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Marine heatwaves recurrence aggravates thermal stress in the surfgrass Phyllospadix scouleri
Abstract and Figures
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.
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... 27 In the case of surfgrasses, changes in total phenols of P. torreyi and P. scouleri from Baja California (Mexico) have been related to their acclimation and stress responses to emersion 16 and marine heatwaves. 22, 38 The stable high concentration of phenolic compounds has been linked to the antioxidant defense of P. torreyi facing emersion during low tides. 16 In P. scouleri, marine heatwaves have led to a decline in phenolic content and antioxidant responses, which in turn has been linked to plant metabolic disruption and oxidative damage. ...
... 16 In P. scouleri, marine heatwaves have led to a decline in phenolic content and antioxidant responses, which in turn has been linked to plant metabolic disruption and oxidative damage. 38 Although our results represent an important advance in the knowledge of the sulfated flavonoid profiles of surfgrasses, further research is needed to better understand their biosynthesis, accumulation dynamics, and physiological/ ecological functions. Phyllospadix is considered one of the most divergent seagrass genera due to its unique physical habitat and adaptive physiological and morphological characteristics. ...
Sulfated flavonoids, a class of polyphenols integral to plant secondary metabolism and chemical defense, exhibit notable pharmacological potential. Seagrasses, marine angiosperms with critical ecological and socioeconomic roles, often accumulate these compounds in high concentrations. However, their complex chemical profiles�including closely related sulfated flavonoids� are challenging to characterize due to potential degradation during extraction. This study provides the first comprehensive analysis of sulfated flavonoids in Phyllospadix scouleri alongside a comparative analysis of P. torreyi. The Phyllospadix genus, known for forming productive intertidal meadows on rocky Pacific coastlines of North America, serves as a valuable model for understanding flavonoid diversity and adaptation in marine environments. From P. scouleri foliar tissues, we isolated and identified 1 phenolic acid and 15 sulfated flavonoids (HPLC-DAD, NMR, LC-MS), including previously undescribed 6-hydroxyflavonoid disulfates and monosulfates, and flavonoids not earlier reported for the genus. Lower amounts of sulfated glycosides were also tentatively identified in both species for the first time. The flavonoid profiles showed clear species-specific patterns: P. scouleri primarily produced 6-hydroxyflavonoids (70%), while P. torreyi favored 5-and 6-methoxyflavonoids (60 and 70%). Samples collected from nearby locations in May 2024 from both species showed similar flavonoid concentrations (∼20 mg/g DW) and comparable ratios between total flavonoids and rosmarinic acid (∼6:1). P. torreyi exhibited more disulfated flavonoids (84.3%) than monosulfated types (11.9%), whereas P. scouleri had 25.2% disulfated and 66.5% monosulfated flavonoids. Given the proven link between phenolic compounds and the physiological acclimation of surfgrasses to emersion during intertidal periods, as well as to marine heatwaves, this study provides a robust baseline for further research into the basic chemical ecology of these compounds and their responses to climate change.
... While initial research revealed physiological responses to elevated temperatures, there is a growing recognition of the need for a nuanced understanding of stress in natural environments, often involving repeated episodes (Fox-Kemper, 2021). The consequences of persistent or recurrent warming events on seagrasses are relatively understudied but hold significance in elucidating their resilience mechanisms (DuBois et al., 2020; Saha et al., 2020;Vivanco-Bercovich et al., 2024). Such research can offer valuable insights into whether repeated stress induces acclimation, thereby enhancing resilience, or exacerbates negative impacts, leading to a deterioration in seagrass health. ...
Ocean warming has both direct physiological and indirect ecological consequences for marine organisms. Sessile animals may be particularly vulnerable to anomalous warming given constraints in food acquisition and reproduction imposed by sessility. In temperate reef ecosystems, sessile suspension feeding invertebrates provide food for an array of mobile species and act as a critical trophic link between the plankton and the benthos. Using 14 years of seasonal benthic community data across five coastal reefs, we evaluated how communities of sessile invertebrates in southern California kelp forests responded to the "Blob", a period of anomalously high temperatures and low phytoplankton production. We show that this event had prolonged consequences for kelp forest ecosystems. Changes to community structure, including species invasions, have persisted six years post-Blob, suggesting that a climate-driven shift in California kelp forests is underway.
Seagrasses are remarkable plants that have adapted to live in a marine environment. They form extensive meadows found globally that bioengineer their local environments and preserve the coastal seascape. With the increasing realization of the planetary emergency that we face, there is growing interest in using seagrasses as a nature-based solution for greenhouse gas mitigation. However, seagrass sensitivity to stressors is acute, and in many places, the risk of loss and degradation persists. If the ecological state of seagrasses remains compromised, then their ability to contribute to nature-based solutions for the climate emergency and biodiversity crisis remains in doubt. We examine the major ecological role that seagrasses play and how rethinking their conservation is critical to understanding their part in fighting our planetary emergency.
The California Current Marine Ecosystem is a highly productive system that exhibits strong natural variability and vulnerability to anthropogenic climate trends. Relating projections of ocean change to biological sensitivities requires detailed synthesis of experimental results. Here, we combine measured biological sensitivities with high‐resolution climate projections of key variables (temperature, oxygen, and pCO2) to identify the direction, magnitude, and spatial distribution of organism‐scale vulnerabilities to multiple axes of projected ocean change. Among 12 selected species of cultural and economic importance, we find that all are sensitive to projected changes in ocean conditions through responses that affect individual performance or population processes. Response indices were largest in the northern region and inner shelf. While performance traits generally increased with projected changes, fitness traits generally decreased, indicating that concurrent stresses can lead to fitness loss. For two species, combining sensitivities to temperature and oxygen changes through the Metabolic Index shows how aerobic habitat availability could be compressed under future conditions. Our results suggest substantial and specific ecological susceptibility in the next 80 years, including potential regional loss of canopy‐forming kelp, changes in nearshore food webs caused by declining rates of survival among red urchins, Dungeness crab, and razor clams, and loss of aerobic habitat for anchovy and pink shrimp. We also highlight fillable gaps in knowledge, including specific physiological responses to stressors, variation in responses across life stages, and responses to multistressor combinations. These findings strengthen the case for filling information gaps with experiments focused on fitness‐related responses and those that can be used to parameterize integrative physiological models, and suggest that the CCME is susceptible to substantial changes to ecosystem structure and function within this century.
Climate change is causing an increase in the frequency and intensity of marine heatwaves (MHWs) and mass mortality events (MMEs) of marine organisms are one of their main ecological impacts. Here, we show that during the 2015–2019 period, the Mediterranean Sea has experienced exceptional thermal conditions resulting in the onset of five consecutive years of widespread MMEs across the basin. These MMEs affected thousands of kilometers of coastline from the surface to 45 m, across a range of marine habitats and taxa (50 taxa across 8 phyla). Significant relationships were found between the incidence of MMEs and the heat exposure associated with MHWs observed both at the surface and across depths. Our findings reveal that the Mediterranean Sea is experiencing an acceleration of the ecological impacts of MHWs which poses an unprecedented threat to its ecosystems' health and functioning. Overall, we show that increasing the resolution of empirical observation is critical to enhancing our ability to more effectively understand and manage the consequences of climate change.
Marine heatwaves (MHWs) are increasing in frequency and intensity as part of climate change, yet their impact on seagrass is poorly known. The present work evaluated the physiological and morphological responses of Cymodocea nodosa to a MHW. C. nodosa shoots were transplanted into a mesocosm facility. To simulate a MHW, water temperature was raised from 20 to 28 °C, kept 7 days at 28 °C, cooled down back to 20 °C and then maintained at 20 °C during an 8-day recovery period. The potentially stressful effects of the simulated heatwave on the photosynthetic performance, antioxidative-stress level and area vs dry weight ratio of leaves were investigated. The maximum quantum yield of photosystem II (ΦPSII) increased during the heatwave, allowing the plants to maintain their photosynthetic activity at control level. Negative effects on the photosynthetic performance and leaf biomass of C. nodosa were observed during the recovery period. No significant oxidative stress was observed throughout the experiment. Overall, although C. nodosa showed a relative tolerance to MHWs compared to other species, its population in Ria Formosa is likely to be negatively affected by the forecasted climate change scenarios.
Marine heat waves (MHWs), prolonged discrete anomalously warm water events, have been increasing significantly in duration, intensity and frequency all over the world, and have been associated with a variety of impacts including alteration of ecosystem structure and function. This study assessed the effects of current and future MHWs on the Mediterranean seagrass Posidonia oceanica performance, also testing the importance of the thermal environment where the plant lives. The effects of current MHWs were studied through a mensurative experiment in a cold and in a warm site (West and NorthWest Sardinia, Italy, respectively). Future MHWs effects were tested through a manipulative experiment using P. oceanica shoots collected from the cold and warm sites and transplanted in a common garden in front of a power plant (North-West Sardinia): here plants were exposed to heat longer in duration and stronger in intensity than the natural MHWs of the last 20 years, resembling the future scenario. Morphological (total # of leaves, maximum leaf length, and percentage of total necrotic leaf length per shoot) and biochemical variables (leaf proteins, carbohydrates, and lipids) were considered. Plants had similar sublethal responses in both the experiments for most of the variables, revealing that current and future MHWs had similar effect types, but different in magnitude depending on the intensity of the waves: in general, the number of leaves, the maximum leaf length and lipid content decreased, while the leaf necrosis and carbohydrates increased. However, also the origin of the plants affected the results, corroborating the hypothesis that the thermal context the plants live affects their tolerance to the heat. Overall, this study provided evidence about the importance of biochemical variations, such as carbohydrate and lipid levels, as potentially good indicators of seagrass heat stress.
A better understanding of species and population responses to thermal stress is critical to predict changes in their distribution under warming scenarios. Seagrasses are a unique group of marine plants that play fundamental roles in marine environments and provide vital ecosystem services. Nevertheless, previous studies on seagrass thermal tolerance have focused exclusively on a handful of species, with the majority of these remaining virtually unexplored. Moreover, to date, no study has compared the response to thermal stress between northern and southern hemisphere seagrasses. Here, we conducted comparative mesocosm experiments using four seagrass species from the northern (i.e. Mediterranean: Posidonia oceanica, Cymodocea nodosa) and southern (i.e. Australia: Posidonia australis and Zostera muelleri) hemisphere as representative of two different life strategies, i.e. climax (P. oceanica, P. australis) and pioneer (C. nodosa, Z. muelleri). Plants acclimatized to the mesocosm conditions at ambient temperature (i.e. 26 °C) during a 5-week period, were exposed to a simulated marine heatwave (i.e. 32 °C) for 2 weeks. Measurements of plant responses, including photo-physiology, morphology, and pigment content, were performed at the end of the warming exposure. Results showed that warming had no significant effects on photosynthetic performances of northern hemisphere seagrasses while negatively impacted their southern hemisphere counterparts. Similarly, warming favored the growth of northern hemisphere plants, but strongly inhibited the development of southern hemisphere species. Furthermore, photo-physiological and pigment content results suggested pioneer seagrasses better dealt with warming than climax species. Our study provides more insights into the field of seagrass ecology and yields potential implication for future seagrass conservation and restoration activities.
Global climate change, specifically the intensification of marine heatwaves, affect seagrasses. In the Ria Formosa, saturating light intensities may aggravate heatwave effects on seagrasses, particularly during low spring tides. However, the photophysiological and antioxidant responses of seagrasses to such extreme events are poorly known. Here, we evaluated the responses of Cymodocea nodosa exposed at 20 °C and 40 °C and 150 and 450 μmol quanta m−2 s−1. After four-days, we analyzed (a) photosynthetic responses to irradiance, maximum photochemical efficiency (Fv/Fm), the effective quantum yield of photosystem II (ɸPSII); (b) soluble sugars and starch; (c) photosynthetic pigments; (d) antioxidant responses (ascorbate peroxidase, APX; oxygen radical absorbance capacity, ORAC, and antioxidant capacity, TEAC); (d) oxidative damage (malondialdehyde, MDA). After four days at 40 °C, C. nodosa showed relevant changes in photosynthetic pigments, independent of light intensity. Increased TEAC and APX indicated an “investment” in the control of reactive oxygen species levels. Dark respiration and starch concentration increased, but soluble sugar concentrations were not affected, suggesting higher CO2 assimilation. Our results show that C. nodosa adjusts its photophysiological processes to successfully handle thermal stress, even under saturating light, and draws a promising perspective for C. nodosa resilience under climate change scenarios.
Seagrass meadows deliver important ecosystem services such as nutrient cycling, enhanced biodiversity, and contribution to climate change mitigation and adaption through carbon sequestration and coastal protection. Seagrasses, however, are facing the impacts of ocean warming and marine heatwaves, which are altering their ecological structure and function. Shifts in species composition, mass mortality events, and loss of ecosystem complexity after sudden extreme climate events are increasingly common, weakening the ecosystem services they provide. In the west coast of Australia, Shark Bay holds between 0.7 and 2.4% of global seagrass extent (>4300 km²), but in the austral summer of 2010/2011, the Ningaloo El Niño marine heatwave resulted in the collapse of ~1300 km² of seagrass ecosystem extent. The loss of the seagrass canopy resulted in the erosion and the likely remineralization of ancient carbon stocks into 2–4 Tg CO2-eq over 6 years following seagrass loss, increasing emissions from land-use change in Australia by 4–8% per annum. Seagrass collapse at Shark Bay also impacted marine food webs, including dugongs, dolphins, cormorants, fish communities, and invertebrates. With increasing recurrence and intensity of marine heatwaves, seagrass resilience is being compromised, underlining the need to implement conservation strategies. Such strategies must precede irreversible climate change-driven tipping points in ecosystem functioning and collapse and result from synchronized efforts involving science, policy, and stakeholders. Management should aim to maintain or enhance the resilience of seagrasses, and using propagation material from heatwave-resistant meadows to restore impacted regions arises as a challenging but promising solution against climate change threats. Although scientific evidence points to severe impacts of extreme climate events on seagrass ecosystems, the occurrence of seagrass assemblages across the planet and the capacity of humans to modify the environment sheds some light on the capability of seagrasses to adapt to changing ecological niches.
Coastal oceans are particularly affected by rapid and extreme environmental changes with dramatic consequences for the entire ecosystem. Seagrasses are key ecosystem engineers or foundation species supporting diverse and highly 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 found that the implemented experimental approaches, whether performed with controlled or field experiments, provided 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.
Prolonged high-temperature extreme events in the ocean, marine heatwaves, can have severe and long-lasting impacts on marine ecosystems, fisheries and associated services. This study applies a marine heatwave framework to analyse a global sea surface temperature product and identify the most extreme events, based on their intensity, duration and spatial extent. Many of these events have yet to be described in terms of their physical attributes, generation mechanisms, or ecological impacts. Our synthesis identifies commonalities between marine heatwave characteristics and seasonality, links to the El Niño-Southern Oscillation, triggering processes and impacts on ocean productivity. The most intense events preferentially occur in summer, when climatological oceanic mixed layers are shallow and winds are weak, but at a time preceding climatological maximum sea surface temperatures. Most subtropical extreme marine heatwaves were triggered by persistent atmospheric high-pressure systems and anomalously weak wind speeds, associated with increased insolation, and reduced ocean heat losses. Furthermore, the most extreme events tended to coincide with reduced chlorophyll-a concentration at low and mid-latitudes. Understanding the importance of the oceanic background state, local and remote drivers and the ocean productivity response from past events are critical steps toward improving predictions of future marine heatwaves and their impacts.
The heat is on
Anthropogenic climate change is causing not only more episodes of historically high air temperatures but also more frequent spells of unusually increased ocean temperatures. Marine heatwaves, defined as periods of anomalously high regional surface ocean temperatures, have also become common in recent decades. Laufkötter et al. show that the frequency of these events has already increased more than 20-fold because of anthropogenic global warming, making marine heatwaves, which typically occurred once in hundreds to thousands of years in preindustrial times, likely to occur on an annual to decadal basis if the global average air temperature rises by 3°C.
Science , this issue p. 1621
Evolutionary theory predicts that clonal organisms are more susceptible to extinction than sexually reproducing organisms, due to low genetic variation and slow rates of evolution. In agreement, conservation management considers genetic variation as the ultimate measure of a population’s ability to survive over time. However, clonal plants are among the oldest living organisms on our planet. Here, we test the hypothesis that clonal seagrass meadows display epigenetic variation that complements genetic variation as a source of phenotypic variation. In a clonal meadow of the seagrass Zostera marina, we characterized DNA methylation among 42 shoots. We also sequenced the whole genome of 10 shoots to correlate methylation patterns with photosynthetic performance under exposure to and recovery from 27°C, while controlling for somatic mutations. Here, we show for the first time that clonal seagrass shoots display DNA methylation variation that is independent from underlying genetic variation, and associated with variation in photosynthetic performance under experimental conditions. It remains unknown to what degree this association could be influenced by epigenetic responses to transplantation-related stress, given that the methylomes showed a strong shift under acclimation to laboratory conditions. The lack of untreated control samples in the heat stress experiment did not allow us to distinguish methylome shifts induced by acclimation from such induced by heat stress. Notwithstanding, the co-variation in DNA methylation and photosynthetic performance may be linked via gene expression because methylation patterns varied in functionally relevant genes involved in photosynthesis, and in the repair and prevention of heat-induced protein damage. While genotypic diversity has been shown to enhance stress resilience in seagrass meadows, we suggest that epigenetic variation plays a similar role in meadows dominated by a single genotype. Consequently, conservation management of clonal plants should consider epigenetic variation as indicator of resilience and stability.
Mortality and shifts in species distributions are among the most obvious consequences of extreme climatic events. However, the sublethal effects of an extreme event can have persistent impacts throughout an individual’s lifetime and into future generations via within‐generation and transgenerational phenotypic plasticity. These changes can either confer resilience or increase susceptibility to subsequent stressful events, with impacts on population, community, and potentially ecosystem processes. Here, we show how a simulated extreme warming event causes persistent changes in the morphology and growth of a foundation species (eelgrass, Zostera marina) across multiple clonal generations and multiple years. The effect of previous parental exposure to warming increased aboveground biomass, shoot length, and aboveground–belowground biomass ratios while also greatly decreasing leaf growth rates. Long‐term increases in aboveground–belowground biomass ratios could indicate an adaptive clonal transgenerational response to warmer climates that reduces the burden of increased respiration in belowground biomass. These transgenerational responses were likely decoupled from clonal parent provisioning as rhizome size of clonal offspring was standardized at planting and rhizome starch reserves were not impacted by warming treatments. Future investigations into potential epigenetic mechanisms underpinning such clonal transgenerational plasticity will be necessary to understand the resilience of asexual foundation species to repeated extreme climatic events.
While thermal priming and the relative role of epigenetic modifications have been widely studied in terrestrial plants, their roles remain unexplored in seagrasses so far. Here, we experimentally compared the ability of two different functional types of seagrass species, dominant in the Southern hemisphere, climax species Posidonia australis and pioneer species Zostera muelleri, to acquire thermal-stress memory to better survive successive stressful thermal events. To this end, a two-heatwave experimental design was conducted in a mesocosm setup. Findings across levels of biological organization including the molecular (gene expression), physiological (photosynthetic performances and pigments content) and organismal (growth) levels provided the first evidence of thermal priming in seagrasses. Non-preheated plants suffered a significant reduction in photosynthetic capacity, leaf growth and chlorophyll a content, while preheated plants were able to cope better with the recurrent stressful event. Gene expression results demonstrated significant regulation of methylation-related genes in response to thermal stress, suggesting that epigenetic modifications could play a central role in seagrass thermal stress memory. In addition, we revealed some interspecific differences in thermal responses between the two different functional types of seagrass species. These results provide the first insights into thermal priming and relative epigenetic modifications in seagrasses paving the way for more comprehensive forecasting and management of thermal stress in these marine foundation species in an era of rapid environmental change.
The impact of global warming on the metabolic state of a species may be examined by either measuring physiological rates across a latitudinal gradient or by assessing short‐term responses under experimentally controlled temperature regimes. The combination of the two approaches is seldom used but it provides valuable information on an organism's responses to temperature at broader temporal and spatial scales while allowing the isolation of temperature effects from other environmental variables.
Here we used both approaches to assess the warming effects on the total acquisition of dissolved inorganic nitrogen (DIN; nitrate, ammonium) and organic N (DON; amino acids, peptides) by the globally widespread seagrass Zostera marina. DIN and DON uptake rates were measured in plants from three sites covering the species latitudinal distribution in Europe (Iceland, UK and Portugal). The responses of DIN and DON uptake rates of plants from the middle latitude (UK) to a latitudinal range of temperatures (8, 12 and 17°C) were also measured. We further examined the microbial uptake of DON along the latitudinal distribution and whether temperature is the main driver of that uptake.
Our results showed that warming greatly increased the total N uptake by Z. marina and also the relative contribution of DON to total N acquisition. The microbial uptake of DON increased towards warmer latitudes, and temperature was the main driver of these observations.
Ocean warming will increase the nitrogen demand of Z. marina and this demand may be met by an increasing uptake of organic nitrogen forms. This indicates that Z. marina, and probably other seagrass species, can be winners under global change as nitrogen uptake capacity will not limit growth driven by increased photosynthetic assimilation of CO2.
A free Plain Language Summary can be found within the Supporting Information of this article.
The increased occurrence of extreme climate events, such as marine heatwaves (MHWs), has resulted in substantial ecological impacts worldwide. To date, metrics of thermal stress within marine systems have focussed on coral communities, and less is known about measuring stress relevant to other primary producers, such as seagrasses. An extreme MHW occurred across the Western Australian coastline in the austral summer of 2010–2011, exposing marine communities to summer seawater temperatures 2–5°C warmer than average. Using a combination of satellite imagery and in situ assessments, we provide detailed maps of seagrass coverage across the entire Shark Bay World Heritage Area (ca. 13,000 km²) before (2002 and 2010) and after the MHW (2014 and 2016). Our temporal analysis of these maps documents the single largest loss in dense seagrass extent globally (1,310 km²) following an acute disturbance. Total change in seagrass extent was spatially heterogeneous, with the most extensive declines occurring in the Western Gulf, Wooramel Bank and Faure Sill. Spatial variation in seagrass loss was best explained by a model that included an interaction between two heat stress metrics, the most substantial loss occurring when degree heating weeks (DHWm) was ≥10 and the number of days exposed to extreme sea surface temperature during the MHW (DaysOver) was ≥94. Ground truthing at 622 points indicated that change in seagrass cover was predominantly due to loss of Amphibolis antarctica rather than Posidonia australis, the other prominent seagrass at Shark Bay. As seawater temperatures continue to rise and the incidence of MHWs increase globally, this work will provide a basis for identifying areas of meadow degradation, or stability and recovery, and potential areas of resilience.
Marine heatwaves have been observed worldwide and are expected to increase in both frequency and intensity due to climate change. Such events may cause ecosystem reconfigurations arising from species range contraction or redistribution, with ecological, economic and social implications. Macrophytes such as the brown seaweed Fucus vesiculosus and the seagrass Zostera marina are foundation species in many coastal ecosystems of the temperate northern hemisphere. Hence, their response to extreme events can potentially determine the fate of associated ecosystems. Macrophyte functioning is intimately linked to the maintenance of photosynthesis, growth and reproduction, and resistance against pathogens, epibionts and grazers. We investigated morphological, physiological, pathological and chemical defence responses of western Baltic Sea F. vesiculosus and Z. marina populations to simulated near‐natural marine heatwaves. Along with (a) the control, which constituted no heatwave but natural stochastic temperature variability (0HW), two treatments were applied: (b) two late‐spring heatwaves (June, July) followed by a summer heatwave (August; 3HW) and (c) a summer heatwave only (1HW). The 3HW treatment was applied to test whether preconditioning events can modulate the potential sensitivity to the summer heatwave. Despite the variety of responses measured in both species, only Z. marina growth was impaired by the accumulative heat stress imposed by the 3HW treatment. Photosynthetic rate, however, remained high after the last heatwave indicating potential for recovery. Only epibacterial abundance was significantly affected in F. vesiculosus. Hence both macrophytes, and in particular F. vesiculosus, seem to be fairly tolerant to short‐term marine heatwaves at least at the intensities applied in this experiment (up to 5°C above mean temperature over a period of 9 days). This may partly be due to the fact that F. vesiculosus grows in a highly variable environment, and may have a high phenotypic plasticity.
Analyses of the integrated seagrass response to depth support the previously documented low plasticity and consistent shade-adapted leaf physiology of a habitat-builder that dominates well-illuminated reef environments. Two structural responses, “canopy-opening” and “below-ground-mass-depletion”, govern the photoacclimatory response and facilitate, respectively, light penetration within the canopy and functional adjustments in whole-plant carbon balances. Conversely, “canopy-closing” may also explain dense canopies formed close to the waterline, as they provide shade and photoprotection to a susceptible leaf physiology under high-light. Canopy light attenuation is primarily regulated by the leaf area index (LAI), which is governed by changes in shoot size and density. Shoot density diminishes non-linearly with depth, while shoot size increases to a maximum followed by a decline. The initial increase in shoot size, which resembles a self-thinning response, increases LAI and meadow production in shallow depths. These seagrass structural adjustments have relevant ecological implications. Canopy-thinning allows macrophyte diversity to increase with depth, while seagrass production and carbon storage diminish exponentially, and are maximal only in a shallow coastal fringe. The results support the universality of plant self-thinning, from phytoplankton to complex canopies, likely the consequence of simple physical laws related to light limitation and pigment self-shading within photosynthetic structures and communities.
Global warming is increasingly affecting our biosphere. However, in addition to global warming, a panoply of local stressors caused by human activities is having a profound impact on our environment. The risk that these local stressors could modify the response of organisms to global warming has attracted interest and fostered research on their combined effect, especially with a view to identifying potential synergies. In coastal areas, where human activities are heavily concentrated, this scenario is particularly worrying, especially for foundation species such as seagrasses. In this study we explore these potential interactions in the seagrass Posidonia oceanica. This species is endemic to the Mediterranean Sea. It is well known that the Mediterranean is already experiencing the effects of global warming, especially in the form of heat waves, whose frequency and intensity are expected to increase in the coming decades. Moreover, this species is especially sensitive to stress and plays a key role as a foundation species. The aim of this work is thus to evaluate plant responses (in terms of photosynthetic efficiency and growth) to the combined effects of short-term temperature increases and ammonium additions.To achieve this, we conducted a mesocosm experiment in which plants were exposed to three thermal treatments (20°C, 30°C and 35°C) and three ammonium concentrations (ambient, 30 μM and 120 μM) in a full factorial experiment. We assessed plant performance by measuring chlorophyll fluorescence variables (maximum quantum yield (Fv/Fm), effective quantum yield of photosystem II (ΔF/Fm’), maximum electron transport rate (ETRmax) and non-photochemical quenching (NPQ)), shoot growth rate and leaf necrosis incidence. At ambient ammonium concentrations, P. oceanica tolerates short-term temperature increases up to 30°C. However, at 35°C, the plant loses functionality as indicated by a decrease in photosynthetic performance, an inhibition of plant growth and an increase of the necrosis incidence in leaves. On the other hand, ammonium additions at control temperatures showed only a minor effect on seagrass performance. However, the combined effects of warming and ammonium were much worse than those of each stressor in isolation, given that photosynthetic parameters and, above all, leaf growth were affected. This serves as a warning that the impact of global warming could be even worse than expected (based on temperature-only approaches) in environments that are already subject to eutrophication, especially in persistent seagrass species living in oligotrophic environments.
Climate change is increasing the frequency and severity of marine heatwaves. A recent extreme warming event (2014–2016) of unprecedented magnitude and duration in the California Current System allowed us to evaluate the response of the kelp forest community near its southern (warm) distribution limit. We obtained sea surface temperatures for the northern Pacific of Baja California, Mexico, and collected kelp forest community data at three islands, before and after the warming event. The warming was the most intense and persistent event observed to date, with low-pass anomalies 1°C warmer than the previous extremes during the 1982–1984 and 1997–1998 El Niños. The period between 2014 and 2017 accounted for ∼50% of marine heatwaves days in the past 37 years, with the highest maximum temperature intensities peaking at 5.9°C above average temperatures for the period. We found significant declines in the number of Macrocystis pyrifera individuals, except at the northernmost island, and corresponding declines in the number of fronds per kelp individual. We also found significant changes in the community structure associated with the kelp beds: half of the fish and invertebrate species disappeared after the marine heatwaves, species with warmer affinities appeared or increased their abundance, and introduced algae, previously absent, appeared at all islands. Changes in subcanopy and understory algal assemblages were also evident; however, the response varied among islands. These results suggest that the effect of global warming can be more apparent in sensitive species, such as sessile invertebrates, and that warming-related impacts have the potential to facilitate the establishment of tropical and invasive species.
Marine macrophytes are the foundation of algal forests and seagrass meadows–some of the most productive and diverse coastal marine ecosystems on the planet. These ecosystems provide nursery grounds and food for fish and invertebrates, coastline protection from erosion, carbon sequestration, and nutrient fixation. For marine macrophytes, temperature is generally the most important range limiting factor, and ocean warming is considered the most severe threat among global climate change factors. Ocean warming induced losses of dominant macrophytes along their equatorial range edges, as well as range extensions into polar regions, are predicted and already documented. While adaptive evolution based on genetic change is considered too slow to keep pace with the increasing rate of anthropogenic environmental changes, rapid adaptation may come about through a set of non-genetic mechanisms involving the functional composition of the associated microbiome, as well as epigenetic modification of the genome and its regulatory effect on gene expression and the activity of transposable elements. While research in terrestrial plants demonstrates that the integration of non-genetic mechanisms provide a more holistic picture of a species' evolutionary potential, research in marine systems is lagging behind. Here, we aim to review the potential of marine macrophytes to acclimatize and adapt to major climate change effects via intraspecific variation at the genetic, epigenetic, and microbiome levels. All three levels create phenotypic variation that may either enhance fitness within individuals (plasticity) or be subject to selection and ultimately, adaptation. We review three of the most important phenotypic variations in a climate change context, including physiological variation, variation in propagation success, and in herbivore resistance. Integrating different levels of plasticity, and adaptability into ecological models will allow to obtain a more holistic understanding of trait variation and a realistic assessment of the future performance and distribution of marine macrophytes. Such multi-disciplinary approach that integrates various levels of intraspecific variation, and their effect on phenotypic and physiological variation, is of crucial importance for the effective management and conservation of seagrasses and macroalgae under climate change.
Coastal upwelling ecosystems are among the most productive ecosystems in the world, meaning that their response to climate change is of critical importance. Our understanding of climate change impacts on marine ecosystems is largely limited to the open ocean, mainly because coastal upwelling is poorly reproduced by current earth system models. Here, a high-resolution model is used to examine the response of nutrients and plankton dynamics to future climate change in the California Current System (CCS). The results show increased upwelling intensity associated with stronger alongshore winds in the coastal region, and enhanced upper-ocean stratification in both the CCS and open ocean. Warming of the open ocean forces isotherms downwards, where they make contact with water masses with higher nutrient concentrations, thereby enhancing the nutrient flux to the deep source waters of the CCS. Increased winds and eddy activity further facilitate upward nutrient transport to the euphotic zone. However, the plankton community exhibits a complex and nonlinear response to increased nutrient input, as the food web dynamics tend to interact differently. This analysis highlights the difficulty in understanding how the marine ecosystem responds to a future warming climate, given to range of relevant processes operating at different scales.
Global warming may exert diverging effects on eelgrass (Zostera marina L.) populations originating from the northern versus the central part of the distribution range and on populations growing at saturating versus limiting light. We experimentally examined growth and physiological temperature responses of 3 eelgrass populations adapted to different temperature regimes in subarctic Greenland (2 populations) and in Denmark (1 population). Shoots were incubated at 5 different temperatures (10, 15, 20, 25 and 28°C) for 15 to 16 d at a saturating irradiance (200 μmol m−2 s−1) and one of the populations was also incubated at a limited irradiance of 50 μmol m−2 s−1. All populations exhibited optimum temperatures of 20 to 25°C for photosynthesis and growth under saturating light, while light limitation reduced the optimum by 5 to 10°C. When compared at their respective in situ summer temperature (i.e. 10, 15 and 20°C), all populations exhibited similar relative growth rates, indicating a capacity for local adaptation. The 2 subarctic populations exhibited higher activation energy for growth and, hence, greater responsiveness to warming than the centrally located population. However, subarctic populations were also more sensitive to extreme high temperatures, showing faster increases in respiration rates and declines in photosynthesis. Sensitivity to warming varied across light conditions with light-limited plants being most vulnerable to extreme temperatures, causing a negative carbon budget. In conclusion, projected warming would stimulate the performance of subarctic eelgrass populations but could eventually compromise populations in the center of the distribution range, which currently grow close to their temperature optimum.
KEY WORDS: Experimental warming · Latitude comparison · Production · Energy activation · Photosynthetic response · Greenland · Denmark · Seagrass · Zostera marina
The analysis of the variation of the capacity and efficiency of photosynthetic tissues to collect solar energy is fundamental to understand the differences among species in their ability to transform this energy into organic molecules. This analysis may also help to understand natural changes in species distribution and/or abundance, and differences in species ability to colonize contrasting light environments or respond to environmental changes. Unfortunately, the challenge that optical determinations on highly dispersive samples represent has strongly limited the progression of this analysis on multicellular tissues, limiting our knowledge of the role that optical properties of photosynthetic tissues may play in the optimization of photosynthesis and growth of benthonic primary producers. The aim of this study is to stimulate the use of optical tools in marine eco-physiology, offering a succinct description of the more convenient tools and also solutions to resolve the more common technical difficulties that arise while performing optical determinations on highly dispersive samples. Our study focuses on two-dimensional (2D-) parameters: absorptance, transmittance, and reflectance, and illustrates with correct and incorrect examples, specific problems and their respective solutions. We also offer a general view of the broad variation in light absorption shown by photosynthetic structures of marine primary producers, and its low association with pigment content. The ecological and evolutionary functional implications of this variability deserve to be investigated across different taxa, populations, and marine environments.
Climate-driven changes are altering production and functioning of biotic assemblages in terrestrial and aquatic environments. In temperate coastal waters, rising sea temperatures, warm water anomalies and poleward shifts in the distribution of tropical herbivores have had a detrimental effect on algal forests. We develop generalized scenarios of this form of tropicalization and its potential effects on the structure and functioning of globally significant and threatened seagrass ecosystems, through poleward shifts in tropical seagrasses and herbivores. Initially, we expect tropical herbivorous fishes to establish in temperate seagrass meadows, followed later by megafauna. Tropical seagrasses are likely to establish later, delayed by more limited dispersal abilities. Ultimately, food webs are likely to shift from primarily seagrass-detritus to more direct-consumption-based systems, thereby affecting a range of important ecosystem services that seagrasses provide, including their nursery habitat role for fishery species, carbon sequestration, and the provision of organic matter to other ecosystems in temperate regions.
The increase in extreme heat events associated to global warming threatens seagrass ecosystems, likely by affecting key plant physiological processes such as photosynthesis and respiration. Understanding species’ ability to acclimate to warming is crucial to better predict their future trends. Here, we study tolerance to warming in two key Mediterranean seagrasses, Posidonia oceanica and Cymodocea nodosa. Stress responses of shallow and deep plants were followed during and after short-term heat exposure in mesocosms by coupling photo-physiological measures with analysis of expression of photosynthesis and stress-related genes. Contrasting tolerance and capacity to heat acclimation were shown by shallow and deep P. oceanica ecotypes. While shallow plants acclimated through respiratory homeostasis and activation of photo-protective mechanisms, deep ones experienced photosynthetic injury and impaired carbon balance. This suggests that P. oceanica ecotypes are thermally adapted to local conditions and that Mediterranean warming will likely diversely affect deep and shallow meadow stands. On the other hand, contrasting mechanisms of heat-acclimation were adopted by the two species. P. oceanica regulates photosynthesis and respiration at the level of control plants while C. nodosa balances both processes at enhanced rates. These acclimation discrepancies are discussed in relation to inherent attributes of the two species.
Foundation species are important components of ecosystems because they provide habitat and ameliorate stressful conditions for residents. Comparisons of congeneric foundation species have mostly been limited to comparisons of native and invasive species, with less attention paid to multiple native species. Surfgrasses (Phyllospadix spp.) are ubiquitous foundation species on the coast of Oregon, USA, protecting resident invertebrates from waves and providing them with access to sandy substrate in an otherwise rocky habitat. Two native surfgrass species, P. scouleri and P. serrulatus, have superficially similar morphological characteristics and co-occur within the same rocky intertidal zones. We investigated whether these native congeneric species function similarly as foundation species by comparing the 2 species' morphology, sediment accretion and associated resident macro invertebrates at 3 capes that vary in oceanographic conditions. The results show that although the macroinvertebrate abundance was the same between surfgrass species, macroinvertebrate species richness, composition and functional groups varied considerably, with more infauna and deposit feeders found within P. serrulatus. P. serrulatus also had fewer tillers and rhizomes, and lower biomass per given area, but greater sediment accretion than its congener P. scouleri. One notably strong result was the difference in macroinvertebrate abundance among capes, with Cape Perpetua having 2.5-3 times more animals per given area than Capes Foulweather or Blanco. Overall, we conclude that although the 2 co-occurring surfgrass congeners provided functionally different habitat for resident macro invertebrates, regional oceanographic processes (i.e. upwelling and productivity) may be more influential in determining the overall abundance and productivity of these diverse animal communities.
Climate models predict increases in frequency of summer heat waves. In Europe, such events have already caused declines in seagrass meadows, highlighting the importance of short-term responses of local communities to climate stress. Understanding the variability among populations along the European thermal gradient in response to heat waves is crucial for seagrass conservation and management. Using a mesocosm we compared effects of a simulated heat wave on the photophysiology of Zostera marina populations coming from low (43 degrees N, Adriatic Sea) and high latitudes (56 degrees N, North and Baltic Seas). Measurements before, during and up to 4 wk after the heat wave included photophysiological parameters derived from light response curves generated by PAM fluorometry and gene expression using qRT-PCR. In all 3 populations, initial exposures to thermal stress were characterized by increases in dark adapted effective quantum yield (Y-0), maximum electron transfer rate of PSII (ETRmax) and slope of the light response curve (alpha), coinciding with upregulations of the gene superoxidase dismutase [Mn]. With continuation of the heat wave these initial effects disappeared, demonstrated by declines in Y-0, ETRmax and alpha relative to controls. Z. marina from the Adriatic suffered from the simulated heat wave as much as its high-latitude counterparts. However, we also demonstrate slight photophysiological differences between the populations during the recovery phase, where performance of high-latitude populations continued declining even after water temperatures returned to control levels, while photochemical activity fully recovered in the Adriatic population. These results might draw the attention of future studies and seagrass conservation efforts.
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.
This study aimed to elucidate for the first time the combined effects of marine heatwaves (MHWs) and light limitation simulated in mesocosm on critical physiological descriptors of the surfgrass Phyllospadix torreyi, which constitutes highly productive meadows along the intertidal and subtidal rocky shores of the Pacific coast of North America. Our results revealed that short-term exposure (~7 days) to extreme thermal anomalies of +9 °C had positive effects on the photosynthetic capacities of P. torreyi, as indicated by increments in maximum photosynthetic rates, photosynthetic efficiency (α), maximum electron transport rate, and effective quantum yield. Despite that its photosynthetic performance was enhanced, exposure to warming caused a decrease in its internal carbon reserves (i.e. energy status), likely as a consequence of carbon mobilization/utilization to activate heat-stress responses. Plants exposed to light limitation (i.e. sub-saturating irradiance of 30 μmol photon m⁻² s⁻¹) generally exhibited an increase in α and/or a decrease in respiration, which ultimately allowed for a reduction in plant compensation irradiance. The combination of low light and seawater warming resulted in a decrease in non-structural carbohydrates content, daily net-productivity, and leaf growth rates. Gross photosynthetic rates at control saturating irradiance exhibited higher activation energy and, thus, greater responsiveness to seawater warming than plants kept under light limitation. While our results indicated that unusual warming events might favor the photosynthetic performance of P. torreyi, light-limiting conditions can lead to internal carbon depletion and potentially compromise plant survival in the long term.
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.
Intertidal seagrasses are subjected to desiccation and direct solar radiation during low tides. It is assumed that the canopy structure can self-protect the underlying shoots during these events, although there is no evidence on a physiological basis. The physiological responses of the surfgrass Phyllospadix torreyi were examined when emerged during low tide, on i) shoots overlaying the canopy, and ii) shoots sheltered within the canopy. Leaf water potential and water content decreased in external leaves after emersion, and the higher concentration of organic osmolytes reflected osmoregulation. Additionally, these shoots also exhibited a drastic reduction in carbohydrates after re-immersion, likely from cellular damage. Lipid peroxidation and antioxidant activity increments were also detected, while photosynthetic efficiency strongly diminished from direct exposure to solar radiation. Conversely, the sheltered shoots did not dehydrate and solely accumulated some oxidative stress, likely resulting from the warming of the canopy. In conclusion, the leaf canopy structure buffers physiological stress in the sheltered shoots, thus acting as a self-protective mechanism to cope with emersion.
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.
Spatiotemporal variability in primary producer growth rates is a fundamental aspect of community structure. Understanding drivers of these patterns and their response to climate variability and change are ongoing challenges. Nutrient and light limitations often are invoked as proximate drivers of these patterns, but many other environmental and biological factors vary across spatial and temporal scales. In temperate rocky intertidal habitats, macrophytes are major space occupiers and the base of the food web, and thus their patterns of primary production relate directly to their functions and services in these communities. We investigated spatiotemporal patterns of the primary production of two species of macrophytes, the kelp Hedophyllum sessile and the surfgrass Phyllospadix scouleri, across 908 km of Oregon and California coastline. Spatiotemporal variability in macrophyte growth rates and their relationships to regional or local‐scale environmental variables (upwelling, nutrients, temperature, light, phytoplankton blooms) and climate regimes were explored. Paradoxically, we found that both warmer water temperature (e.g., warm phases of climate patterns, weaker upwelling) and increased nutrients (e.g., with stronger upwelling) increased macrophyte productivity. Kelp growth decreased with dense phytoplankton blooms, while surfgrass growth decreased with increasing air temperature. Growth rates reflected tissue elemental content in surfgrass but only weakly in kelp. Hence, as climate warms and/or if upwelling intensifies, productivity of these and perhaps other macrophytes should increase, at least until thermal conditions, particularly low tide air temperature, become too stressful.
Due to climate change, the incidence of marine heat waves (MHWs) has increased, yet their effects on seaweeds are still not well understood. Adult sporophytes of Macrocystis pyrifera, the species forming the iconic Giant Kelp forests, can be negatively affected by thermal stress and associated environmental factors (e.g., nutrient depletion, light deprivation); however, little is known about the tolerance/vulnerability of juvenile sporophytes. Simultaneously to MHWs, juveniles can be subjected to light limitation for extended periods of time (days‐weeks) due to factors causing turbidity, or even because of shading by understory canopy‐forming seaweeds. This study evaluated the effects of a simulated MHW (24°C, 7 d) in combination (or not) with light deprivation, on the photosynthetic capacities, nutrient uptake and tissue composition, as well as oxidative stress descriptors of M. pyrifera juvenile sporophytes (single blade stage, up to 20 cm length). Maximum quantum yield (Fv/Fm) decreased in juveniles under light at 24°C, likely reflecting some damage on the photosynthetic apparatus or dynamic photoinhibition; however, no other sign of physiological alteration was found in this treatment (i.e., pigments, nutrient reserves and uptake, oxidative stress). Photosynthetic capacities were maintained or even enhanced in plants under light deprivation, likely supported by photo‐acclimation (pigments increment); by contrast, nitrate uptake and internal storage of carbohydrates were strongly reduced, regardless of temperature. This study indicated that light limitation can be more detrimental to juvenile survival, and therefore recruitment success of M. pyrifera forests, than episodic thermal stress from MHWs.
Prolonged nitrogen (N) fertilization can impact seagrass survival and productivity; however, the effects of N enrichment pulses (e.g., upwelling or sediment resuspension) remain poorly understood. This study examined the effects of short-term (1 h) pulsing of nitrate (NO3⁻) enrichment, simulating an upwelling event, on dissolved inorganic carbon (DIC) and NO3⁻ uptake capacities, critical in controlling eelgrass productivity. Zostera marina dominates submerged vegetation in coastal lagoons influenced by upwelling in the California Current system. Laboratory incubations were conducted in winter (non-upwelling) and spring (upwelling) with shoots collected from San Quintín Bay meadows, Baja California, Mexico, differentially exposed to upwelled NO3⁻. Results suggest that NO3⁻ enrichment stimulated DIC and NO3⁻ uptake in winter, reflecting the close relationship between carbon metabolism and NO3⁻ assimilation. Eelgrass shoots showed reduced NO3⁻ incorporation in spring; neither NO3⁻ uptake nor photosynthesis increased when exposed to high NO3⁻. Saturation of spring shoots at lower ambient NO3⁻ concentrations may be interpreted as a physiological strategy to restrict metabolically costly NO3⁻ incorporation during upwelling; this regulation of NO3⁻ uptake strongly contrasts to the apparently full exploitation of this nutrient by seaweeds also dominant within the bay, as indicated in previous works. Despite their reduced NO3⁻ uptake, eelgrass meadows near the bay mouth acquire NO3⁻ at rates up to 4.2 mmol N m⁻² day⁻¹. This represents non-trivial water column NO3⁻ removal compared to the estimated oceanic NO3⁻ supply (~ 7.1 mmol m⁻² day⁻¹) during upwelling, highlighting the importance of Z. marina beds in controlling the lagoonal N-budget.
Abstract
Increased plant mortality in temperate seagrass populations has been recently observed after summer heatwaves, although the underlying causes of plant death are yet unknown. The potential energetic constrains resulting from anomalous thermal events could be the reason that triggered seagrass mortality, as demonstrated for benthic invertebrates. To test this hypothesis, the carbon balance of Posidonia oceanica and Cymodocea nodosa plants from contrasting thermal environments was investigated during a simulated heatwave, by analyzing their photosynthetic performance, carbon balance (ratio photosynthesis:respiration), carbohydrates content, growth and mortality. Both species were able to overcome and recover from the thermal stress produced by the six-week exposure to temperatures 4 °C above mean summer levels, albeit plants from cold waters were more sensitive to warming than plants from warm waters as reflected by their inability to maintain their P:R ratio unaltered. The strategies through which plants tend to preserve their energetic status varied depending on the biology of the species and the thermal origin of plants. These included respiratory homeostasis (P. oceanica warm-plants), carbon diversion from growth to respiration (C. nodosa cold-plants) or storage (P. oceanica warm-plants) and changes in biomass allocation (C. nodosa warm-plants). Findings suggest an important geographic heterogeneity in the overall response of Mediterranean seagrasses to warming with potential negative impacts on the functions and services offered by seagrass meadows including among others their capacity for carbon sequestration and carbon export to adjacent ecosystems.
While light availability plays a critical role in seagrass growth and distribution, there is limited understanding of how changes in light exposure impact belowground processes. We investigated the effect of prolonged and fluctuating reductions in light on root growth and exudation by three colonizing seagrasses: Cymodocea serrulata, Halophila ovalis, and Halodule uninervis. Seagrasses were grown in mesocosms under continuous full light (control), under continuous light reduction (medium or low), or under fluctuating light (10 d of low and 4 d of high light, repeated three times). Plants were harvested (1) 6 weeks after light treatments (impact), and (2) after an additional 4 weeks of continuous full light (recovery). Root exudates were collected from trap solutions and measured for dissolved organic carbon (DOC), total dissolved nitrogen (TDN), and dissolved organic matter (DOM) excitation/emission fluorescence spectroscopy. Root biomass decreased in all shading treatments. The most notable impact of light treatment was an increase in root exudation of DOC, protein-like DOM and humic-like DOM under fluctuating light for all species. After 4 weeks of recovery, exudation of DOC, and protein-like DOM observed under fluctuating light returned to the control light levels. However exudation of DOC and protein-like DOM by H. ovalis grown in continuous low light remained greater than the control, likely due to root death. This study suggests the belowground environment of seagrasses is sensitive to light reduction. Monitoring changes in root exudation of seagrasses can provide an effective and rapid method to assess light stress and short-term recovery of seagrasses.
Kinetic studies of protein dephosphorylation in photosynthetic thylakoid membranes revealed specifically accelerated dephosphorylation of photosystem II (PSII) core proteins at elevated temperatures. Raising the temperature from 22°C to 42°C resulted in a more than 10-fold increase in the dephosphorylation rates of the PSII reaction center proteins D1 and D2 and of the chlorophyll abinding protein CP43 in isolated spinach (Spinacia oleracea) thylakoids. In contrast the dephosphorylation rates of the light harvesting protein complex and the 9-kD protein of the PSII (PsbH) were accelerated only 2- to 3-fold. The use of a phospho-threonine antibody to measure in vivo phosphorylation levels in spinach leaves revealed a more than 20-fold acceleration in D1, D2, and CP43 dephosphorylation induced by abrupt elevation of temperature, but no increase in light harvesting protein complex dephosphorylation. This rapid dephosphorylation is catalyzed by a PSII-specific, intrinsic membrane protein phosphatase. Phosphatase assays, using intact thylakoids, solubilized membranes, and the isolated enzyme, revealed that the temperature-induced lateral migration of PSII to the stroma-exposed thylakoids only partially contributed to the rapid increase in the dephosphorylation rate. Significant activation of the phosphatase coincided with the temperature-induced release of TLP40 from the membrane into thylakoid lumen. TLP40 is a peptidyl-prolyl cis-trans isomerase, which acts as a regulatory subunit of the membrane phosphatase. Thus dissociation of TLP40 caused by an abrupt elevation in temperature and activation of the membrane protein phosphatase are suggested to trigger accelerated repair of photodamaged PSII and to operate as possible early signals initiating other heat shock responses in chloroplasts.
Hydrographic data collected over the period 1997-2013 are analyzed to investigate the seasonality of hydrographic features and associated geostrophic flows off the Baja California peninsula. The upper ocean in the region was found to be homogeneous in winter and spring but subdivided into two regions in the summer and autumn. In the first case, the system typically shows relatively low temperature and salinity waters, which give it a subarctic character. In the second, only the region north of Punta Eugenia (28° N) maintains subarctic characteristics, while the southern region receives an inflow of tropical and subtropical waters that results from the weakening of northwesterly winds, which allows the poleward advection of surface waters. Also during this period, a positive wind stress curl promotes the zonal advection of North Pacific's eastern edge waters into the coast and to the north as a surface coastal flow. Average seasonal patterns of geostrophic flow at 200 dbar revealed that the differentiation into provinces is also evident at that depth, with two clearly defined cyclonic structures in summer and autumn, both separated at the latitude of Punta Eugenia. The analyses conducted also showed a clear continuity of the California undercurrent along the shelf break, with more diffuse currents in the winter. Poleward flows were observed throughout the water column, especially in summer and autumn, although the origin of the surface flow does not necessarily involve a surfacing of the California Undercurrent. This article is protected by copyright. All rights reserved.
This work represents the first contribution to (i) examine the changes in plant-water relations of an inter-tidal seagrass during air exposure (Zostera noltii), and (ii) compare the water status descriptors between inter-tidal- and subtidal-adapted species (Cymodocea nodosa, Zostera marina). Two different morphotypes of Z. noltii that develop in the highest and lowest inter-tidal levels in the Portuguese lagoon of Ria Formosa were exposed to natural emersion periods under laboratory conditions, and the evolution of leaf water relations and osmolytes (ions, proline and non-structural carbohydrates) was measured. Both morphotypes regulated their water potential (Ψw) by reducing the osmotic potential (Ψπ) through osmolyte accumulation, but only high inter-tidal plants were able to do this by adjusting the turgor pressure through cell wall hardening. This is a conservative mechanism for osmotic acclimation, which occurred only after long emersion periods (7 h). After a rapid increase in ion concentration under air exposure, the high inter-tidal morphotype replaced them by more physiologically compatible solutes (proline and non-structural carbohydrates) to maintain the osmotic adjustment. Altered ionic homeostasis was found in low inter-tidal plants when exposed to such unnatural, long emersion periods. Osmotic unbalances were also observed during the submerged recovery phase. Descriptors of leaf pressure–volume (P–V) curves and Höfler diagrams were derived for seagrasses for the first time. They support the divergences in water relations observed between inter-tidal and subtidal seagrasses according to their vertical distribution. More negative water and osmotic potentials and higher rigidity of cell walls (higher elastic modulus, ε) were found to be specific osmotic adaptations of seagrasses to the inter-tidal.
Extreme heating (up to 43°C measured from five-year temperature records) occurs in shallow coastal seagrass meadows of the Great Barrier Reef at low tide. We measured effective quantum yield (ϕPSII), growth, senescence and mortality in four tropical seagrasses to experimental short-duration (2.5h) spikes in water temperature to 35°C, 40°C and 43°C, for 6 days followed by one day at ambient temperature. Increasing temperature to 35°C had positive effects on ϕPSII (the magnitude varied between days and was highly correlated with PPFD), with no effects on growth or mortality. 40°C represented a critical threshold as there were strong species differences and there was a large impact on growth and mortality. At 43°C there was complete mortality after 2-3days. These findings indicate that increasing duration (more days in a row) of thermal events above 40°C is likely to affect the ecological function of tropical seagrass meadows.
Little is known about the reproductive ecology of aquatic angiosperms, despite their wide distribution and ecological importance. Surfgrass (Phyllospadix torreyi) is a clonal marine angiosperm that lives on turbulent rocky shores. Surfgrass exhibits a strongly female-biased sex ratio in flowering shoots throughout its distribution along the Pacific coast of North America. The ecological causes for this biased sex ratio were examined over 3 yr in a surfgrass population off Catalina Island in southern California, USA. Abundances, biomass, and C:N content of male and female flowering ramets were measured, and the reproductive phenology, reproductive losses to abortions, herbivore damage to fruits and seeds, and clonal survival and growth were quantified. Each year, a quarter of the vegetative ramets reproduced sexually and seed production in the population was prolific. The population sex ratio was female biased across the entire depth distribution of surfgrass, but males were more abundant deeper in the bed. Despite male rarity, pollen was abundant in the population, and virtually all ovules were fertilized, with few losses to abortions or herbivory before seed release. Potential female fitness (seeds produced) was highest at shallow depths where light availability was greatest and abortions were reduced. The spatial segregation of the sexes was not due to environmental sex lability but to greater ramification of female vs. male clones in shallow depths. Female flowering shoots had significantly higher biomass than males across water depth, despite no obvious cost in terms of vegetative growth, or advantage in terms of plant size. If current theory on sex allocation that the sex ratio should be biased toward the gender with the lower reproductive cost is true for surfgrass, then surfgrass provides an example of how a subtle resource allocation difference can result in a dramatic population bias. An alternative explanation for the female bias in surfgrass populations is greater male mortality due to significantly weaker attachment to the substratum. This study demonstrates the potential role hydrodynamics can play in aquatic plant reproduction and in structuring their populations.