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Non-structural carbohydrates (NSCs) are energetic compounds that can be accumulated in tissues and mobilized during periods of unfavorable conditions to maintain the biological functions of plants. The balance of these biochemical compounds is controlled by environmental factors such as temperature and irradiance. Zostera noltei and Zostera marina find one of their southern distribution limits in southern Spain, where relatively high seawater temperatures are reached during summer (23–24 °C). To better understand the effects of elevated temperatures on the concentration of NSCs, we conducted a seasonal study at Cadiz Bay, representing warm-adapted populations of these species. Our results showed a bimodal pattern in both species, with the highest NSC content observed in December and June, followed by a depletion in March and August. In addition, the NSC content observed in the leaves of Z. noltei (71.26 ± 30.77 mg g−1 dry weight) was higher than in the rhizomes and roots (52.14 ± 38.86 mg g−1 DW). The observed patterns suggest that these species accumulated NSCs to cope with periods of unfavorable environmental conditions. We also suggest that the limited concentration of NSCs in Z. noltei rhizomes and roots indicates that this population may be suffering physiological stress.

Seagrasses, which are marine flowering plants, provide numerous ecological services and goods. Zostera marina is the most widely distributed seagrass in temperate regions of the northern hemisphere, tolerant of a wide range of environmental conditions. This study aimed to (i) examine seasonal trends and correlations between key seagrass traits such as biomass production and biochemical composition, and (ii) compare seasonal adaptation of two ecotypes of Z. marina exposed to similar environmental conditions on the west coast of Ireland. During summer, plants accumulated higher levels of energetic compounds and levels of unsaturated fatty acids (FAs) decreased. Conversely, the opposite trend was observed during colder months. These findings indicate a positive seasonal correlation between the production of non-structural carbohydrates and saturated fatty acids (SFAs), suggesting that seagrasses accumulate and utilize both energetic compounds simultaneously during favorable and unfavorable environmental conditions. The two ecotypes displayed differential seasonal responses by adjusting plant morphology and production, the utilization of energetic reserves, and modulating unsaturation levels of fatty acids in seagrass leaves. These results underscore the correlated seasonal responses of key compounds, capturing ecotype-specific environmental adaptations and ecological strategies, emphasizing the robust utility of these traits as a valuable eco-physiological tool.

Abstract Background Halophila stipulacea seagrass meadows are an ecologically important and threatened component of the ecosystem in the Gulf of Aqaba. Recent studies have demonstrated correlated geographic patterns for leaf epiphytic community composition and leaf morphology, also coinciding with different levels of water turbidity and nutrient concentrations. Based on these observations, workers have suggested an environmental microbial fingerprint, which may reflect various environmental stress factors seagrasses have experienced, and may add a holobiont level of plasticity to seagrasses, assisting their acclimation to changing environments and through range expansion. However, it is difficult to tease apart environmental effects from host-diversity dependent effects, which have covaried in field studies, although this is required in order to establish that differences in microbial community compositions among sites are driven by environmental conditions rather than by features governed by the host. Results In this study we carried out a mesocosm experiment, in which we studied the effects of warming and nutrient stress on the composition of epiphytic bacterial communities and on some phenological traits. We studied H. stipulacea collected from two different meadows in the Gulf of Aqaba, representing differences in the host and the environment alike. We found that the source site from which seagrasses were collected was the major factor governing seagrass phenology, although heat increased shoot mortality and nutrient loading delayed new shoot emergence. Bacterial diversity, however, mostly depended on the environmental conditions. The most prominent pattern was the increase in Rhodobacteraceae under nutrient stress without heat stress, along with an increase in Microtrichaceae. Together, the two taxa have the potential to maintain nitrate reduction followed by an anammox process, which can together buffer the increase in nutrient concentrations across the leaf surface. Conclusions Our results thus corroborate the existence of environmental microbial fingerprints, which are independent from the host diversity, and support the notion of a holobiont level plasticity, both important to understand and monitor H. stipulacea ecology under the changing climate.

The Gulf of Aqaba (GoA; northern Red Sea) supports extensive seagrass meadows, dominated by the small tropical seagrass species, Halophila stipulacea. Due to its semi-closed structure, in the GoA, regional nutrient loading and global warming are considered the biggest threats to local seagrass meadows, and their combination can potentially amplify their negative impacts. Using a seagrass-dedicated mesocosm, we exposed two seagrass populations with different local “nutrient history” to control (27 °C) and simulated warming (31 °C), with and without nutrients (20 µM DIN). Following four weeks of these treatments (“stress phase”), all plants were returned to control conditions (“recovery phase”) for another three weeks. Results showed that exposure to only thermal stress favoured growth, compared to exposure to only nutrient increase that reduced Fv/Fm and growth but favoured algae proliferation. Exposure to the combined thermal and nutrient stress, negatively affected seagrass performance resulting in high mortality observed after four weeks of combined exposure. The negative effects of combined stressors were stronger in populations with low “nutrient history”. Additionally, we propose two novel fatty acid (FA) biomarkers, one based on FA unsaturation, 16:3n-3/16:2n-6, and the other on FA elongation processes, 18:2n-6/16:2n-6. Fatty acid analyses showed a significant decrease in 16:3n-3/16:2n-6 and 18:3n-3/18:2n-6 with increases in temperature and nutrients; a more drastic decline was found under the interaction of both stressors. Our results point out that C16 PUFAs, that are synthesized within the “prokaryotic pathway”, are more sensitive to thermal and the combined thermal + nutrients stressors than C18 PUFAs, which are synthesized within the “eukaryotic pathway”. In general, following a month of control conditions, a clear recovery of most of the seagrass descriptors was observed, highlighting the great capability of Halophila stipulacea to recover from stress conditions. Our results have important ecological and management implications to the seagrass meadows in the GoA and elsewhere. For seagrasses to survive climate change, managers must put efforts into limiting other stressors such as eutrophication that would potentially reduce the seagrass resilience to climate change.

Posidonia oceanica is an endemic seagrass species from the Mediterranean Sea that provides critical ecological services to coastal environments. This species is distributed from the Turkish to the Spanish coast, where its westernmost record was documented in Punta Chullera, Malaga (36°18′36.45′′ N, 5°14′54.31′′ W). Nevertheless, previous studies suggested that its distribution was even further west, although these populations were never described. In this study, we documented and characterised the only known P. oceanica population on the coast of Cadiz, in Cala Sardina (36°18′38.80′′ N, 5°15′15.13′′ W). The newly documented population of P. oceanica presented a fragmented structure, consisting of nine patches found in a rocky shallow area surrounded by the invasive algae Rugulopteryx okamurae, with a total size of 61.14 m2. Shoots had a relatively small size (21.0 ± 2.9 cm) in comparison with centrally-distributed populations. The relatively small size of the plants, alongside the observed low shoot density (437 ± 42 shoots m−2) and leaf area index (4.8 ± 0.7 m2 m−2), may indicate that this meadow could be exposed to sub-optimal environmental conditions for plant development. By contrast, the meadow showed relatively high production rates (0.03 ± 0.01 leaf day−1 shoot−1) in comparison with other Mediterranean populations. The percentage of carbon in plant leaves was 38.73 ± 1.38%, while the nitrogen and C/N were 1.38 ± 0.37% and 29.93 ± 6.57, respectively. The documentation of this meadow extends the distribution of this species to the Mediterranean coast of Cadiz, making this region the place with the highest seagrass biodiversity (four species) in the Iberian Peninsula, and potentially in Europe. This exploratory study provides a baseline to examine the potential effects of climate change, anthropogenic disturbances or the presence of invasive species.

Increases in seawater temperature and reduction in light quality have emerged as some of the most important threats to marine coastal communities including seagrass ecosystems. Temperate seagrasses, including Zostera marina, typically have pronounced seasonal cycles which modulate seagrass growth, physiology and reproductive effort. These marked temporal patterns can affect experimental seagrass responses to climate change effects depending on the seasons of the year in which the experiments are conducted. This study aimed at evaluating how seasonal acclimatization modulates productivity and biochemical responses of Zostera marina to experimental warming and irradiance reduction. Seagrass shoots were exposed to different temperatures (6, 12, 16, 20, and 24°C), combined with high (180 μmol photons m–2 s–1) and low (60 μmol photons m–2 s–1) light conditions across four seasons (spring: April, summer: July, and autumn: November 2015, and winter: January 2016). Plants exhibited similar temperature growth rates between 16 and 20°C; at 24°C, a drastic reduction in growth was observed; this was more accentuated in colder months and under low irradiance conditions. Higher leaf growth rates occurred in winter while the largest rhizomes were reached in experiments conducted in spring and summer. Increases in temperature induced a significant reduction in polyunsaturated fatty acids (PUFA), particularly omega-3 (n-3 PUFA). Our results highlight that temperate seagrass populations currently living under temperature limitation will be favored by future increases in sea surface temperature in terms of leaf and rhizome productivity. Together with results from this study on Z. marina from a temperate region, a wider review of the reported impacts of experimental warming indicates the likely reduction in some compounds of nutritional importance for higher trophic levels in seagrass leaves. Our results further demonstrate that data derived from laboratory-based studies investigating environmental stress on seagrass growth and acclimation, and their subsequent interpretation, are strongly influenced by seasonality and in situ conditions that precede any experimental exposure.

Halophila stipulacea is a small tropical seagrass, native to the Red Sea, Persian Gulf, and the Indian Ocean. It invaded the Mediterranean Sea 150 years ago as a Lessepsian migrant, but so far has remained in insulated, small populations across this basin. Surprisingly, in 2002 it was reported in the Caribbean Sea, where within less than two decades it spread to most of the Caribbean Island nations and reaching the South American continent. Unlike its invasion of Mediterranean, in the Caribbean H. stipulacea creates large, continuous populations in many areas. Reports from the Caribbean demonstrated the invasiveness of H. stipulacea by showing that it displaces local Caribbean seagrass species. The motivation for this review comes from the necessity to unify the existing knowledge on several aspects of this species in its native and invasive habitats, identify knowledge gaps and develop a critical strategy to understand its invasive capacity and implement an effective monitoring and conservation plan to mitigate its potential spread outside its native ranges. We systematically reviewed 164 studies related to H. stipulacea to create the “Halophila stipulacea database.” This allowed us to evaluate the current biological, ecological, physiological, biochemical, and molecular knowledge of H. stipulacea in its native and invasive ranges. Here we (i) discuss the possible environmental conditions and plant mechanisms involved in its invasiveness, (ii) assess the impact of H. stipulacea on native seagrasses and ecosystem functions in the invaded regions, (iii) predict the ability of this species to invade European and transoceanic coastal waters, (iv) identify knowledge gaps that should be addressed to better understand the biology and ecology of this species both in its native and non-native habitats, which would improve our ability to predict H. stipulacea's potential to expand into new areas in the future. Considering the predicted climate change scenarios and exponential human pressures on coastal areas, we stress the need for coordinated global monitoring and mapping efforts that will record changes in H. stipulacea and its associated communities over time, across its native, invasive and prospective distributional ranges. This will require the involvement of biologists, ecologists, economists, modelers, managers, and local stakeholders.