The role of grazers in early-life stages of Cystoseira sensu lato can be crucial in the restoration of marine forests

Grazing is one of the most important biological factors controlling the abundance of early-life stages of fucoids and one of the major issues when restoring marine forests. Benthic macroinvertebrates (e.g., sea urchins) and fish shape and regulate benthic macroalgal communities from polar to tropical regions and can be responsible for regime shifts leading to the predominance of turfs and/or barren grounds. However, other herbivores (i.e., mesograzers) could also significantly participate in the grazing, especially on early-life stages, hampering the persistence and capacity of Cystoseira sensu lato populations to recover after major disturbances and being a cause of failure of restoration actions. We performed experiments in the field and in mesocosm in order to investigate the herbivory pressure and the effects of different grazers on recruits of Cystoseira compressa. The results highlight that non-strict herbivorous invertebrates, such as Clibanarius erythropus, Cerithium vulgatum, and Idotea balthica, graze on recruits of Cystoseira s.l. spp., with I. balthica showing the highest consumption rate. We concluded that biotic factors such as herbivory, which affect key life stages, can be crucial for the conservation of Cystoseira s.l. forests and need to be better understood and considered on a case-by-case basis when planning restoration actions

Data from: Are Niemann-Pick type C proteins key players in cnidarian-dinoflagellate endosymbioses?

The symbiotic interaction between cnidarians, such as corals and sea anemones, and the unicellular algae Symbiodinium is regulated by yet poorly understood cellular mechanisms, despite the ecological importance of coral reefs. These mechanisms, including host-symbiont recognition and metabolic exchange, control symbiosis stability under normal conditions, but also lead to symbiosis breakdown (bleaching) during stress. This study describes the repertoire of the sterol-trafficking proteins Niemann-Pick type C (NPC1 and NPC2) in the symbiotic sea anemone Anemonia viridis. We found one NPC1 gene instead of two in vertebrates. While only one NPC2 gene is present in most metazoans, this gene has been duplicated in cnidarians and we detected four NPC2 genes in A. viridis. However, only one gene (AvNPC2-d) was upregulated in symbiotic sea anemones and displayed higher expression in the gastrodermis (symbiont-containing tissue) than in the epidermis. We performed immunolabeling experiments on tentacle cross sections and demonstrated that the AvNPC2-d protein was closely associated with symbiosomes. In addition, AvNPC1 and AvNPC2-d gene expression was strongly downregulated during stress, especially at the onset of symbiosis breakdown. These data suggest that AvNPC2-d is involved in both the stability and dysfunction of cnidarian-dinoflagellate symbioses

Thermal and menthol stress induce different cellular events during sea anemone bleaching

International audienceCnidarian-dinoflagellate symbiosis disruption and subsequent bleaching are major concerns, especially regarding their ecological consequences on coral reefs and temperate coralligenous communities. Cnidarian bleaching is caused by a variety of environmental stressors, such as elevated seawater temperature associated with global climate change, and by pollutants, such as herbicides and metals. Several cellular events have been described to explain symbiosis dysfunction and bleaching. Excess or damaged Symbiodinium symbionts are removed through a variety of mechanisms, including exocytosis, apoptosis, necrosis and autophagy. However, few studies have compared in the same species the relative involvement of these mechanisms, according to the stress inducing the bleaching. In this study, we used two different treatments —temperature and menthol— to induce bleaching in the sea anemone Anemonia viridis. By monitoring the ultrastructural tissue modifications, in control specimens we observed a basal rate of in situ symbiont digestion —or symbiophagy— induced by starvation. Symbiophagy was strongly induced in menthol-treated specimens and was the main cellular process of bleaching, whereas apoptosis and necrosis predominated in hyperthermal-induced bleaching. These results suggested a host effect through autophagy in menthol-treated specimens. These observations also suggested that symbiont removal may result from reengagement of the phagosomal maturation process in the host. These overall data demonstrate that several Symbiodinium cell removal mechanisms coexist and that stressors can activate one or more of these pathways, depending on the stress type, intensity or duration

Alignment file of NPC1 protein sequences_Figure2

Sequences of NPC1 proteins aligned using the MAFFT program. This alignment was used to generate a phylogenetic tree using the phyML 3.0 sofware, the maximum likelihood method and the LG+I+G substitution model (I=0.1 and gamma factor=1.266). Accession numbers: HsNPC1L1, NP_001095118.1; BtNPC1L1, XP_588051; DrNPC1L1, XP_002663230.2; CiNPC1-b, XP_002122922; DmNPC1-a, NP_609357; DmNPC1-b, NP_608417; HsNPC1, AAK25791.1; BtNPC1, AAI51277; DrNPC1, XP_001919958.3; CiNPC1-a, XP_002120129; SpNPC1, XP_780036; AvNPC1, HG670297; NvNPC1, XM_001634881.1; AdNPC1, adi_v1.19271 from ADIG_G-PEP_111201 database; HmNPC1, XM_002164383.1; AqNPC1, XP_003384854.1

Seawater carbonate chemistry and the recruitment of macroalgal marine forests

Marine forests are shrinking globally due to several anthropogenic impacts including climate change. Forest-forming macroalgae, such as Cystoseira s.l. species, can be particularly sensitive to environmental conditions (e.g. temperature increase, pollution or sedimentation), especially during early life stages. However, not much is known about their response to the interactive effects of ocean warming (OW) and acidification (OA). These drivers can also affect the performance and survival of crustose coralline algae, which are associated understory species likely playing a role in the recruitment of later successional species such as forest-forming macroalgae. We tested the interactive effects of elevated temperature, low pH and species facilitation on the recruitment of Cystoseira compressa. We demonstrate that the interactive effects of OW and OA negatively affect the recruitment of C. compressa and its associated coralline algae Neogoniolithon brassica-florida. The density of recruits was lower under the combinations OW and OA, while the size was negatively affected by the temperature increase but positively affected by the low pH. The results from this study show that the interactive effects of climate change and the presence of crustose coralline algae can have a negative impact on the recruitment of Cystoseira s.l. species. While new restoration techniques recently opened the door to marine forest restoration, our results show that the interactions of multiple drivers and species interactions have to be considered to achieve long-term population sustainability

Climate change and species facilitation affect the recruitment of macroalgal marine forests

International audienceMarine forests are shrinking globally due to several anthropogenic impacts including climate change. Forest-forming macroalgae, such as Cystoseira s.l. species, can be particularly sensitive to environmental conditions (e.g. temperature increase, pollution or sedimentation), especially during early life stages. However, not much is known about their response to the interactive effects of ocean warming (OW) and acidification (OA). These drivers can also affect the performance and survival of crustose coralline algae, which are associated understory species likely playing a role in the recruitment of later successional species such as forest-forming macroalgae. We tested the interactive effects of elevated temperature, low pH and species facilitation on the recruitment of Cystoseira compressa. We demonstrate that the interactive effects of OW and OA negatively affect the recruitment of C. compressa and its associated coralline algae Neogoniolithon brassica-florida. The density of recruits was lower under the combinations OW and OA, while the size was negatively affected by the temperature increase but positively affected by the low pH. The results from this study show that the interactive effects of climate change and the presence of crustose coralline algae can have a negative impact on the recruitment of Cystoseira s.l. species. While new restoration techniques recently opened the door to marine forest restoration, our results show that the interactions of multiple drivers and species interactions have to be considered to achieve long-term population sustainability

PrimersEfficiency

PCR efficiency of primers used in this study (DNA quantification and heat stress experiment

TreeFile_NPC1_Figure2

Tree data generated using the maximum likelihood method and the PhyML3.0 software. Compute these data with the SeaView program to display the NPC1 phylogenetic tree

TreeFile_NPC2_Figure1

Tree data generated using the maximum likelihood method and the PhyML3.0 software. Compute these data with the SeaView program to display the NPC2 phylogenetic tree

qPCR_QuantifZxAv

Symbiodinium quantification by real-time quantitative PCR measurement of the relative nuclear gene copy number (symbiont to host nuclei) during hyperthermal stress