Mass flowering and unprecedented extended pseudovivipary in seagrass (Posidonia oceanica) after a Marine Heat Wave.

Seagrasses are marine flowering plants that create critical coastal ecosystems and are threatened by warming. Clonal expansion is generally the dominant strategy for meadow recovery, while sexual reproduction strongly differs among species (e.g., monoecious and diecious species, some creating seed banks, viviparous seedlings). In 2022, the Western Mediterranean underwent unprecedented warming, and, associated with it, we observed flowering (100 %) across 11 Posidonia oceanica meadows in Mallorca, Balearic Islands. Furthermore, 64 % of the sites also exhibited pseudovivipary, an extremely rare phenomenon in angiosperms whereby plantlets replace sexual reproductive structures, producing clones of the maternal plant. Our results support the notion that P. oceanica flowering and pseudovivipary (genetically confirmed) are triggered by warming, never before being pseudovivipary reported across multiple sites in a marine plant. Considering the negative impacts that warming can have on seagrasses, existence of widespread pseudovivipary is a critical aspect to consider for understanding mechanisms of resilience in seagrasses.

Thermo-priming triggers species-specific physiological and transcriptome responses in Mediterranean seagrasses.

Heat-priming improves plants' tolerance to a recurring heat stress event. The underlying molecular mechanisms of heat-priming are largely unknown in seagrasses. Here, ad hoc mesocosm experiments were conducted with two Mediterranean seagrass species, Posidonia oceanica and Cymodocea nodosa. Plants were first exposed to heat-priming, followed by a heat-triggering event. A comprehensive assessment of plant stress response across different levels of biological organization was performed at the end of the triggering event. Morphological and physiological results showed an improved response of heat-primed P. oceanica plants while in C. nodosa both heat- and non-primed plants enhanced their growth rates at the end of the triggering event. As resulting from whole transcriptome sequencing, molecular functions related to several cellular compartments and processes were involved in the response to warming of non-primed plants, while the response of heat-primed plants involved a limited group of processes. Our results suggest that seagrasses acquire a primed state during the priming event, that eventually gives plants the ability to induce a more energy-effective response when the thermal stress event recurs. Different species may differ in their ability to perform an improved heat stress response after priming. This study provides pioneer molecular insights into the emerging topic of seagrass stress priming and may benefit future studies in the field.

Marine heatwaves recurrence aggravates thermal stress in the surfgrass Phyllospadix scouleri.

The surfgrass Phyllospadix scouleri grows in highly productive meadows along the Pacific coast of North America. This region has experienced increasingly severe marine heatwaves (MHWs) in recent years. Our study evaluated the impact of consecutive MHWs, simulated in mesocosms, on essential ecophysiological features of P. scouleri. Overall, our findings show that the plants' overall physiological status has been progressively declining. Interestingly, the indicators of physiological stress in photosynthesis only showed up once the initial heat exposure stopped (i.e., during the recovery period). The warming caused increased oxidative damage and a decrease in nitrate uptake rates. However, the levels of non-structural carbohydrates and relative growth rates were not affected. Our findings emphasize the significance of incorporating recovery periods in this type of study as they expose delayed stress responses. Furthermore, experiencing consecutive intense MHWs can harm surfgrasses over time, compromising the health of their meadows and the services they offer to the ecosystem.

Seagrass genomes reveal ancient polyploidy and adaptations to the marine environment.

We present chromosome-level genome assemblies from representative species of three independently evolved seagrass lineages: Posidonia oceanica, Cymodocea nodosa, Thalassia testudinum and Zostera marina. We also include a draft genome of Potamogeton acutifolius, belonging to a freshwater sister lineage to Zosteraceae. All seagrass species share an ancient whole-genome triplication, while additional whole-genome duplications were uncovered for C. nodosa, Z. marina and P. acutifolius. Comparative analysis of selected gene families suggests that the transition from submerged-freshwater to submerged-marine environments mainly involved fine-tuning of multiple processes (such as osmoregulation, salinity, light capture, carbon acquisition and temperature) that all had to happen in parallel, probably explaining why adaptation to a marine lifestyle has been exceedingly rare. Major gene losses related to stomata, volatiles, defence and lignification are probably a consequence of the return to the sea rather than the cause of it. These new genomes will accelerate functional studies and solutions, as continuing losses of the 'savannahs of the sea' are of major concern in times of climate change and loss of biodiversity.

Ocean acidification impairs seagrass performance under thermal stress in shallow and deep water.

Despite the effects of ocean acidification (OA) on seagrasses have been widely investigated, predictions of seagrass performance under future climates need to consider multiple environmental factors. Here, we performed a mesocosm study to assess the effects of OA on shallow and deep Posidonia oceanica plants. The experiment was run in 2021 and repeated in 2022, a year characterized by a prolonged warm water event, to test how the effects of OA on plants are modulated by thermal stress. The response of P. oceanica to experimental conditions was investigated at different levels of biological organization. Under average seawater temperature, there were no effects of OA in both shallow and deep plants, indicating that P. oceanica is not limited by current inorganic carbon concentration, regardless of light availability. In contrast, under thermal stress, exposure of plants to OA increased lipid peroxidation and decreased photosynthetic performance, with deep plants displaying higher levels of heat stress, as indicated by the over-expression of stress-related genes and the activation of antioxidant systems. In addition, warming reduced plant growth, regardless of seawater CO2 and light levels, suggesting that thermal stress may play a fundamental role in the future development of seagrass meadows. Our results suggest that OA may exacerbate the negative effects of future warming on seagrasses.

Signs of local adaptation by genetic selection and isolation promoted by extreme temperature and salinity in the Mediterranean seagrass Posidonia oceanica.

Adaptation to local conditions is known to occur in seagrasses; however, knowledge of the genetic basis underlying this phenomenon remains scarce. Here, we analysed Posidonia oceanica from six sites within and around the Stagnone di Marsala, a semi-enclosed coastal lagoon where salinity and temperature exceed the generally described tolerance thresholds of the species. Sea surface temperatures (SSTs) were measured and plant samples were collected for the assessment of morphology, flowering rate and for screening genome-wide polymorphisms using double digest restriction-site-associated DNA sequencing. Results demonstrated more extreme SSTs and salinity levels inside the lagoon than the outer lagoon regions. Morphological results showed significantly fewer and shorter leaves and reduced rhizome growth of P. oceanica from the inner lagoon and past flowering events were recorded only for a meadow farthest away from the lagoon. Using an array of 51,329 single nucleotide polymorphisms, we revealed a clear genetic structure among the study sites and confirmed the genetic isolation and high clonality of the innermost site. In all, 14 outlier loci were identified and annotated with several proteins including those relate to plant stress response, protein transport and regulators of plant-specific developmental events. Especially, five outlier loci showed maximum allele frequency at the innermost site, likely reflecting adaptation to the extreme temperature and salinity regimes, possibly due to the selection of more resistant genotypes and the progressive restriction of gene flow. Overall, this study helps us to disentangle the genetic basis of seagrass adaptation to local environmental conditions and may support future works on assisted evolution in seagrasses.

A trait-based framework for seagrass ecology: Trends and prospects.

In the last three decades, quantitative approaches that rely on organism traits instead of taxonomy have advanced different fields of ecological research through establishing the mechanistic links between environmental drivers, functional traits, and ecosystem functions. A research subfield where trait-based approaches have been frequently used but poorly synthesized is the ecology of seagrasses; marine angiosperms that colonized the ocean 100M YA and today make up productive yet threatened coastal ecosystems globally. Here, we compiled a comprehensive trait-based response-effect framework (TBF) which builds on previous concepts and ideas, including the use of traits for the study of community assembly processes, from dispersal and response to abiotic and biotic factors, to ecosystem function and service provision. We then apply this framework to the global seagrass literature, using a systematic review to identify the strengths, gaps, and opportunities of the field. Seagrass trait research has mostly focused on the effect of environmental drivers on traits, i.e., "environmental filtering" (72%), whereas links between traits and functions are less common (26.9%). Despite the richness of trait-based data available, concepts related to TBFs are rare in the seagrass literature (15% of studies), including the relative importance of neutral and niche assembly processes, or the influence of trait dominance or complementarity in ecosystem function provision. These knowledge gaps indicate ample potential for further research, highlighting the need to understand the links between the unique traits of seagrasses and the ecosystem services they provide.

Gene co-expression network analysis for the selection of candidate early warning indicators of heat and nutrient stress in Posidonia oceanica.

The continuous worldwide seagrasses decline calls for immediate actions in order to preserve this precious marine ecosystem. The main stressors that have been linked with decline in seagrasses are 1) the increasing ocean temperature due to climate change and 2) the continuous inputs of nutrients (eutrophication) associated with coastal human activities. To avoid the loss of seagrass populations, an "early warning" system is needed. We used Weighed Gene Co-expression Network Analysis (WGCNA), a systems biology approach, to identify potential candidate genes that can provide an early warning signal of stress in the Mediterranean iconic seagrass Posidonia oceanica, anticipating plant mortality. Plants were collected from both eutrophic (EU) and oligotrophic (OL) environments and were exposed to thermal and nutrient stress in a dedicated mesocosm. By correlating the whole-genome gene expression after 2-weeks exposure with the shoot survival percentage after 5-weeks exposure to stressors, we were able to identify several transcripts that indicated an early activation of several biological processes (BP) including: protein metabolic process, RNA metabolic process, organonitrogen compound biosynthetic process, catabolic process and response to stimulus, which were shared among OL and EU plants and among leaf and shoot apical meristem (SAM), in response to excessive heat and nutrients. Our results suggest a more dynamic and specific response of the SAM compared to the leaf, especially the SAM from plants coming from a stressful environment appeared more dynamic than the SAM from a pristine environment. A vast list of potential molecular markers is also provided that can be used as targets to assess field samples.

DNA methylation dynamics in a coastal foundation seagrass species under abiotic stressors.

DNA methylation (DNAm) has been intensively studied in terrestrial plants in response to environmental changes, but its dynamic changes in a temporal scale remain unexplored in marine plants. The seagrass Posidonia oceanica ranks among the slowest-growing and longest-living plants on Earth, and is particularly vulnerable to sea warming and local anthropogenic pressures. Here, we analysed the dynamics of DNAm changes in plants collected from coastal areas differentially impacted by eutrophication (i.e. oligotrophic, Ol; eutrophic, Eu) and exposed to abiotic stressors (nutrients, temperature increase and their combination). Levels of global DNAm (% 5-mC) and the expression of key genes involved in DNAm were assessed after one, two and five weeks of exposure. Results revealed a clear differentiation between plants, depending on environmental stimuli, time of exposure and plants' origin. % 5-mC levels were higher during the initial stress exposure especially in Ol plants, which upregulated almost all genes involved in DNAm. Contrarily, Eu plants showed lower expression levels, which increased under chronic exposure to stressors, particularly to temperature. These findings show that DNAm is dynamic in P. oceanica during stress exposure and underlined that environmental epigenetic variations could be implicated in the regulation of acclimation and phenotypic differences depending on local conditions.

Nested interactions between chemosynthetic lucinid bivalves and seagrass promote ecosystem functioning in contaminated sediments.

In seagrass sediments, lucinid bivalves and their chemoautotrophic bacterial symbionts consume H2S, relying indirectly on the plant productivity for the presence of the reduced chemical. Additionally, the role of lucinid bivalves in N provisioning to the plant (through N2 fixation by the symbionts) was hypothesized. Thus, lucinids may contribute to sediment detoxification and plant fitness. Seagrasses are subject to ever-increasing human pressure in coastal environments. Here, disentangling nested interactions between chemosynthetic lucinid bivalves and seagrass exposed to pollution may help to understand seagrass ecosystem dynamics and to develop successful seagrass restoration programs that consider the roles of animal-microbe symbioses. We evaluated the capacity of lucinid bivalves (Loripes orbiculatus) to promote nutrient cycling and seagrass (Cymodocea nodosa) growth during a 6-week mesocosm experiment. A fully crossed design was used to test for the effect of sediment contamination (metals, nutrients, and hydrocarbons) on plant and bivalve (alone or interacting) fitness, assessed by mortality, growth, and photosynthetic efficiency, and for the effect of their nested interaction on sediment biogeochemistry. Plants performed better in the contaminated sediment, where a larger pool of dissolved nitrogen combined with the presence of other trace elements allowed for an improved photosynthetic efficiency. In fact, pore water nitrogen accumulated during the experiment in the controls, while it was consumed in the contaminated sediment. This trend was accentuated when lucinids were present. Concurrently, the interaction between clams and plants benefitted both organisms and promoted plant growth irrespective of the sediment type. In particular, the interaction with lucinid clams resulted in higher aboveground biomass of C. nodosa in terms of leaf growth, leaf surface, and leaf biomass. Our results consolidate the notion that nested interactions involving animal-microbe associations promote ecosystem functioning, and potentially help designing unconventional seagrass restoration strategies that exploit chemosynthetic symbioses.

2b-RAD Genotyping of the Seagrass Cymodocea nodosa Along a Latitudinal Cline Identifies Candidate Genes for Environmental Adaptation.

Plant populations distributed along broad latitudinal gradients often show patterns of clinal variation in genotype and phenotype. Differences in photoperiod and temperature cues across latitudes influence major phenological events, such as timing of flowering or seed dormancy. Here, we used an array of 4,941 SNPs derived from 2b-RAD genotyping to characterize population differentiation and levels of genetic and genotypic diversity of three populations of the seagrass Cymodocea nodosa along a latitudinal gradient extending across the Atlantic-Mediterranean boundary (i.e., Gran Canaria-Canary Islands, Faro-Portugal, and Ebro Delta-Spain). Our main goal was to search for potential outlier loci that could underlie adaptive differentiation of populations across the latitudinal distribution of the species. We hypothesized that such polymorphisms could be related to variation in photoperiod-temperature regime occurring across latitudes. The three populations were clearly differentiated and exhibited diverse levels of clonality and genetic diversity. Cymodocea nodosa from the Mediterranean displayed the highest genotypic richness, while the Portuguese population had the highest clonality values. Gran Canaria exhibited the lowest genetic diversity (as observed heterozygosity). Nine SNPs were reliably identified as outliers across the three sites by two different methods (i.e., BayeScan and pcadapt), and three SNPs could be associated to specific protein-coding genes by screening available C. nodosa transcriptomes. Two SNPs-carrying contigs encoded for transcription factors, while the other one encoded for an enzyme specifically involved in the regulation of flowering time, namely Lysine-specific histone demethylase 1 homolog 2. When analyzing biological processes enriched within the whole dataset of outlier SNPs identified by at least one method, "regulation of transcription" and "signalling" were among the most represented. Our results highlight the fundamental importance signal integration and gene-regulatory networks, as well as epigenetic regulation via DNA (de)methylation, could have for enabling adaptation of seagrass populations along environmental gradients.

Sugars dominate the seagrass rhizosphere.

Seagrasses are among the most efficient sinks of carbon dioxide on Earth. While carbon sequestration in terrestrial plants is linked to the microorganisms living in their soils, the interactions of seagrasses with their rhizospheres are poorly understood. Here, we show that the seagrass, Posidonia oceanica excretes sugars, mainly sucrose, into its rhizosphere. These sugars accumulate to µM concentrations-nearly 80 times higher than previously observed in marine environments. This finding is unexpected as sugars are readily consumed by microorganisms. Our experiments indicated that under low oxygen conditions, phenolic compounds from P. oceanica inhibited microbial consumption of sucrose. Analyses of the rhizosphere community revealed that many microbes had the genes for degrading sucrose but these were only expressed by a few taxa that also expressed genes for degrading phenolics. Given that we observed high sucrose concentrations underneath three other species of marine plants, we predict that the presence of plant-produced phenolics under low oxygen conditions allows the accumulation of labile molecules across aquatic rhizospheres.

Local environment modulates whole-transcriptome expression in the seagrass Posidonia oceanica under warming and nutrients excess.

The intensification of anomalous events of seawater warming and the co-occurrence with local anthropogenic stressors are threatening coastal marine habitats, including seagrasses, which form extensive underwater meadows. Eutrophication highly affects coastal environments, potentially summing up to the widespread effects of global climate changes. In the present study, we investigated for the first time in seagrasses, the transcriptional response of different plant organs (i.e., leaf and shoot apical meristem, SAM) of the Mediterranean seagrass Posidonia oceanica growing in environments with a different history of nutrient enrichment. To this end, a mesocosm experiment exposing plants to single (nutrient enrichment or temperature increase) and multiple stressors (nutrient enrichment plus temperature increase), was performed. Results revealed a differential transcriptome regulation of plants under single and multiple stressors, showing an organ-specific sensitivity depending on plants' origin. While leaf tissues were more responsive to nutrient stress, SAM revealed a higher sensitivity to temperature treatments, especially in plants already impacted in their native environment. The exposure to stress conditions induced the modulation of different biological processes. Plants living in an oligotrophic environment were more responsive to nutrients compared to plants from a eutrophic environment. Evidences that epigenetic mechanisms were involved in the regulation of transcriptional reprogramming were also observed in both plants' organs. These results represent a further step in the comprehension of seagrass response to abiotic stressors pointing out the importance of local pressures in a global warming scenario.

Thermo-priming increases heat-stress tolerance in seedlings of the Mediterranean seagrass P. oceanica.

Seawater warming and increased incidence of marine heatwaves (MHW) are threatening the integrity of coastal marine habitats including seagrasses, which are particularly vulnerable to climate changes. Novel stress tolerance-enhancing strategies, including thermo-priming, have been extensively applied in terrestrial plants for enhancing resilience capacity under the re-occurrence of a stress event. We applied, for the first time in seedlings of the Mediterranean seagrass Posidonia oceanica, a thermo-priming treatment through the exposure to a simulated warming event. We analyzed the photo-physiological and growth performance of primed and non-primed seedlings, and the gene expression responses of selected genes (i.e. stress-, photosynthesis- and epigenetic-related genes). Results revealed that during the re-occurring stress event, primed seedlings performed better than unprimed showing unaltered photo-physiology supported by high expression levels of genes related to stress response, photosynthesis, and epigenetic modifications. These findings offer new opportunities to improve conservation and restoration efforts in a future scenario of environmental changes.

Improved chromosome-level genome assembly and annotation of the seagrass, Zostera marina (eelgrass).

Background: Seagrasses (Alismatales) are the only fully marine angiosperms.  Zostera marina (eelgrass) plays a crucial role in the functioning of coastal marine ecosystems and global carbon sequestration. It is the most widely studied seagrass and has become a marine model system for exploring adaptation under rapid climate change. The original draft genome (v.1.0) of the seagrass  Z. marina (L.) was based on a combination of Illumina mate-pair libraries and fosmid-ends. A total of 25.55 Gb of Illumina and 0.14 Gb of Sanger sequence was obtained representing 47.7× genomic coverage. The assembly resulted in ~2000 unordered scaffolds (L50 of 486 Kb), a final genome assembly size of 203MB, 20,450 protein coding genes and 63% TE content. Here, we present an upgraded chromosome-scale genome assembly and compare v.1.0 and the new v.3.1, reconfirming previous results from Olsen et al. (2016), as well as pointing out new findings.   Methods: The same high molecular weight DNA used in the original sequencing of the Finnish clone was used. A high-quality reference genome was assembled with the MECAT assembly pipeline combining PacBio long-read sequencing and Hi-C scaffolding.  Results: In total, 75.97 Gb PacBio data was produced. The final assembly comprises six pseudo-chromosomes and 304 unanchored scaffolds with a total length of 260.5Mb and an N50 of 34.6 MB, showing high contiguity and few gaps (~0.5%). 21,483 protein-encoding genes are annotated in this assembly, of which 20,665 (96.2%) obtained at least one functional assignment based on similarity to known proteins.  Conclusions: As an important marine angiosperm, the improved  Z. marina genome assembly will further assist evolutionary, ecological, and comparative genomics at the chromosome level. The new genome assembly will further our understanding into the structural and physiological adaptations from land to marine life.

Gene body DNA methylation in seagrasses: inter- and intraspecific differences and interaction with transcriptome plasticity under heat stress.

The role of DNA methylation and its interaction with gene expression and transcriptome plasticity is poorly understood, and current insight comes mainly from studies in very few model plant species. Here, we study gene body DNA methylation (gbM) and gene expression patterns in ecotypes from contrasting thermal environments of two marine plants with contrasting life history strategies in order to explore the potential role epigenetic mechanisms could play in gene plasticity and responsiveness to heat stress. In silico transcriptome analysis of CpGO/E ratios suggested that the bulk of Posidonia oceanica and Cymodocea nodosa genes possess high levels of intragenic methylation. We also observed a correlation between gbM and gene expression flexibility: genes with low DNA methylation tend to show flexible gene expression and plasticity under changing conditions. Furthermore, the empirical determination of global DNA methylation (5-mC) showed patterns of intra and inter-specific divergence that suggests a link between methylation level and the plants' latitude of origin and life history. Although we cannot discern whether gbM regulates gene expression or vice versa, or if other molecular mechanisms play a role in facilitating transcriptome responsiveness, our findings point to the existence of a relationship between gene responsiveness and gbM patterns in marine plants.

Unusually Warm Summer Temperatures Exacerbate Population and Plant Level Response of Posidonia oceanica to Anthropogenic Nutrient Stress.

Posidonia oceanica is a key foundation species in the Mediterranean providing valuable ecosystem services. However, this species is particularly vulnerable towards high coastal nutrient inputs and the rising frequency of intense summer heat waves, but their combined effect in situ has received little attention so far. Here, we investigated the effects of in situ nutrient addition during an unusually warm summer over a 4-month period, comparing different morphological, physiological and biochemical population metrics of seagrass meadows growing in protected areas (Ischia) with meadows already exposed to significant anthropogenic pressure (Baia - Gulf of Pozzuoli). Our study highlights that the effects of warmer than usual summer temperatures on the population level of seagrass meadows can be exacerbated if the plants are already exposed to higher anthropogenic pressures. Morphological and population level indicators mainly changed over time, possibly impacted by season and the warmer temperatures, and displayed more pronounced reductions in seagrasses from impacted sites. The additional nutrient supply had even more deleterious effects, as shown by a decrease in approximately 67% in cover in fertilized plots at high impacted sites and 33% at low impacted sites. Moreover, while rhizome starch concentration showed a seasonal increase in plants from low impacted sites it displayed a trend of a 27% decrease in fertilized plots of the high impacted sites. Epiphyte biomass was approximately four-fold higher on leaves of plants growing in impacted sites and even doubled with the additional nutrient input. Predicting and anticipating stress in P. oceanica is of crucial importance for conservation and management efforts, given the limited colonizing and reproductive ability and extremely slow growth of this ecosystem engineer. Our results suggest that monitoring efforts should focus especially on leaf area index (LAI), carbohydrate concentrations in the rhizomes, and epiphyte cover on leaves as indicators of the onset of stress in Posidonia oceanica, which can be used by decision makers to take appropriate measures before damage to the ecosystem becomes irreversible, minimize future human interference and strengthen the resilience of these important ecosystems.

Phenotypic plasticity under rapid global changes: The intrinsic force for future seagrasses survival.

Coastal oceans are particularly affected by rapid and extreme environmental changes with dramatic consequences for the entire ecosystem. Seagrasses are key ecosystem engineering or foundation species supporting diverse and productive ecosystems along the coastline that are particularly susceptible to fast environmental changes. In this context, the analysis of phenotypic plasticity could reveal important insights into seagrasses persistence, as it represents an individual property that allows species' phenotypes to accommodate and react to fast environmental changes and stress. Many studies have provided different definitions of plasticity and related processes (acclimation and adaptation) resulting in a variety of associated terminology. Here, we review different ways to define phenotypic plasticity with particular reference to seagrass responses to single and multiple stressors. We relate plasticity to the shape of reaction norms, resulting from genotype by environment interactions, and examine its role in the presence of environmental shifts. The potential role of genetic and epigenetic changes in underlying seagrasses plasticity in face of environmental changes is also discussed. Different approaches aimed to assess local acclimation and adaptation in seagrasses are explored, explaining strengths and weaknesses based on the main results obtained from the most recent literature. We conclude that the implemented experimental approaches, whether performed with controlled or field experiments, provide new insights to explore the basis of plasticity in seagrasses. However, an improvement of molecular analysis and the application of multi-factorial experiments are required to better explore genetic and epigenetic adjustments to rapid environmental shifts. These considerations revealed the potential for selecting the best phenotypes to promote assisted evolution with fundamental implications on restoration and preservation efforts.

Seagrasses in an era of ocean warming: a review.

Seagrasses are valuable sources of food and habitat for marine life and are one of Earth's most efficient carbon sinks. However, they are facing a global decline due to ocean warming and eutrophication. In the last decade, with the advent of new technology and molecular advances, there has been a dramatic increase in the number of studies focusing on the effects of ocean warming on seagrasses. Here, we provide a comprehensive review of the future of seagrasses in an era of ocean warming. We have gathered information from published studies to identify potential commonalities in the effects of warming and the responses of seagrasses across four distinct levels: molecular, biochemical/physiological, morphological/population, and ecosystem/planetary. To date, we know that although warming strongly affects seagrasses at all four levels, seagrass responses diverge amongst species, populations, and over depths. Furthermore, warming alters seagrass distribution causing massive die-offs in some seagrass populations, whilst also causing tropicalization and migration of temperate species. In this review, we evaluate the combined effects of ocean warming with other environmental stressors and emphasize the need for multiple-stressor studies to provide a deeper understanding of seagrass resilience. We conclude by discussing the most significant knowledge gaps and future directions for seagrass research.

Partitioning resilience of a marine foundation species into resistance and recovery trajectories.

The resilience of an ecological unit encompasses resistance during adverse conditions and the capacity to recover. We adopted a 'resistance-recovery' framework to experimentally partition the resilience of a foundation species (the seagrass Cymodocea nodosa). The shoot abundances of nine seagrass meadows were followed before, during and after simulated light reduction conditions. We determined the significance of ecological, environmental and genetic drivers on seagrass resistance (% of shoots retained during the light deprivation treatments) and recovery (duration from the end of the perturbed state back to initial conditions). To identify whether seagrass recovery was linearly related to prior resistance, we then established the connection between trajectories of resistance and recovery. Finally, we assessed whether recovery patterns were affected by biological drivers (production of sexual products-seeds-and asexual propagation) at the meadow-scale. Resistance to shading significantly increased with the genetic diversity of the meadow and seagrass recovery was conditioned by initial resistance during shading. A threshold in resistance (here, at a ca. 70% of shoot abundances retained during the light deprivation treatments) denoted a critical point that considerably delays seagrass recovery if overpassed. Seed densities, but not rhizome elongation rates, were higher in meadows that exhibited large resistance and quick recovery, which correlated positively with meadow genetic diversity. Our results highlight the critical role of resistance to a disturbance for persistence of a marine foundation species. Estimation of critical trade-offs between seagrass resistance and recovery is a promising field of research to better manage impacts on seagrass meadows.