Mar Menor lagoon: an iconic case of ecosystem collapse

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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.Versión del editor2,35

A Critical Gap in Seagrass Protection: Impact of Anthropogenic Off-Shore Nutrient Discharges on Deep Posidonia oceanica Meadows

In the Mediterranean, anthropogenic pressures (specifically those involving nutrient loads) have been progressively moved to deeper off-shore areas to meet current policies dealing with the protection of marine biodiversity (e.g., European Directives). However, conservation efforts devoted to protecting Posidonia oceanica and other vulnerable marine habitats against anthropogenic pressures have dedicated very little attention to the deepest areas of these habitats. We studied the remote influence of off-shore nutrient discharge on the physiology and structure of deep P. oceanica meadows located nearest to an urban sewage outfall (WW; 1 km) and an aquaculture facility (FF; 2.5 km). Light reduction and elevated external nutrient availability (as indicated by high δ15N, total N and P content and N uptake rates of seagrass tissues) were consistent with physiological responses to light and nutrient stress. This was particularly evident in the sites located up to 2.5 km from the WW source, where carbon budget imbalances and structural alterations were more evident. These results provide evidence that anthropogenic nutrient inputs can surpass critical thresholds for the species, even in off-shore waters at distances within the km scale. Therefore, the critical distances between this priority habitat and nutrient discharge points have been underestimated and should be corrected to achieve a good conservation status.J.-C.J.’s PhD was funded by a grant from the University of Alicante. This research was funded by the POSINET2 project (Monitoring network of Posidonia oceanica meadow and climate change of the Murcia Region) of the Spanish Institute of Oceanography (CN IEO-CSIC), the Department of Fishery and Aquaculture of the Regional Ministry of Agriculture and Water of the Murcia Region and by the UMBRAL project (Responses of marine benthic macrophytes to stress: critical transitions, resilience and management opportunities) financed by the National Plan of Research of the Spanish Government (CTM2017-86695-C3-2-R) to R.J.M. The research was also supported by project 19-ESMARES2-ANG funded by the Ministry of Ecological Transition and Demographic Challenge of the Spanish government for the application of the Marine Strategy Framework Directive (MSFD) in Spanish waters

The role of competition and herbivory in biotic resistance against invaders: a synergistic effect

Invasive species pose a major threat to global diversity, and once they are well established their eradication typically becomes unfeasible. However, certain natural mechanisms can increase the resistance of native communities to invaders and can be used to guide effective management policies. Both competition and herbivory have been identified as potential biotic resistance mechanisms that can limit plant invasiveness, but it is still under debate to what extent they might be effective against well-established invaders. Surprisingly, whereas biotic mechanisms are known to interact strongly, most studies to date have examined single biotic mechanisms separately, which likely influences our understanding of the strength and effectiveness of biotic resistance against invaders. Here we use long-term field data, benthic assemblage sampling, and exclusion experiments to assess the effect of native assemblage complexity and herbivory on the invasion dynamics of a successful invasive species, the alga Caulerpa cylindracea. A higher complexity of the native algal assemblage limited C. cylindracea invasion, probably through competition by canopy-forming and erect algae. Additionally, high herbivory pressure by the fish Sarpa salpa reduced C. cylindracea abundance by more than four times. However, long-term data of the invasion reflects that biotic resistance strength can vary across the invasion process and it is only where high assemblage complexity is concomitant with high herbivory pressure, that the most significant limitation is observed (synergistic effect). Overall, the findings reported in this study highlight that neglecting the interactions between biotic mechanisms during invasive processes and restricting the studied time scales may lead to underestimations of the true capacity of native assemblages to develop resistance to invaders.Versión del editor4,84

The modulation of leaf metabolism plays a role in salt tolerance of Cymodocea nodosa exposed to hypersaline stress in mesocosms

Applying proteomics, we tested the physiological responses of the euryhaline seagrass Cymodocea nodosa to deliberate manipulation of salinity in a mesocosm system. Plants were subjected to a chronic hypersaline condition (43 psu) to compare protein expression and plant photochemistry responses after 15 and 30 days of exposure with those of plants cultured under normal/ambient saline conditions (37 psu). Results showed a general decline in the expression level of leaf proteins in hypersaline stressed plants, with more intense reductions after long-lasting exposure. Specifically, the carbon-fixing enzyme RuBisCo displayed a lower accumulation level in stressed plants relative to controls. In contrast, the key enzymes involved in the regulation of glycolysis, cytosolic glyceraldehyde-3-phosphate dehydrogenase, enolase 2 and triose-phosphate isomerase, showed significantly higher accumulation levels. These responses suggested a shift in carbon metabolism in stressed plants. Hypersaline stress also induced a significant alteration of the photosynthetic physiology of C. nodosa by means of a downregulation in structural proteins and enzymes of both PSII and PSI. However we found an over-expression of the cytochrome b559 alpha subunit of the PSII initial complex, which is a receptor for the PSII core proteins involved in biogenesis or repair processes and therefore potentially involved in the absence of effects at the photochemical level of stressed plants. As expected hypersalinity also affects vacuolar metabolism by increasing the leaf cell turgor pressure and enhancing the up-take of Na+ by overaccumulating the tonoplast specific intrinsic protein pyrophosphate-energized inorganic pyrophosphatase (H(+)-PPase) coupled to the Na+/H+-antiporter. The modulation of carbon metabolism and the enhancement of vacuole capacity in Na+ sequestration and osmolarity changes are discussed in relation to salt tolerance of C. nodosa.Postprin

Photo-acclimatory thresholds anticipate sudden shifts in seagrass ecosystem state under reduced light conditions

Seagrass ecosystems usually respond in a nonlinear fashion to increasing pressures and environmental changes. Feedback mechanisms operating at the ecosystem level and involving multiple interactions among the seagrass meadow, its associated community and the physical environment are known to play a major role in such nonlinear responses. Phenotypic plasticity may also be important for buffering these ecological thresholds (i.e., regime shifts) as many physiological processes show nonlinear responses to gradual environmental changes, conferring the appearance of resistance before the effects at the organism and population levels are visible. However, the potential involvement of plant plasticity in driving catastrophic shifts in seagrass ecosystems has not yet been assessed. In this study, we conducted a manipulative 6-month light-gradient experiment in the field to capture nonlinearities of the physiological and population responses of the seagrass Cymodocea nodosa to gradual light reduction. The aim was to explore if and how the photo-acclimatory responses of shaded plants are translated to the population level and, hence, to the ecosystem level. Results showed that the seagrass population was rather stable under increasing shading levels through the activation of multilevel photo-acclimative responses, which are initiated with light reduction and modulated in proportion to shading intensity. The activation of photo-physiological and metabolic compensatory responses allowed shaded plants to sustain nearly constant plant productivity (metabolic carbon balance) along a range of shading levels before losing linearity and starting to decline. The species then activated plant- and meadow-scale photo-acclimative responses and drew on its energy reserves (rhizome carbohydrates) to confer additional population resilience. However, when the integration of all these buffering mechanisms failed to counterbalance the effects of extreme light limitation, the population collapsed, giving place to a phase shift from vegetated to bare sediments with catastrophic ecosystem outcomes. Our findings evidence that ecological thresholds in seagrass ecosystems under light limitation can be explained by the role of species’ compensatory responses in modulating population-level responses. The thresholds of these plastic responses anticipate the sudden loss of seagrass meadows with the potential to be used as early warning indicators signalling the imminent collapse of the ecosystem, which is of great value for the real-world management of seagrass ecosystems.En prens

Factors structuring microbial communities in highly impacted coastal marine sediments (Mar Menor lagoon, SE Spain)

Coastal marine lagoons are environments highly vulnerable to anthropogenic pressures such as agriculture nutrient loading or runoff from metalliferous mining. Sediment microorganisms, which are key components in the biogeochemical cycles, can help attenuate these impacts by accumulating nutrients and pollutants. The Mar Menor, located in the southeast of Spain, is an example of a coastal lagoon strongly altered by anthropic pressures, but the microbial community inhabiting its sediments remains unknown. Here, we describe the sediment prokaryotic communities along a wide range of environmental conditions in the lagoon, revealing that microbial communities were highly heterogeneous among stations, although a core microbiome was detected. The microbiota was dominated by Delta- and Gammaproteobacteria and members of the Bacteroidia class. Additionally, several uncultured groups such as Asgardarchaeota were detected in relatively high proportions. Sediment texture, the presence of Caulerpa or Cymodocea, depth, and geographic location were among the most important factors structuring microbial assemblages. Furthermore, microbial communities in the stations with the highest concentrations of potentially toxic elements (Fe, Pb, As, Zn, and Cd) were less stable than those in the non-contaminated stations. This finding suggests that bacteria colonizing heavily contaminated stations are specialists sensitive to change.The study of the microbial communities has been carried out within the project “Metafluidics” and it was funded by the European Union’s framework program Horizon 2020 (LEIT-BIO-2015-685474 to JA). Samplings were supported by the projects MEMM (financed by the Spanish Institute of Oceanography), 19-ESMARES2-ANG (financed by the Spanish Ministry of Ecological Transition and Demographic Challenge), and BIOFOM (Ref. TEC0004869 financed by the Regional Government of Murcia). M-DB and JB-E were supported by a contract within the Program Personal Técnico de Apoyo funded by the Ministerio de Economía y Competitividad. BA-R was also supported by the ACIF fellow of the Generalitat Valenciana government

Long-term coexistence between the macroalga Caulerpa prolifera and the seagrass Cymodocea nodosa in a Mediterranean lagoon

En prensa1,51

Factors structuring microbial communities in highly impacted coastal marine sediments (Mar Menor lagoon, SE Spain)

Coastal marine lagoons are environments highly vulnerable to anthropogenic pressures such as agriculture nutrient loading or runoff from metalliferous mining. Sediment microorganisms, which are key components in the biogeochemical cycles, can help attenuate these impacts by accumulating nutrients and pollutants. The Mar Menor, located in the southeast of Spain, is an example of a coastal lagoon strongly altered by anthropic pressures, but the microbial community inhabiting its sediments remains unknown. Here, we describe the sediment prokaryotic communities along a wide range of environmental conditions in the lagoon, revealing that microbial communities were highly heterogeneous among stations, although a core microbiome was detected. The microbiota was dominated by Delta- and Gammaproteobacteria and members of the Bacteroidia class. Additionally, several uncultured groups such as Asgardarchaeota were detected in relatively high proportions. Sediment texture, the presence of Caulerpa or Cymodocea, depth, and geographic location were among the most important factors structuring microbial assemblages. Furthermore, microbial communities in the stations with the highest concentrations of potentially toxic elements (Fe, Pb, As, Zn, and Cd) were less stable than those in the non-contaminated stations. This finding suggests that bacteria colonizing heavily contaminated stations are specialists sensitive to change