Matthew W. Fraser

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.

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.

Science behind management of Shark Bay and Florida Bay, two P-limited subtropical systems with different climatology and human pressures

This special issue on ‘Science for the management of subtropical embayments: examples from Shark Bay and Florida Bay’ is a valuable compilation of individual research outcomes from Florida Bay and Shark Bay from the past decade and addresses gaps in our scientific knowledge base in Shark Bay especially. Yet the compilation also demonstrates excellent research that is poorly integrated, and driven by interests and issues that do not necessarily lead to a more integrated stewardship of the marine natural values of either Shark Bay or Florida Bay. Here we describe the status of our current knowledge, introduce the valuable extension of the current knowledge through the papers in this issue and then suggest some future directions. For management, there is a need for a multidisciplinary international science program that focusses research on the ecological resilience of Shark Bay and Florida Bay, the effect of interactions between physical environmental drivers and biological control through behavioural and trophic interactions, and all under increased anthropogenic stressors. Shark Bay offers a ‘pristine template’ for this scale of study.

Hydrogen sulfide intrusion in seagrasses from Shark Bay, Western Australia

Sulfides in sediments and hydrogen sulfide (H2S) intrusion in plant tissues were investigated for six species of seagrass in Shark Bay, Western Australia, at two sites with elevated salinities of 42 and 45 psu. H2S intrusion ranged from <20% to 100% in roots and rhizomes, indicating a high degree of sulfide intrusion in some cases, although this did not vary consistently between larger, long-lived species and smaller, less persistent species. There were significant differences in accumulation of total sulfur (TS) among species. Anatomy of rhizomes and roots showed species-specific differences in aerenchyma, the air channels that allow oxygen to diffuse down to the roots and sediments, and tissues with thickened cell walls that could present a barrier to diffusion of H2S, suggesting that morphology may influence sulfide intrusion and sulfur accumulation. Sulfide concentrations in seagrass sediments were far lower in Shark Bay than in Florida Bay, a subtropical embayment where sulfide toxicity has been implicated in seagrass dieback. Despite significant H2S intrusion into tissues of some Shark Bay seagrasses, there was no evidence of any deleterious effects in the current conditions.

Seagrass derived organic matter influences biogeochemistry, microbial communities, and seedling biomass partitioning in seagrass sediments

AimsSeedling establishment is a crucial life history stage in seagrasses, yet factors that affect seedling health are poorly characterized. We investigated if organic matter (OM) additions to sediments provided nutritional benefits for seagrass seedlings through microbial degradation.MethodsWe tested the effects of sedimentary OM additions on Posidonia australis seedlings growing in tank cultures. We focussed on sediment biogeochemical processes and microbial communities that may impact seedling growth and physiology.ResultsEnrichment of sediments with OM changed microbial community composition (DNA-ARISA) and a significant increase in hydrolytic enzyme expression. Total seedling biomass did not differ between OM treatments, but above:belowground biomass increased with OM enrichment. Nitrogen and phosphorus concentration of seagrass leaves was lower with increasing OM.ConclusionsSeagrass derived OM has been considered a refractory store of carbon, yet here we show its deposition into sediments significantly alters belowground conditions. Remineralization of the OM changes both physical and chemical nature of sediments that leads to greater biochemical activity, change in microbial communities and greater investment into above ground photosynthetic biomass. The presence of OM may assist seagrass seedling survival during early development by enhancing root branching and stability in sediments, but is unlikely to provide nutritional benefits.

Nutrient status of seagrasses cannot be inferred from system-scale distribution of phosphorus in Shark Bay, Western Australia

Differences in phosphorus (P) availability can influence the ecology and physiology of seagrass communities; and are usually inferred from changes in the relative P content in seagrass leaves. Shark Bay is a subtropical marine embayment, with decreasing P concentrations in the water column and sediments from north to south across the entire embayment. We examined the P and nitrogen (N) content of seagrass leaves and P content of sediments across the Faure Sill and Wooramel delta region of Shark Bay, to determine whether the leaf content of seagrasses in Shark Bay also decreased from north to south over smaller spatial scales. Nutrient content of Amphibolis antarctica and Halodule uninervis were highly variable and were not strongly correlated with sediment P concentrations. Mean N : P ratios of seagrasses ( 100 km) of sedimentary P distributions. We suggest that P availability to seagrasses is more likely a complex function of differing nutrient inputs, rates of delivery to the plants and cycling rates.

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.

Coastal connectivity and spatial subsidy from a microbial perspective

Abstract 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.

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.

Comment on ‘Seagrass Viviparous Propagules as a Potential Long-Distance Dispersal Mechanism’ by A. C. G. Thomson et al.

In a recent paper by Thomson et al. (2014), vivipary is implied for the eastern Australian Zostera, Zostera nigricaulis (revised from Zostera tasmanica; Kuo 2005). However, the definition of vivipary (production of genetically distinct offspring resulting from sexual reproduction) needs to be fully explored in terms of the experimental claims by the authors. Thomson et al. (2014) appear to confuse vivipary with vegetative (clonal) growth, where the clonal units have potentially dispersive capabilities. Importantly, the authors claim that ‘viviparous propagules may disperse over large distances and successfully recruit or contribute to population connectivity’ is not supported by appropriate data demonstrating dispersal and long-term survival. A key issue we found was the need for an understanding of the accepted definition of what comprises vivipary, pseudovivipary and vegetative reproduction and the attendant genetic consequences. We reinterpret the results of Thomson et al. (2014) based on the likelihood that the propagules they used for in situ and ex situ trials are simply vegetative growth forms, potentially produced under conditions of stress and/or failure to reproduce sexually. We also point out misinterpretations and conclude with a warning and recommendation. Vivipary in flowering plants is the precocious and continuous growth of sexual offspring while still attached to the maternal parent (Goebel 1905; Arber 1965; Elmquist and Cox 1996). There are two main types of vivipary: true vivipary and pseudovivipary. True vivipary involves the germination of sexually produced offspring while still attached to the parent plant. Offspring are genetically distinct from parent plants, as true vivipary results from sexual reproduction. True vivipary has been demonstrated in Cactaceae (Cota-Sánchez 2004) and mangroves (which Thomson et al. 2014 refer to correctly). A molecular phylogenetic analysis of mangroves inferred that vivipary originated in multiple independent times within the group (Shi et al. 2005). Currently, vivipary is reported and demonstrated based on anatomical characters in only two seagrass genera: Amphibolis and Thalassodendron (Cymodoceaceae; Kuo and Kirkman 1990). The position of these taxa in a phylogeny of marine flowering plants (Les et al. 1997) suggests that this trait has evolved only once in seagrasses. In pseudovivipary, the floral organs are replaced by plantlets, providing an asexual means for many terrestrial monocots (ancestors of marine seagrasses) to reproduce in extreme environments, such as alpine or arid ecosystems (Elmquist and Cox 1996). The upper portion of these plantlets has reverted from sexual to vegetative development. The important difference between pseudoviviparous plantlets and typical vegetative growth is that the plantlets retain the dehiscence Communicated by John C. Callaway