivity and spatial subsidy from a microbial perspective.

The transfer of organic material from one coastal environment to another can increase production in recipient habitats in a process known as spatial subsidy. Microorganisms drive the generation, transformation, and uptake of organic material in shallow coastal environments, but their significance in connecting coastal habitats through spatial subsidies has received limited attention. We address this by presenting a conceptual model of coastal connectivity that focuses on the flow of microbially mediated organic material in key coastal habitats. Our model suggests that it is not the difference in generation rates of organic material between coastal habitats but the amount of organic material assimilated into microbial biomass and respiration that determines the amount of material that can be exported from one coastal environment to another. Further, the flow of organic material across coastal habitats is sensitive to environmental change as this can alter microbial remineralization and respiration rates. Our model highlights microorganisms as an integral part of coastal connectivity and emphasizes the importance of including a microbial perspective in coastal connectivity studies.

Photosynthetic response to globally increasing CO2 of co-occurring temperate seagrass species.

Photosynthesis of most seagrass species seems to be limited by present concentrations of dissolved inorganic carbon (DIC). Therefore, the ongoing increase in atmospheric CO2 could enhance seagrass photosynthesis and internal O2 supply, and potentially change species competition through differential responses to increasing CO2 availability among species. We used short-term photosynthetic responses of nine seagrass species from the south-west of Australia to test species-specific responses to enhanced CO2 and changes in HCO3 (-) . Net photosynthesis of all species except Zostera polychlamys were limited at pre-industrial compared to saturating CO2 levels at light saturation, suggesting that enhanced CO2 availability will enhance seagrass performance. Seven out of the nine species were efficient HCO3 (-) users through acidification of diffusive boundary layers, production of extracellular carbonic anhydrase, or uptake and internal conversion of HCO3 (-) . Species responded differently to near saturating CO2 implying that increasing atmospheric CO2 may change competition among seagrass species if co-occurring in mixed beds. Increasing CO2 availability also enhanced internal aeration in the one species assessed. We expect that future increases in atmospheric CO2 will have the strongest impact on seagrass recruits and sparsely vegetated beds, because densely vegetated seagrass beds are most often limited by light and not by inorganic carbon.

Strategy for assessing impacts in ephemeral tropical seagrasses.

We investigated the phenology and spatial patterns in Halophila decipiens by assessing biomass, reproduction and seed density in ~400 grab samples collected across nine sites (8 to 14 m water depth) between June 2011 and December 2012. Phenology correlated with light climate which is governed by the summer monsoon (wet period). During the wet period, sedimentary seed banks prevailed, varying spatially at both broad and fine scales, presenting a source of propagules for re-colonisation following the unfavourable growing conditions of the monsoon. Spatial patterns in H. decipiens biomass following monsoon conditions were highly variable within a landscape that largely comprised potential seagrass habitat. Management strategies for H. decipiens and similar transient species must recognise the high temporal and spatial variability of these populations and be underpinned by a framework that emphasises vulnerability assessments of different life stages instead of relying solely on thresholds for standing stock at fixed reference sites.

Extreme temperatures, foundation species, and abrupt ecosystem change: an example from an iconic seagrass ecosystem.

Extreme climatic events can trigger abrupt and often lasting change in ecosystems via the reduction or elimination of foundation (i.e., habitat-forming) species. However, while the frequency/intensity of extreme events is predicted to increase under climate change, the impact of these events on many foundation species and the ecosystems they support remains poorly understood. Here, we use the iconic seagrass meadows of Shark Bay, Western Australia--a relatively pristine subtropical embayment whose dominant, canopy-forming seagrass, Amphibolis antarctica, is a temperate species growing near its low-latitude range limit--as a model system to investigate the impacts of extreme temperatures on ecosystems supported by thermally sensitive foundation species in a changing climate. Following an unprecedented marine heat wave in late summer 2010/11, A. antarctica experienced catastrophic (>90%) dieback in several regions of Shark Bay. Animal-borne video footage taken from the perspective of resident, seagrass-associated megafauna (sea turtles) revealed severe habitat degradation after the event compared with a decade earlier. This reduction in habitat quality corresponded with a decline in the health status of largely herbivorous green turtles (Chelonia mydas) in the 2 years following the heat wave, providing evidence of long-term, community-level impacts of the event. Based on these findings, and similar examples from diverse ecosystems, we argue that a generalized framework for assessing the vulnerability of ecosystems to abrupt change associated with the loss of foundation species is needed to accurately predict ecosystem trajectories in a changing climate. This includes seagrass meadows, which have received relatively little attention in this context. Novel research and monitoring methods, such as the analysis of habitat and environmental data from animal-borne video and data-logging systems, can make an important contribution to this framework.