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.

Variation in reproductive effort, genetic diversity and mating systems across Posidonia australis seagrass meadows in Western Australia.

Populations at the edges of their geographical range tend to have lower genetic diversity, smaller effective population sizes and limited connectivity relative to centre of range populations. Range edge populations are also likely to be better adapted to more extreme conditions for future survival and resilience in warming environments. However, they may also be most at risk of extinction from changing climate. We compare reproductive and genetic data of the temperate seagrass, Posidonia australis on the west coast of Australia. Measures of reproductive effort (flowering and fruit production and seed to ovule ratios) and estimates of genetic diversity and mating patterns (nuclear microsatellite DNA loci) were used to assess sexual reproduction in northern range edge (low latitude, elevated salinities, Shark Bay World Heritage Site) and centre of range (mid-latitude, oceanic salinity, Perth metropolitan waters) meadows in Western Australia. Flower and fruit production were highly variable among meadows and there was no significant relationship between seed to ovule ratio and clonal diversity. However, Shark Bay meadows were two orders of magnitude less fecund than those in Perth metropolitan waters. Shark Bay meadows were characterized by significantly lower levels of genetic diversity and a mixed mating system relative to meadows in Perth metropolitan waters, which had high genetic diversity and a completely outcrossed mating system. The combination of reproductive and genetic data showed overall lower sexual productivity in Shark Bay meadows relative to Perth metropolitan waters. The mixed mating system is likely driven by a combination of local environmental conditions and pollen limitation. These results indicate that seagrass restoration in Shark Bay may benefit from sourcing plant material from multiple reproductive meadows to increase outcrossed pollen availability and seed production for natural recruitment.

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.

Effects of desalination brine and seawater with the same elevated salinity on growth, physiology and seedling development of the seagrass Posidonia australis.

Desalination has the potential to provide an important source of potable water to growing coastal populations but it also produces highly saline brines with chemical additives, posing a possible threat to benthic marine communities. The effects of brine (0%, 50%, 100%) were compared to seawater treatments with the same salinity (37, 46, 54 psu) for seagrass (Posidonia australis) in mesocosms over 2 weeks. There were significant differences between brine and salinity treatments for photosynthesis, water relations and growth. Germinating seedlings of P. australis were also tested in brine treatments (0%, 25%, 50%, 100%) over 7 weeks followed by 2.5 weeks recovery in seawater. Growth was severely inhibited only in 100% brine. These experiments demonstrated that brine increased the speed and symptoms of stress in adult plants compared to treatments with the same salinity, whereas seedlings tolerated far longer brine exposure, and so could potentially contribute to seagrass recovery through recruitment.

Determining light stress responses for a tropical multi-species seagrass assemblage.

Existing mitigations to address deterioration in water clarity associated with human activities are based on responses from single seagrass species but may not be appropriate for diverse seagrass assemblages common to tropical waters. We present findings from a light experiment designed to determine the effects of magnitude and duration of low light on a mixed tropical seagrass assemblage. Mixed assemblages of three commonly co-occurring Indo-West Pacific seagrasses, Cymodocea serrulata, Halodule uninervis and Halophila ovalis were grown in climate-controlled tanks, where replicate pots were subjected to a gradient in light availability (0.9-21.6 mols PAR m-2 day-1) for 12 weeks. Increased shading resulted in declines in growth and changes in cellular and photosynthesis responses for all species, although time-scale and magnitude of response were species-specific. Applying management criteria (e.g. thresholds) relevant to one species may under- or over-estimate potential for impact on other species and the meadow as a whole.

Identifying critical recruitment bottlenecks limiting seedling establishment in a degraded seagrass ecosystem.

Identifying early life-stage transitions limiting seagrass recruitment could improve our ability to target demographic processes most responsive to management. Here we determine the magnitude of life-stage transitions along gradients in physical disturbance limiting seedling establishment for the marine angiosperm, Posidonia australis. Transition matrix models and sensitivity analyses were used to identify which transitions were critical for successful seedling establishment during the first year of seed recruitment and projection models were used to predict the most appropriate environments and seeding densities. Total survival probability of seedlings was low (0.001), however, transition probabilities between life-stages differed across the environmental gradients; seedling recruitment was affected by grazing and bioturbation prevailing during the first life-stage transition (1 month), and 4-6 months later during the third life-stage transition when establishing seedlings are physically removed by winter storms. Models projecting population growth from different starting seed densities showed that seeds could replace other more labour intensive and costly methods, such as transplanting adult shoots, if disturbances are moderated sufficiently and if large numbers of seed can be collected in sufficient quantity and delivered to restoration sites efficiently. These outcomes suggest that by improving management of early demographic processes, we could increase recruitment in restoration programs.

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.

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.

Short-term Responses of Posidonia australis to Changes in Light Quality.

Seagrass meadows are highly productive ecosystems that provide ecosystem services to the coastal zone but are declining globally, particularly due to anthropogenic activities that reduce the quantity of light reaching seagrasses, such as dredging, river discharge and eutrophication. Light quality (the spectral composition of the light) is also altered by these anthropogenic stressors as the differential attenuation of wavelengths of light is caused by materials within the water column. This study addressed the effect of altered light quality on different life-history stages of the seagrass Posidonia australis, a persistent, habitat-forming species in Australia. Aquarium-based experiments were conducted to determine how adult shoots and seedlings respond to blue (peak λ = 451 nm); green (peak λ = 522 nm); yellow (peak λ = 596 nm) and red (peak λ = 673 nm) wavelengths with a control of full-spectrum light (λ = 400 - 700 nm, at 200 µmol photons m-2 s-1). Posidonia australis adults did not respond to changes in light quality relative to full-spectrum light, demonstrating a capacity to obtain enough photons from a range of wavelengths across the visible spectrum to maintain short-term growth at high irradiances. Posidonia australis seedlings (<4 months old) grown in blue light showed a significant increase in xanthophyll concentrations when compared to plants grown in full-spectrum, demonstrating a pigment acclimation response to blue light. These results differed significantly from negative responses to changes in light quality recently described for Halophila ovalis, a colonizing seagrass species. Persistent seagrasses such as P. australis, appear to be better at tolerating short-term changes in light quality compared to colonizing species when sufficient PPFD is present.

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.

Reproduction at the extremes: pseudovivipary, hybridization and genetic mosaicism in Posidonia australis (Posidoniaceae).

BACKGROUND AND AIMS: Organisms occupying the edges of natural geographical ranges usually survive at the extreme limits of their innate physiological tolerances. Extreme and prolonged fluctuations in environmental conditions, often associated with climate change and exacerbated at species' geographical range edges, are known to trigger alternative responses in reproduction. This study reports the first observations of adventitious inflorescence-derived plantlet formation in the marine angiosperm Posidonia australis, growing at the northern range edge (upper thermal and salinity tolerance) in Shark Bay, Western Australia. These novel plantlets are described and a combination of microsatellite DNA markers and flow cytometry is used to determine their origin. METHODS: Polymorphic microsatellite DNA markers were used to generate multilocus genotypes to determine the origin of the adventitious inflorescence-derived plantlets. Ploidy and genome size were estimated using flow cytometry. KEY RESULTS: All adventitious plantlets were genetically identical to the maternal plant and were therefore the product of a novel pseudoviviparous reproductive event. It was found that 87 % of the multilocus genotypes contained three alleles in at least one locus. Ploidy was identical in all sampled plants. The genome size (2 C value) for samples from Shark Bay and from a separate site much further south was not significantly different, implying they are the same ploidy level and ruling out a complete genome duplication (polyploidy). CONCLUSIONS: Survival at range edges often sees the development of novel responses in the struggle for survival and reproduction. This study documents a physiological response at the trailing edge, whereby reproductive strategy can adapt to fluctuating conditions and suggests that the lower-than-usual water temperature triggered unfertilized inflorescences to 'switch' to growing plantlets that were adventitious clones of their maternal parent. This may have important long-term implications as both genetic and ecological constraints may limit the ability to adapt or range-shift; this seagrass meadow in Shark Bay already has low genetic diversity, no sexual reproduction and no seedling recruitment.

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.

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.