Effects of local and global stressors on the status and future persistence of intertidal canopy-forming algae

Abstract

Marine canopy-forming seaweeds are among the most important habitat-forming species along temperate and polar rocky coasts. They form diverse, productive and valuable forest habitats that play a key role in coastal primary production, nutrient cycling and disturbance regulation, and facilitate abundant algae and animal communities. They are also some of the most heavily impacted coastal habitats, facing increasing pressures from urban sprawl, pollution, overfishing and climatic instabilities. Identifying the type and strength of interactions between multiple anthropogenic and natural stressors can help setting achievable management targets for degraded ecosystems and support ecological resilience through local actions. My research focuses primarily on understanding the effects of multiple local and global stressors on canopy-forming seaweeds of the genus Cystoseira, with and emphasis on field investigation and experimentation. I approached my research integrating different approaches: 1) I investigated which are the factors driving the loss of canopy-forming seaweeds at global level. The results allowed to detect important synergistic interactions between nutrient enrichment, caused mainly by human activities, and different other stressors such as heavy metals, the presence of competitors, low light and increasing temperature. This suggested that local management of nutrient levels would provide the greatest opportunity for preventing the shift from canopy to mat-forming algae; 2) as second step, I analysed the status of the intertidal Cystoseira populations around the Italian coast, and explored which factors are most likely to influence it. The results reported severe depletion of intertidal populations of Cystoseira, and identified urbanization as one of the main factors related to these poor conditions, confirming the need for urgent management actions to reduce human pressures on these valuable habitat forming species; 3) then, I experimentally investigated the effects of extreme events caused by climate change. I focused my attention on the effects of abrupt increases of air temperature caused by heat-wave events on the intertidal C. compressa around the Italian coast. The results indicated that extreme heat-wave negatively affect the photosynthetic activity of C. compressa, and that local biodiversity and thermal history of the alga seem to play a role reducing or increasing respectively the impact of such extreme events. 4) I also explored the possible overlooked role of the epiphytic bacteria growing on C. compressa. Bacteria can interact with seaweeds in symbiotic, pathological and opportunistic ways, modulating the health, performance and resilience of their hosts and could, therefore play a critical role on the responses of Cystoseira spp. to stress factors. I characterised for the first time the epiphytic bacteria associated to the surface of C. compressa using Illumina Miseq sequences of V1-V3 hypervariable regions of 16S rRNA gene, and investigated their seasonal variations and their relationships with the bacterial populations in the surrounding seawater. I found that bacterial populations associated to C. compressa were clearly distinct from those in the surrounding media, and identified a clear successional pattern, interestingly characterized by an increase in abundance of potential microbial pathogens associated to older thalli of C. compressa; 5) the previous quantitative descriptive work represented an important base-knowledge to further explore experimentally whether surface bacteria could influence the responses of their hosting Cystoseira populations to stressors. I analysed experimentally in the field the interacting effects of nutrient enrichment and heat-wave events on C. compressa population, and explored whether any resulting changes in the photosynthetic activity of C. compressa were associated to changes in the epiphytic bacterial communities. The heat wave caused marked declines of the photosynthetic activity of the intertidal C. compressa. These effects persisted for at least 3 hours, while recovery generally occurred after 24 hours. The heat-wave altered the structure of the epiphytic bacteria of C. compressa. Thalli exposed to the heat-wave presented an increase of OTUs previously shown to be associated with the natural degradation of the thalli of C. compressa, or implied in causing disease or damage to macroalgae. As observed for the photosynthetic activity, these differences decreased over time, suggesting that the microbial community has the ability to recover. Differently from previous work, this experiment did not detect significant effects related to nutrient enrichment, suggesting that the effects of nutrients could be context dependent. These results open new questions concerning the mechanisms by which the epibacterial community could influence the responses and future persistence of these important canopy-forming seaweeds.