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Field Collection and Laboratory Maintenance of Canopy-Forming Giant Kelp to Facilitate Restoration

Canopy-forming kelps are essential foundation species, supporting biodiversity and providing ecosystem services valued at more than USD$500 billion ...

Universidad Autónoma de Baja California

This study was designed to understand better if and how juvenile sporophytes of Macrocystis pyrifera can photoacclimate to high-light conditions when transplanted from 10 to 3 meters over 7 d. Acclimation of adult sporophytes to light regimes in the bathymetric gradient has been extensively documented. It primarily depends on photoacclimation and translocation of resources among blades. Among other physiological differences, juvenile sporophytes of M. pyrifera lack the structural complexity shown by adults. As such, juveniles may primarily depend on their photoacclimation capacities to maintain productivity and even avoid mortality under changing light regimes. However, little is known about how these mechanisms operate in young individuals. The capacity of sporophytes to photoacclimate was assessed by examining changes in their photosynthetic performance, pigment content, and bio-optical properties of the blade. Sporophytes nutritional status and oxidative damage were also determined. Results showed that juvenile sporophytes transplanted to shallow water were able to regulate light harvesting by reducing pigment concentration, and thus, absorptance and photosynthetic efficiency. Also, shallow-water sporophytes notably enhanced the dissipation of light energy as heat (NPQ) as a photoprotective mechanism. Generally, these adjustments allowed sporophytes to manage the absorption and utilization of light energy, hence reducing the potential for photo-oxidative damage. Furthermore, no substantial changes were found in the internal reserves (i.e., soluble carbohydrates and nitrogen) of these sporophytes. To our knowledge, these results are the first to provide robust evidence of photoprotective and photoacclimation strategies in juveniles of M. pyrifera, allowing them to restrict or avoid photodamage during shallow-water cultivation.

Photoacclimation and Photoprotection of Juvenile Sporophytes of Macrocystis pyrifera (Laminariales, Phaeophyceae) Under High-light Conditions During Short-term Shallow-water Cultivation.

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 (F /F ) 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 photoacclimation (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.

Effects of Heat Waves and Light Deprivation on Giant Kelp Juveniles (Macrocystis pyrifera, Laminariales, Phaeophyceae).

The toxic potential of Chattonella is associated with a high production of reactive oxygen species (ROS). Chattonella species can tolerate high irradiance levels but seems not to be efficient in the induction of nonphotochemical chl a fluorescence (NPQ) under light stress conditions. Therefore, we postulated that high ROS production of this microalgal group is related to the lack of effective photoprotection mechanisms. We compared the NPQ induction, xanthophyll cycle interconversion (XC), and the production of the ion superoxide (O ) in Chattonella marina var. antiqua, Chattonella sp., and C. marina acclimated to 43 (LL) and 300 µmol photons · m  · s (HL). We also evaluated the photosynthetic characteristics of the three strains. Photosynthesis saturated at relative high irradiances (above 500 µmol photons · m  · s ) in LL and HL Chattonella strains. For the first time, we documented the conversion of diadinoxanthin into diatoxanthin in microalgae that have violaxanthin as the major XC carotenoid. The slow NPQ induction indicated that qE (fast component of NPQ) was not present, and this process was related to the interconversion of XC pigments. However, the quenching efficiency (QE) of deepoxidated xanthophylls was low in the three Chattonella strains. The strain with the lowest QE produced the highest amount of a O . Therefore, ROS production in Chattonella seems to be related to a low expression of XC-related thermal PSII dissipation.

Photosynthesis and photoprotection characteristics related to ROS production in three Chattonella (Raphidophyceae) species.

Vegetated coastal ecosystems have an important role as contaminant filters. Temporal variations in concentrations, enrichment factors (EF), and fluxes of trace elements (As, Cd, Co, Cr, Cu, Ni, Pb, V, and Zn) were evaluated in Pb-dated sediment cores from salt marsh and seagrass ecosystems at San Quintín Bay (Mexican northern Pacific). Trace element contamination was negligible in seagrass sediments, but minor to severe, depending on the element, in salt marsh cores, owing to higher organic carbon and fine sediment contents. EF temporal variation in salt marsh cores was attributed to agriculture technology changes (e.g. installation of greenhouses, and improved irrigation and fertilization systems). Trace element flux ratios increased during the past 100 years, likely caused by steadily increasing sediment accumulation rates promoted by land-use changes in the catchment. The conservation of salt marsh areas is important to preserve their function as contaminants biofilters and the health of adjacent ecosystems.

Influence of agricultural system transition on trace element contamination in salt marsh and seagrass sediments from a coastal Ramsar site.

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.

Ecophysiological responses and self-protective canopy effects of surfgrass (Phyllospadix torreyi) in the intertidal.

Human- and nature-induced hypersaline conditions in coastal systems can lead to profound alterations of the structure and vitality of seagrass meadows and their socio-ecological benefits. In the last two decades, recent research efforts (>50 publications) have contributed significantly to unravel the physiological basis underlying the seagrass-hypersalinity interactions, although most (∼70%) are limited to few species (e.g. Posidonia oceanica, Zostera marina, Thalassia testudinum, Cymodocea nodosa). Variables related to photosynthesis and carbon metabolism are among the most prevalent in the literature, although other key metabolic processes such as plant water relations and responses at molecular (i.e. gene expression) and ultrastructure level are attracting attention. This review emphasises all these latest insights, offering an integrative perspective on the interplay among biological responses across different functional levels (from molecular to clonal structure), and their interaction with biotic/abiotic factors including those related to climate change. Other issues such as the role of salinity in driving the evolutionary trajectory of seagrasses, their acclimation mechanisms to withstand salinity increases or even the adaptive properties of populations that have historically lived under hypersaline conditions are also included. The pivotal role of the costs and limits of phenotypic plasticity in the successful acclimation of marine plants to hypersalinity is also discussed. Finally, some lines of research are proposed to fill the remaining knowledge gaps.

Advances in understanding multilevel responses of seagrasses to hypersalinity.

The spread of non-indigenous and invasive seaweeds has increased worldwide, and their potential effects on native seaweeds have raised concern. Undaria pinnatifida is considered among the most prolific non-indigenous species. This species has expanded rapidly in the Northeast Pacific, overlapping with native communities such as the iconic giant kelp forests (Macrocystis pyrifera). Canopy shading by giant kelp has been argued to be a limiting factor for the presence of U. pinnatifida in the understory, thus its invasiveness capacity. However, its physiological plasticity under light limitation remains unclear. In this work, we compared the physiology and growth of juvenile U. pinnatifida and M. pyrifera sporophytes transplanted to the understory of a giant kelp forest, to juveniles growing outside of the forest. Extreme low light availability compared to that outside (~0.2 and ~4.4 mol photon ⋅ m ⋅ d , respectively) likely caused a "metabolic energy crisis" in U. pinnatifida, thus restricting its photoacclimation plasticity and nitrogen acquisition, ultimately reducing its growth. Despite M. pyrifera juveniles showing photoacclimatory responses (e.g., increases in photosynthetic efficiency and lower compensation irradiance, E ), their physiological/vegetative status deteriorated similarly to U. pinnatifida, which explains the low recruitment inside the forest. Generally, our results revealed the ecophysiological basis behind the limited growth and survival of juvenile U. pinnatifida sporophytes in the understory.

Shading by giant kelp canopy can restrict the invasiveness of Undaria pinnatifida (Laminariales, Phaeophyceae).

Marine heatwaves (MHWs) can have detrimental effects on seagrasses, but knowledge about the impacts on their ecosystem services remains scarce. This work evaluated Phyllospadix scouleri (surgrass) as a biofilter for wastewater discharges, and how warming associated with MHW may affect this ecological function. The nitrogen uptake kinetics and assimilation abilities for ammonium, nitrate, and urea were examined under two different warming scenarios (single and repeated events) simulated in a mesocosm. N-uptake kinetics were related to urban sewage discharges close to surfgrass meadows. Our results revealed that surfgrasses can serve as effective biofilters because of their high nitrogen uptake rates and above-average canopy biomass. Nonetheless, exposure to both experimental warmings resulted in a significant decline in their ability to incorporate and assimilate nitrogen. Consequently, MHWs may reduce the capacity of surfgrasses to function as nitrogen sinks and green filters for sewage waters, jeopardizing their role as Blue Nitrogen systems.

Marine heatwaves can limit the role of surfgrasses as biofilters for wastewaters.

Anaerobic ammonium oxidation, associated with both iron (Feammox) and manganese (Mnammox) reduction, is a microbial nitrogen (N) removal mechanism recently identified in natural ecosystems. Nevertheless, the spatial distributions of these non-canonical Anammox (NC-Anammox) pathways and their environmental drivers in subtidal coastal sediments are still unknown. Here, we determined the potential NC-Anammox rates and abundance of dissimilatory metal-reducing bacteria (Acidomicrobiaceae A6 and Geobacteraceae) at different horizons (0-20 cm at 5 cm intervals) of subtidal coastal sediments using the N isotope-tracing technique and molecular analyses. Sediments were collected across three sectors (inlet, transition, and inner) in a coastal lagoon system (Bahia de San Quintin, Mexico) dominated by seagrass meadows. The positive relationship between N production rates and dissimilatory Fe and Mn reduction provided evidence for Feammox's and Mnammox's co-occurrence. N loss through NC-Anammox was detected in subtidal sediments, with potential rates of 0.07-0.62 μg N g day. NC-Anammox process in vegetated sediments tended to be higher than those in adjacent unvegetated ones. NC-Anammox rates showed a subsurface peak (between 5 and 15 cm) in the vegetated sediments but decreased consistently with depth in the adjacent bare bottoms. Thus, the presence/absence of seagrasses and sediment characteristics, particularly the availability of organic carbon and microbiologically reducible Fe(III) and Mn(IV), affected the abundance of dissimilatory metal-reducing bacteria, which mediated NC-Anammox activity and the associated N removal. An annual loss of 32.31 ± 3.57 t N was estimated to be associated with Feammox and Mnammox within the investigated area, accounting for 2.8-4.7% of the gross total import of reactive N from the ocean into the Bahia de San Quintin. Taken as a whole, this study reveals the distribution patterns and controlling factors of the NC-Anammox pathways along a coastal lagoon system. It improves our understanding of the coupling between N and trace metal cycles in coastal environments.

Ammonium loss microbiologically mediated by Fe(III) and Mn(IV) reduction along a coastal lagoon system.

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.

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

Kelp communities are experiencing exacerbated heat-related impacts from more intense, frequent, and deeper marine heatwaves (MHWs), imperiling the long-term survival of kelp forests in the climate change scenario. The occurrence of deep thermal anomalies is of critical importance, as elevated temperatures can impact kelp populations across their entire bathymetric range. This study evaluates the impact of MHWs on mature sporophytes of Pterygophora californica (walking kelp) from the bathymetric extremes (8-10 vs. 25-27 m) of a population situated in Baja California (Mexico). The location is near the southernmost point of the species's broad distribution (from Alaska to Mexico). The study investigated the ecophysiological responses (e.g., photobiology, nitrate uptake, oxidative stress) and growth of adult sporophytes through a two-phase experiment: warming simulating a MHW and a post-MHW phase without warming. Generally, the effects of warming differed depending on the bathymetric origin of the sporophytes. The MHW facilitated essential metabolic functions of deep-water sporophytes, including photosynthesis, and promoted their growth. In contrast, shallow-water sporophytes displayed metabolic stress, reduced growth, and oxidative damage. Upon the cessation of warming, certain responses, such as a decline in nitrate uptake and net productivity, became evident in shallow-water sporophytes, implying a delay in heat-stress response. This indicates that variation in temperatures can result in more prominent effects than warming alone. The greater heat tolerance of sporophytes in deeper waters shows convincing evidence that deep portions of P. californica populations have the potential to serve as refuges from the harmful impacts of MHWs on shallow reefs.

Article	Year
Photoacclimation and Photoprotection of Juvenile Sporophytes of Macrocystis pyrifera (Laminariales, Phaeophyceae) Under High-light Conditions During Short-term Shallow-water Cultivation. Journal of phycology\| PubMed ID: 31804706	2020
Effects of Heat Waves and Light Deprivation on Giant Kelp Juveniles (Macrocystis pyrifera, Laminariales, Phaeophyceae). Journal of phycology\| PubMed ID: 32282942	2020
Photosynthesis and photoprotection characteristics related to ROS production in three Chattonella (Raphidophyceae) species. Journal of phycology\| PubMed ID: 33523492	2021
Influence of agricultural system transition on trace element contamination in salt marsh and seagrass sediments from a coastal Ramsar site. Ecotoxicology and environmental safety\| PubMed ID: 33711577	2021
Ecophysiological responses and self-protective canopy effects of surfgrass (Phyllospadix torreyi) in the intertidal. Marine environmental research\| PubMed ID: 34656017	2021
Advances in understanding multilevel responses of seagrasses to hypersalinity. Marine environmental research\| PubMed ID: 36435174	2023
Shading by giant kelp canopy can restrict the invasiveness of Undaria pinnatifida (Laminariales, Phaeophyceae). Journal of phycology\| PubMed ID: 36973579	2023
Marine heatwaves can limit the role of surfgrasses as biofilters for wastewaters. Marine pollution bulletin\| PubMed ID: 37832497	2023
Ammonium loss microbiologically mediated by Fe(III) and Mn(IV) reduction along a coastal lagoon system. Chemosphere\| PubMed ID: 38092166	2024
Marine heatwaves recurrence aggravates thermal stress in the surfgrass Phyllospadix scouleri. Marine pollution bulletin\| PubMed ID: 38176159	2024
Bathymetric origin shapes the physiological responses of Pterygophora californica (Laminariales, Phaeophyceae) to deep marine heatwaves. Journal of phycology\| PubMed ID: 38264946	2024

Jose M. Sandoval-Gil

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