Dinitrogen fixation in coral reef ecosystems facing climate change

Abstract

Biological dinitrogen (N2) fixation exerts important control on the ocean s nitrogen (N) inventory and primary productivity. Among marine ecosystems, coral reefs are notable for their very high productivity in extremely oligotrophic waters, where N2 fixation has long been thought to satisfy much of the demand for new N. Furthermore, N2 fixation in coral reef ecosystems may importantly contribute to global marine N inputs. However, because of large uncertainty in (i) the distribution of N2 fixation in coral reefs and (ii) the tightness of the coupling between N2 fixation and primary production, the ecological significance of N2 fixation in coral reef ecosystems is still not resolved. The core of this thesis describes and discusses three different aspects of N2 fixation in coral reefs. The first part of the thesis, through a series of interconnected studies, focuses on the relationship between N2 fixation and primary productivity in the water column and in key benthic organisms at a fringing coral reef in the northern Red Sea (Gulf of Aqaba). This site harbours some of the northernmost warm water coral reefs on Earth. The characteristic seasonality of the sampling location allowed an investigation of the contribution of N2 fixing prokaryotes (diazotrophs) to changing N requirements of the primary producers in response to pronounced seasonal environmental variations. Findings reveal that the reef water and its planktonic community contributed only marginally to the input of fixed N into the reef ecosystem. Concurrently, benthic N2 fixation was conspicuous, and the rule rather than the exception in all benthic substrates investigated. Rates of N2 fixation varied greatly between different substrates. Microbial mats, turf algae, bare hard substrates, and bare sediment contributed most fixed N to the reef, while soft corals showed the lowest N2 fixation activity. N2 fixation rates were significantly higher in summer, when nutrient availability was lowest and water temperature and light intensity highest. This indicates an important role of diazotrophy in sustaining the N demand of reef primary producers during the nutrient-depleted season. Furthermore, the susceptibility of diazotrophs to the varying environmental conditions suggests that disturbances resulting from human activities will also likely determine changes in the extent of N2 fixation on reefs. In this context, in the second part of this thesis, results of two different manipulative experiments are presented that showed that ocean warming and ocean acidification have a high potential to impact N2 fixation in scleractinian corals. This part of the thesis focused on scleractinian coral holobionts (the cnidarian-dinoflagellate-diazotroph symbiosis) because of their role as primary reef ecosystem engineers. Results demonstrate that thermal stress impacted all holobiont members and suggest that physiological plasticity of coral-associated diazotrophs, by fixing additional N under high temperature, may help to maintain constant chlorophyll a levels and prevent the breakdown of the coral-algal symbiosis. However, these beneficial effects may be counterbalanced by the impact of the ongoing increase in dissolved CO2 levels (i.e., ocean acidification). A decrease in coral host calcification resulted in decreased N2 fixation activity, since these two processes may compete for energy in the holobiont. Overall, these results contribute to the understanding of the role that coral-associated diazotrophs play in the holobiont under normal and stressful conditions. Finally, in the third part of this thesis, the relative contribution of all typical reef-associated habitats to primary production and N2 fixation of the entire ecosystem is discussed using budget calculations and a geographic information system approach. Results show that high coral-cover areas of the reef, because of their structural complexity, were not only important for their primary productivity but also for their associated N2 fixation, with areal rates competing with those of flat sandy areas. Overall, N2 fixation was highly susceptible to environmental changes, with 4-fold areal rates in all reef habitats during the nutrient-depleted season, which provided ca. 20% of the N needed for net primary production. Finally, global extrapolations confirm that coral reef ecosystems are among the benthic communities contributing most to marine fixed N inputs. In conclusion, this thesis demonstrates the importance and susceptibility of N2 fixation in coral reef ecosystems. Still, large uncertainties remain in the potential responses to climate change, requiring further assessments. It is clear, however, that the tight coupling between N2 fixation and reef primary productivity will determine feedback loops where perturbations of N2 fixation will have repercussions in the carbon cycle, and vice versa.