John Statton

The Central Role of Dispersal in the Maintenance and Persistence of Seagrass Populations

Global seagrass losses parallel significant declines observed in corals and mangroves over the past 50 years. These combined declines have resulted in accelerated global losses to ecosystem services in coastal waters. Seagrass meadows can be extensive (hundreds of square kilometers) and long-lived (thousands of years), with the meadows persisting predominantly through vegetative (clonal) growth. They also invest a large amount of energy in sexual reproduction. In this article, we explore the role that sexual reproduction, pollen, and seed dispersal play in maintaining species distributions, genetic diversity, and connectivity among seagrass populations. We also address the relationship between long-distance dispersal, genetic connectivity, and the maintenance of genetic diversity that may enhance resilience to stresses associated with seagrass loss. Our reevaluation of seagrass dispersal and recruitment has altered our perception of the importance of long-distance dispersal and has revealed extensive dispersal at scales much larger than was previously thought possible.

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.

The movement ecology of seagrasses

A movement ecology framework is applied to enhance our understanding of the causes, mechanisms and consequences of movement in seagrasses: marine, clonal, flowering plants. Four life-history stages of seagrasses can move: pollen, sexual propagules, vegetative fragments and the spread of individuals through clonal growth. Movement occurs on the water surface, in the water column, on or in the sediment, via animal vectors and through spreading clones. A capacity for long-distance dispersal and demographic connectivity over multiple timeframes is the novel feature of the movement ecology of seagrasses with significant evolutionary and ecological consequences. The space–time movement footprint of different life-history stages varies. For example, the distance moved by reproductive propagules and vegetative expansion via clonal growth is similar, but the timescales range exponentially, from hours to months or centuries to millennia, respectively. Consequently, environmental factors and key traits that interact to influence movement also operate on vastly different spatial and temporal scales. Six key future research areas have been identified.

Demographic and genetic connectivity: the role and consequences of reproduction, dispersal and recruitment in seagrasses

Accurate estimation of connectivity among populations is fundamental for determining the drivers of population resilience, genetic diversity, adaptation and speciation. However the separation and quantification of contemporary versus historical connectivity remains a major challenge. This review focuses on marine angiosperms, seagrasses, that are fundamental to the health and productivity of temperate and tropical coastal marine environments globally. Our objective is to understand better the role of sexual reproduction and recruitment in influencing demographic and genetic connectivity among seagrass populations through an integrated multidisciplinary assessment of our present ecological, genetic, and demographic understanding, with hydrodynamic modelling of transport. We investigate (i) the demographic consequences of sexual reproduction, dispersal and recruitment in seagrasses, (ii) contemporary transport of seagrass pollen, fruits and seed, and vegetative fragments with a focus on hydrodynamic and particle transport models, and (iii) contemporary genetic connectivity among seagrass meadows as inferred through the application of genetic markers. New approaches are reviewed, followed by a summary outlining future directions for research: integrating seascape genetic approaches; incorporating hydrodynamic modelling for dispersal of pollen, seeds and vegetative fragments; integrating studies across broader geographic ranges; and incorporating non‐equilibrium modelling. These approaches will lead to a more integrated understanding of the role of contemporary dispersal and recruitment in the persistence and evolution of seagrasses.

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.

A comparative assessment of approaches and outcomes for seagrass revegetation in Shark Bay and Florida Bay

Here, we review the literature to evaluate seagrass revegetation projects focussed on Posidonia australis and Amphibolis antarctica, the main affected species in Shark Bay in the World Heritage Area in Western Australia, together with projects from Florida Bay, an analogous system with a long history of seagrass revegetation. We assessed the effectiveness of anchoring planting units, plant-unit density and size on planting-unit survival. We found no positive trends in our assessment, suggesting that there is no discrete technique, approach or technology that could be used with confidence to deliver cost-effective, scalable revegetation. Of concern was that revegetation success was evaluated over comparatively short time frames (1–3 years), driven by the strict time frames or deadlines of governing grant funding and commercial activities, leading to concerns that long-term revegetation outcomes may be difficult to assess with confidence. Several factors influenced revegetation outcomes which were grouped into three ‘filter’ categories; abiotic, biotic and socioeconomic. We recommend that future revegetation programs involving seagrass have greater emphasis on understanding how these filters act independently or collectively to drive successful revegetation as well as developing cost-effective, proven and scalable technology supported by longer-term monitoring to ensure revegetation programs do achieve the desired ecological outcomes.

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.

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.

Edge Effects along a Seagrass Margin Result in an Increased Grazing Risk on Posidonia australis Transplants

A key issue in habitat restoration are the changes in ecological processes that occur when fragments of habitat are lost, resulting in the persistence of habitat-degraded margins. Margins often create or enhance opportunities for negative plant-herbivore interactions, preventing natural or assisted re-establishment of native vegetation into the degraded area. However, at some distance from the habitat margin these negative interactions may relax. Here, we posit that the intensity of species interactions in a fragmented Posidonia australis seagrass meadow may be spatially dependent on proximity to the seagrass habitat edge, whereby the risk of grazing is high and the probability of survival of seagrass transplants is low. To test this, transplants were planted 2 m within the meadow, on the meadow edge at 0m, and at 2m, 10m, 30m, 50m and 100m distance from the edge of the seagrass meadow into the unvegetated sand sheet. There was an enhanced grazing risk 0-10m from the edge, but decreased sharply with increasing distances (>30m). Yet, the risk of grazing was minimal inside the seagrass meadow, indicating that grazers may use the seagrass meadow for refuge but are not actively grazing within it. The relationship between short-term herbivory risk and long-term survival was not straightforward, suggesting that other environmental filters are also affecting survival of P. australis transplants within the study area. We found that daily probability of herbivory was predictable and operating over a small spatial scale at the edge of a large, intact seagrass meadow. These findings highlight the risk from herbivory can be high, and a potential contributing factor to seagrass establishment in restoration programs.

Low Light Availability Alters Root Exudation and Reduces Putative Beneficial Microorganisms in Seagrass Roots

Seagrass roots host a diverse microbiome that is critical for plant growth and health. Composition of microbial communities can be regulated in part by root exudates, but the specifics of these interactions in seagrass rhizospheres are still largely unknown. As light availability controls primary productivity, reduced light may impact root exudation and consequently the composition of the root microbiome. Hence, we analyzed the influence of light availability on root exudation and community structure of the root microbiome of three co-occurring seagrass species, Halophila ovalis, Halodule uninervis and Cymodocea serrulata. Plants were grown under four light treatments in mesocosms for 2 weeks; control (100% surface irradiance (SI), medium (40% SI), low (20% SI) and fluctuating light (10 days 20% and 4 days 100%). 16S rDNA amplicon sequencing revealed that microbial diversity, composition and predicted function were strongly influenced by the presence of seagrass roots, such that root microbiomes were unique to each seagrass species. Reduced light availability altered seagrass root exudation, as characterized using fluorescence spectroscopy, and altered the composition of seagrass root microbiomes with a reduction in abundance of potentially beneficial microorganisms. Overall, this study highlights the potential for above-ground light reduction to invoke a cascade of changes from alterations in root exudation to a reduction in putative beneficial microorganisms and, ultimately, confirms the importance of the seagrass root environment – a critical, but often overlooked space.