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Marine forests and kelps as their foundation species are threatened by ocean warming especially at the warm distributional edges. Previously identified genetic divergence and ecotypic differentiation within kelp species may allow to produce more resilient lineages by intraspecific outbreeding among populations. In a mechanistic investigation of heat stress, heterosis (hybrid vigour), and underlying gene expression patterns, we assessed the thermal performance of inbred (selfings) and outbred (reciprocal crosses) sporophytes of the N-Atlantic kelp Laminaria digitata among clonal isolates from two divergent populations; one from the temperate North Sea (Helgoland) and one from the Arctic (Spitsbergen). First, we investigated the upper thermal tolerance of microscopic sporophytes in a 14-day experiment applying sublethal to lethal 20-23 degrees C. The upper survival temperature of microscopic sporophytes was lower for the inbred Arctic selfing (21 degrees C) than for the temperate selfing and the reciprocal crosses (22 degrees C). Only in the temperate selfing, 4.5% of sporophytes survived 23 degrees C. We then subjected 4-7 cm long sporophytes to a control temperature (10 degrees C), moderate (19 degrees C) and sublethal to lethal heat stress (20.5 degrees C) for 18 days to assess gene expression in addition to physiological parameters. Growth and optimum quantum yield decreased similarly in the reciprocal crosses and the temperate selfing at 19 and 20.5 degrees C, while inbred Arctic sporophytes died within seven days at both 19 and 20.5 degrees C. In response to 20.5 degrees C, 252 genes were constitutively regulated across all surviving lineages, which we use to describe metabolic regulation patterns in response to heat stress in kelp. At sublethal 20.5 degrees C, ca. 150 genes were differentially expressed by either crossed lineage in comparison to the temperate selfing, indicating that they maintained a growth response similar to the temperate selfing with differential metabolic regulation during sublethal heat stress. Subtle differences in physiology and the differential expression of nine genes between the reciprocal crosses at 20.5 degrees C indicate that female and male gametophytes may contribute differently to offspring traits. We consider potential inbreeding depression in the Spitsbergen selfing and quantify the better performance of both crosses using heterosis-related parameters. We discuss the potential and risks of outbreeding to produce more resilient crops for mariculture and marine forest restoration. info:eu-repo/semantics/publishedVersion

Restoration of foundation species in historical habitat may be difficult if adult facilitation is obligatory for survival of early life stages. 2. On intertidal Mediterranean coasts, large-scale loss of the dominant forest- forming macroalga Ericaria amentacea have prompted restoration efforts using recruits. Yet, early life stages may be more susceptible to the abiotic stress that characterizes their habitat. 3. We tested strategies to enhance resilience of lab-cultured juveniles of E. amen- tacea to environmental stress in historical habitat lacking conspecifics. Juveniles were exposed in culture to fluctuations of the dominant physical stressors, irra- diance and temperature, and then outplanted in upper and lower zones of their native intertidal range. 4. Without adult canopy, juvenile outplant survival was limited to the lower tidal range, with nearly complete mortality in the upper zone. Survival was also strongly determined by spatial clumping of recruits within the outplant sub- strate. Longer-term growth in the lower zone was enhanced by fluctuating mild stress in culture, with variable irradiance and concurrent heat pulses increas- ing post-outplant cover by 40%–60% after 4 months. Clumping also promoted growth across experimental treatments. 5. Synthesis and applications. Reliance on self-facilitation feedbacks is a common barrier to foundation species restoration in high-stress habitats. Our results sug- gest that without adult habitat amelioration, environmental stress limits recruit survival in intertidal algal forest. Yet, exposure to transient, low environmental stress in culture and outplanting of clumped individuals may confer resilience and allow successful establishment of early life stages in zones of reduced abi- otic stress, providing a source for gradual colonization of more high-stress areas.

Compared to its terrestrial counterpart, work at sea to collect scientific data calls for an efficient workflow and particular skills from personnel, particularly when the study involves several observation variables. Therefore, a procedure that incorporates both the underwater and on-board phases in a coordinated manner is required. Although there exist published and validated sampling protocols for benthic habitats, in the existing literature it is more difficult to find workflows or recommendations for use prior to data collection. Using a kelp forest ecological assessment study as a model, we present a detailed workflow for sampling, both on-board and under hyperbaric conditions, so that it can be used as an example for subsequent evaluations, as a standardized method for systematic study in blue carbon ecosystems. cosystems.

Este artículo contiene 10 páginas, 2 figuras, 3 tablas., [EN]Photosynthetic features of different canopy-forming macroalgae of the order Fucales (Phaeophyceae) living in shallow and sheltered environments show a high homogeneity when compared with other morphologically similar species living across a depth gradient. Photosynthesis at saturation (situated around 5 mg O2 gAFDM 1 h1) and photosynthetic efficiency [around 0.4 mg O2·m2 s (μmol photon·gAFDM·h)-1] are relatively low, while dark respiration (around 1 mg O2 gAFDM 1 h1) and light at compensation (around 24 μmol photon·m-2·s-1) are relatively high, as it corresponds to the characteristics of “sun” plants. C:N and C:P ratios suggest a strong nutrient limitation for growth and photosynthesis, in agreement with the low dissolved nutrient levels usually found in shallow Mediterranean waters. Homogeneity in photosynthetic features points to a good local adaptation of the different species to the prevailing light conditions but opens the question of which are the factors allowing the coexistence of different species of Fucales in sheltered and shallow Mediterranean environments. [FR] Homogénéité des caractéristiques photosynthétiques des macroalgues de l’ordre des Fucales formant une canopée dans les environnements peu profonds et protégés. Les caractéristiques photosynthétiques de différentes algues de l’ordre Fucales (Phaeophyceae) qui croissent dans des environnements peu profonds et protégés montrent une grande homogénéité si on les compare avec d’autres espèces de morphologie similaire présentes dans d’autres environnements le long du gradient bathymétrique. La photosynthèse en saturation (située aux environs de 5 mg O2 g masse sèche sans cendres1 h1) et l’efficacité photosynthétique [environ 0.4 mg O2·m2 s (μmol photon·g masse sèche sans cendres1·h)-1] sont relativement basses, alors que la respiration sombre (environ 1 mg O2 g poids sec sans cendres1 h1) et la lumière à compensation (environ 24 μmol photon·m2·s-1) sont relativement élevées, comme c’est le cas avec les caractéristiques des plantes «de soleil». Les rapports C:N et C:P suggèrent une forte limitation par N et P, ce qui est congruent avec les niveaux de nutriments très bas qu’on observe régulièrement dans les eaux peu profondes méditerranéennes. L’homogénéité des caractéristiques photosynthétiques indique une adaptation locale des différentes espèces aux conditions de lumière présentes mais pose la question des facteurs permettant la coexistence des différentes espèces de Fucales dans les environnements méditerranéens peu profonds et protégés.

Canopy-forming brown algae support highly productive ecosystems whose decline has been attributed to the interplay of several anthropogenic disturbances. Climate change could have disruptive effects on the biology of these species, but the role of temperature in the development of early life stages is poorly understood. The aim of this study was to assess the response of Ericaria giacconei, a winter-reproducing Southern–Mediterranean endemic species, to thermal stress by testing five temperatures (12, 15, 18, 24, and 28°C) on adults and early stages. Chlorophyll a fluorescence of adult plants was measured at 0, 24, 72, and 120 h on nine fronds in each of the three aquaria per treatment. To assess egg release, zygote settlement, and embryo growth rate, approximately 1,200 receptacles were cultured on six Petri dishes per temperature treatment, and 10 random subsections of 2 ×2 mm were examined in three Petri dishes at 0, 20, 44, and 92 h after fertilization. Adult plants showed a plastic physiological response, and thermal stress had no significant effect on PSII efficiency. Embryos fully developed only at 12 and 15°C. Mortality increased at 18 and 24°C, and no zygotes survived at 28°C. In a scenario of further increasing temperatures, the effects of warming could affect the recruitment of E. giacconei and increase its vulnerability to further stresses. These effects on the survival of early stages, which are the bottleneck for the long-term survival of the species, should be taken into account in conservation and restoration measures to maintain canopy-forming macroalgal populations and associated biodiversity and ecosystem services.

Dispersal is a central process that affects population growth, gene flow, and ultimately species persistence. Here we investigate the extent to which gene flow occurs between fragmented populations of the deep-water brown algae Ericaria zosteroides (Turner) Greville (Sargassaceae, Fucales). These investigations were performed at different spatial scales from the bay of Marseille (western Provence) to Corsica. As dispersal of zygotes is shown to be limited over distances beyond a few meters, we used a multidisciplinary approach, based on Lagrangian modeling and population genomics to test the hypothesis that drifting of fertile parts of thallus (eggs on fertile branches), mediated by ocean currents, enable occasional gene flow between populations. Therefore we assessed the respective contribution of oceanographic connectivity, geographical isolation, and seawater temperatures to the genetic structure of this species. The genetic structure was assessed using 10,755 neutral SNPs and 12 outlier SNPs genotyped by dd-RAD sequencing in 261 individuals of E. zosteroides. We find that oceanographic connectivity is the best predictor of genetic structure, while differentiation in outlier SNPs can be explained by the depth of populations, as emphasized by the minimum seawater temperature predictor. However, further investigations will be necessary for clarifying how depth drives adaptive genetic differentiation in E. zosteroides. Our analyses revealed that local hydrodynamic conditions are correlated with the very high divergence of one population in the Bay of Marseille. Overall, the levels of gene flow mediated by drifting were certainly not sufficient to counteract differentiation by local genetic drift, but enough to allow colonization several kilometers away. This study stresses the need to consider secondary dispersal mechanisms of presumed low dispersal marine species to improve inference of population connectivity.

International audience; Dispersal is a central process that affects population growth, gene flow, and ultimately species persistence. Here we investigate the extent to which gene flow occurs between fragmented populations of the deep-water brown algae Ericaria zosteroides (Turner) Greville (Sargassaceae, Fucales). These investigations were performed at different spatial scales from the bay of Marseille (western Provence) to Corsica. As dispersal of zygotes is shown to be limited over distances beyond a few meters, we used a multidisciplinary approach, based on Lagrangian modeling and population genomics to test the hypothesis that drifting of fertile parts of thallus (eggs on fertile branches), mediated by ocean currents, enable occasional gene flow between populations. Therefore we assessed the respective contribution of oceanographic connectivity, geographical isolation, and seawater temperatures to the genetic structure of this species. The genetic structure was assessed using 10,755 neutral SNPs and 12 outlier SNPs genotyped by dd-RAD sequencing in 261 individuals of E. zosteroides. We find that oceanographic connectivity is the best predictor of genetic structure, while differentiation in outlier SNPs can be explained by the depth of populations, as emphasized by the minimum seawater temperature predictor. However, further investigations will be necessary for clarifying how depth drives adaptive genetic differentiation in E. zosteroides. Our analyses revealed that local hydrodynamic conditions are correlated with the very high divergence of one population in the Bay of Marseille. Overall, the levels of gene flow mediated by drifting were certainly not sufficient to counteract differentiation by local genetic drift, but enough to allow colonization several kilometers away. This study stresses the need to consider secondary dispersal mechanisms of presumed low dispersal marine species to improve inference of population connectivity.

In coastal ecosystems, large brown macroalgae are important foundation species, growing on rocky shores from temperate to polar regions. They form marine forests, also known as kelp forests, which are among the most productive coastal marine ecosystems in the world. Kelps are of high ecological and economic value, however, climate change poses a great threat to these ecosystems. Warming has vast implications on marine forests and their global biogeographic patterns, but also other drivers affect kelps and strong interactive effects are observed. The aim of this study was to gain a deeper understanding of the inter- and intraspecific acclimation processes of kelp species to abiotic conditions along large spatial and environmental gradients. The thermal tolerance of the broadly distributed kelp Saccharina latissima towards marine summer heatwaves across latitudes and its biochemical and morphological variability across its entire distribution range in Europe was investigated. Seasonal and inter-annual differences in the susceptibility of S. latissima to marine heatwaves in summer were revealed and the impact of potential interactions of marine heatwaves in summer paired with hyposalinity or enhanced nutrient availability was analyzed. The combined effect of different temperatures and salinities on physiological and biochemical response variables was also investigated in young Laminaria solidungula sporophytes. In conclusion, this thesis presents important information on the functional variability of two kelp species with different distributional ranges. Both studied species exhibit different sensitivity towards drivers related to environmental change. Furthermore, intraspecific variation must not be underestimated. The observed changes in the kelp populations of Europe, thus, cannot exclusively be ascribed to temperature variation but to an interplay of various abiotic and biotic factors. These findings contribute further knowledge to support future approaches to the conservation of marine forests.

1. The worldwide decline of marine forests, due to human impacts and climate change, emphasizes the need to develop and implement effective and sustainable solutions to restore these endangered habitats and to re-establish the services they provide. 2. In this study, the ex situ restoration of Treptacantha barbata, a Mediterranean subtidal habitat-forming species of brown seaweed, was for the first time implemented in a marine protected area in the Adriatic Sea. Two restoration efforts were performed in 2019. The first one was started in winter, after a marine heatwave that triggered early fertility, the second one in spring, when the species usually reproduces. 3. This study aimed to evaluate: 1) the disruptive effects of a thermal anomaly on the reproductive biology and performance in culture of T. barbata; and 2) the impact of the grazing pressure on juveniles after the outplanting. 4. The first cultivation was more productive than the second one, in terms of zygote release and germling growth. To mitigate the low efficiency of the second culture and to avoid prolonged highly-demanding maintenance in the mesocosms, the cultivation period was extended outdoors using a structure suspended in the water column. 5. The modular frames conceived for outplanting T. barbata proved to be effective because of their easy operability and low cost. Controlling for herbivorous fish had significant positive effects on both juvenile survival and growth. 6. The outcomes highlighted that an unpredictable climatic event and fish grazing were major threats that impaired the restoration process of T. barbata. These stressors should be considered when developing plans to implement effective large-scale restoration of canopy-forming macroalgae.

To understand the thermal plasticity of a coastal foundation species across its latitudinal distribution, we assess physiological responses to high temperature stress in the kelp Laminaria digitata in combination with population genetic characteristics and relate heat resilience to genetic features and phylogeography. We hypothesize that populations from Arctic and cold-temperate locations are less heat resilient than populations from warm distributional edges. Using meristems of natural L. digitata populations from six locations ranging between Kongsfjorden, Spitsbergen (79°N), and Quiberon, France (47°N), we performed a common-garden heat stress experiment applying 15°C to 23°C over eight days. We assessed growth, photosynthetic quantum yield, carbon and nitrogen storage, and xanthophyll pigment contents as response traits. Population connectivity and genetic diversity were analyzed with microsatellite markers. Results from the heat stress experiment suggest that the upper temperature limit of L. digitata is nearly identical across its distribution range, but subtle differences in growth and stress responses were revealed for three populations from the species' ecological range margins. Two populations at the species' warm distribution limit showed higher temperature tolerance compared to other populations in growth at 19°C and recovery from 21°C (Quiberon, France), and photosynthetic quantum yield and xanthophyll pigment responses at 23°C (Helgoland, Germany). In L. digitata from the northernmost population (Spitsbergen, Norway), quantum yield indicated the highest heat sensitivity. Microsatellite genotyping revealed all sampled populations to be genetically distinct, with a strong hierarchical structure between southern and northern clades. Genetic diversity was lowest in the isolated population of the North Sea island of Helgoland and highest in Roscoff in the English Channel. All together, these results support the hypothesis of moderate local differentiation across L. digitata's European distribution, whereas effects are likely too weak to ameliorate the species' capacity to withstand ocean warming and marine heatwaves at the southern range edge. Foundation for Science and Technology: UIDB/04326/2020/ PTDC/MAR-EST/6053/2014/ Biodiversa/0004/2015 info:eu-repo/semantics/publishedVersion

To understand the thermal plasticity of a coastal foundation species across its latitudinal distribution, we assess physiological responses to high temperature stress in the kelp Laminaria digitata in combination with population genetic characteristics and relate heat resilience to genetic features and phylogeography. We hypothesize that populations from Arctic and cold‐temperate locations are less heat resilient than populations from warm distributional edges. Using meristems of natural L. digitata populations from six locations ranging between Kongsfjorden, Spitsbergen (79°N), and Quiberon, France (47°N), we performed a common‐garden heat stress experiment applying 15°C to 23°C over eight days. We assessed growth, photosynthetic quantum yield, carbon and nitrogen storage, and xanthophyll pigment contents as response traits. Population connectivity and genetic diversity were analyzed with microsatellite markers. Results from the heat stress experiment suggest that the upper temperature limit of L. digitata is nearly identical across its distribution range, but subtle differences in growth and stress responses were revealed for three populations from the species’ ecological range margins. Two populations at the species’ warm distribution limit showed higher temperature tolerance compared to other populations in growth at 19°C and recovery from 21°C (Quiberon, France), and photosynthetic quantum yield and xanthophyll pigment responses at 23°C (Helgoland, Germany). In L. digitata from the northernmost population (Spitsbergen, Norway), quantum yield indicated the highest heat sensitivity. Microsatellite genotyping revealed all sampled populations to be genetically distinct, with a strong hierarchical structure between southern and northern clades. Genetic diversity was lowest in the isolated population of the North Sea island of Helgoland and highest in Roscoff in the English Channel. All together, these results support the hypothesis of moderate local differentiation across L. digitata's European distribution, whereas effects are likely too weak to ameliorate the species’ capacity to withstand ocean warming and marine heatwaves at the southern range edge., We aimed to understand the intraspecific thermal variation of a coastal foundation species, the kelp Laminaria digitata. Marginal populations in particular differed in their response to heat stress treatments, while multilocus genotypes showed a clear and broad separation of L. digitata populations into a “northern” and a “southern” clade. These results imply that L. digitata populations have phenotypically diverged under the influence of the Quaternary glacial cycles.

In the Mediterranean Sea, brown algae belonging to the Cystoseira genus play a valuable role as foundation species. Due to evidences of regression/loss of the habitats of these species caused by the interplay of human and climatic disturbances, active restoration measures have been encouraged by EU regulations. In particular, nondestructive restoration techniques, which avoid the depletion of threatened species in donor populations, are strongly recommended. In the framework of the EU project ROCPOP-Life, the first ex situ outplanting experience of Cystoseira amentacea var. stricta has been implemented in the Cinque Terre Marine Protected Area (northwestern Mediterranean). A total of 400 clay tiles, hosting approximately three mm-long germlings of C. amentacea, were fixed to the rocky shore with screws: the tiles were monitored for the next 2 months by photographic sampling, and survival (presence/absence of juveniles on the tiles), cover and growth were assessed. Additional sampling was performed 6 months after tile deployment, after which an unprecedented storm surge severely affected the restoration performance. After 2 months, over 40% of the tiles were covered with Cystoseira juveniles, which reached approximately eight mm in total length. The tiles that survived the storm hosted three to six cm-long juveniles. The high cover (≥25%), assuring moisture and shading, and the appropriate size of the juveniles, to avert micro-grazing, at time of deployment were key to the survival and growth of the outplanted juveniles, increasing the potential for restoration success. Our findings show that outplanting of midlittoral canopy-forming species is a feasible approach for restoration efforts, with particular attention given to the early phases: (i) laboratory culture, (ii) transport, and (iii) juvenile densities. These results are strongly encouraging for the implementation of restoration actions for C. amentacea on a large scale, in light of EU guidelines.

In the Mediterranean Sea Cystoseira forests are locally threatened due to several impacts. The low dispersal capacity of most Cystoseira species makes the natural recovery unlikely. The restoration of Cystoseira forests can represent a valuable solution and is recommended where the historical presence is recorded and the impacts that led to its loss are no longer acting (a reasoned forestation could be considered also where historical data are not available). MPAs may play a paramount role in the conservation of Cystoseira forests, guaranteeing protection from several impacts and representing the source of propagules for the restoration of lost or degraded forests outside their borders. MPAs where Cystoseira forests are lacking due to past impacts should be considered as priority experimental sites for artificial forestation.