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    Benthic dinitrogen fixation in a Northern Red Sea coral reef under seasonally changing environmental conditions
    Tropical coral reefs are among the most productive ecosystems on this planet, despite being surrounded by very oligotrophic waters. Effective recycling processes of the limiting nutrients, particularly nitrogen (N), and input of new bioavailable N via dinitrogen (N2) fixation are essential to sustain such high gross primary production. In fact, several benthic reef organisms and substrates are associated with diverse communities of N2 fixing microbes (diazotrophs), but the respective contribution of the different benthic groups to total benthic N2 fixation and the effect of changing environmental conditions on N2 fixation have not been investigated yet. Therefore, this thesis, through a series of interconnected studies carried out in a seasonally dynamic coral reef system, the Northern Red Sea, and in a number of manipulative experiments, contributes to the understanding of benthic N2 fixation in coral reefs by answering the following key questions: 1) How much N2 is fixed by the dominant benthic groups in the Northern Red Sea? 2) What is the relative contribution of the benthic groups to total benthic N2 fixation within the reef? 3) What is the effect of seasonally changing environmental conditions and of single environmental factors on key metabolic processes, particularly N2 fixation, associated with the different benthic groups? Findings revealed that all investigated benthic groups showed N2 fixation activity, whereof bare coral rock, turf algae, carbonate sands and living hard corals were the main N2 fixing components contributing ~ 90% to benthic N2 fixation in investigated Red Sea coral reefs. Soft corals revealed the lowest N2 fixation activity among all investigated groups and released significantly less organic matter to the surrounding water compared to hard corals indicating that N2 fixation may also influence their role as allogenic ecosystem engineers. N2 fixation by most benthic groups was usually highest when nutrient availability was lowest, and water temperature as well as light intensity highest suggesting that the N2 fixation products fuel the metabolic N requirements of reef organisms, particularly during nutrient-depleted conditions (i.e. summer). The manipulation of single environmental factors revealed a stimulation of N2 fixation activities under global warming conditions and a reduction under ocean acidification scenarios indicating that global climate change will affect the nutrient status of reef organisms. In summary, this thesis underlines the ubiquity of N2 fixation associated with different benthic coral reef organisms and substrates, and highlights its importance in sustaining coral reef productivity. Both, the benthic community structure and the prevailing environmental conditions appear to be important in controlling the amount of N2 fixation in coral reefs. Finally, as coral reefs are increasingly and simultaneously exposed to global and local stressors, it is necessary to understand how important metabolic processes on coral reefs (i.e. organic matter fluxes and N2 fixation activity) will be affected, and this thesis provides first quantitative insights into these processes from physiological, biogeochemical and ecological points of view.
    doctoral thesis
      347  189
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    The physiology of coral reef calcifiers under local and global stressors
    Anthropogenic activities have caused coral reefs worldwide to face extreme changes in their environment at both global and local scales. This thesis covers the effects of ocean acidification (OA) and eutrophication through increased dissolved organic carbon (DOC) availability on coral reef calcifiers. In this thesis the individual and combined effects of OA as increased dissolved inorganic carbon (DIC) and high availability of DOC on the physiology of reef building corals from the Great Barrier Reef and calcifying green algae from the Indo-Pacific and the Caribbean are investigated. More specifically, calcification processes, photosynthesis and nitrogen fixation of the coral holobiont and calcifying green algae were investigated. This thesis revealed that the physiology of the calcifiers investigated is negatively affected by both high DIC and DOC concentrations. These findings will be crucial to be able to investigate future reef changes under high DIC and increased DOC concentrations. Our findings on calcification rates and calcification structures can be used as indicators of environmental change and as future predictors.
    doctoral thesis
      432  206
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    Dinitrogen fixation in coral reef ecosystems facing climate change
    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.
    doctoral thesis
      382  208
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    Coral holobiont functioning under global environmental change
    The tropical scleractinian coral holobiont is comprised by the coral animal, dinoflagellate algae of the genus Symbiodinium, and a multitude of other microbes, specifically bacteria, archaea, viruses, and protists. These holobionts are the unit of ecological selection, and remarkably adapted to thrive under oligotrophic (nutrient-poor) conditions. The foundation for this adaptation is provided by the coral-algae symbiosis, a mutualistic nutrient exchange relationship between the coral and Symbiodinium, allowing for the high primary productivity and growth rates of tropical coral holobionts. The coral-algae symbiosis is maintained via nitrogen limitation by the host, and new nitrogen from heterotrophic feeding, dissolved nutrient uptake, or coral-associated nitrogen fixation activity is retained and taken up within the holobiont. This thesis highlights the importance of functional dependencies on nitrogen cycling, particularly the nitrogen fixation pathway, in coral holobiont functioning, and the importance of employing a large set of response parameters covering critical functions of the main holobiont members.
    doctoral thesis
      535  536
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    Effects of disturbances on microbial community composition and activity of biofilms from the Great Barrier Reef
    Tropical coral reefs worldwide are increasingly threatened by disturbances on both global and local scales. Of particular concern are reef ecosystems in close proximity to urbanized coastal areas, where extreme weather events in the summer wet seasons result in terrestrial runoff leading to reduced light and increased nutrient availability for benthic coral reef communities. Such runoff may deteriorate water quality along the Great Barrier Reef coast and hence affect coral reef dynamics, productivity and composition. Microbial biofilms respond rapidly to changing environmental conditions and may be useful bioindicators for water quality. To test this potential, microbial communities associated with biofilms were analysed by terminal restriction fragment length polymorphism (T-RFLP) and sequencing of 16S rRNA genes. Further, O2 fluxes, biofilm biomass and chlorophyll a contents were determined. Overall, microbial communities in biofilms established on standardised substrata (glass slides) shifted in response to high temperature, nitrate, pCO2 and light availability, and thus, efficiently reflect changes in ambient water conditions. Seasonal and water quality driven shifts in the relative abundances of key microbial groups in biofilms suggest they are useful bioindicators for tropical coastal water quality and may have implications for future coastal management. Further, it is suggested that climate change and terrestrial runoff will likely impact productivity, composition and functioning in future coral reef ecosystems.
    doctoral thesis
      344  372
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    The role of macroalgae and the corallivorous fireworm Hermodice carunculata on coral reef resilience in the Caribbean
    This thesis is composed of five chapters representing studies that investigate the impact of two important stressors strongly influencing coral reef resilience in the Caribbean: macroalgal competition with corals and corallivory by fireworms. Macroalgae are superior competitors for space in coral reefs due to their 1) high ability to adapt to changing environmental conditions such as elevated nutrient availabilities and sea surface temperatures, 2) optimized reproductive strategies and life cycles, and 3) potent allelochemical characteristics during interaction processes. Invertebrate corallivory is an important stressor of present-day reefs, in which its impact can lead to fundamental changes in reef state. During a preliminary visit to Curaçao, Netherlands Antilles, the designated study area for this thesis, we observed high abundances of macroalgae and an invertebrate corallivore, the bearded fireworm Hermodice carunculata, particularly in the presence of macroalgae. Together with gastropods, fireworms constitute potentially the most influential corallivorous organisms in Caribbean reefs, and population outbreaks have been associated with impaired coral recovery after disturbances. Recent work showed that this invertebrate corallivore may also act as a vector for coral bleaching pathogens in the Mediterranean, but its importance with regard to coral reef resilience has not been addressed since the late 1960s. Reciprocally, impaired coral reef resilience will inevitably lead to 1) declining reproductive output and recruitment, 2) higher susceptibility to and longer regeneration times after disturbances such as mass coral bleaching and disease events, and 3) the loss of diversity and structural integrity. Alternate and stable state macroalgae-dominated reefs deprived of original functionality are of major concern and have been observed throughout the Caribbean, especially under declining environmental conditions, which hold true for most Caribbean reef systems. The fringing reefs of Curaçao, Southern Caribbean, are considered relatively intact for Caribbean standards, i.e. still in a coral-dominated state, and therefore represent suitable study sites to carry out experimental work. Although detailed studies exist with regard to macroalgal characteristics, very little is known about the corallivore H. carunculata, and no information exists with regard to their specific effects on scleractinian corals, particularly during coral-algal interactions, and their ecological role during impaired coral reef resilience scenarios. The objectives of my thesis thus were to investigate separate and synergistic effects of these two prominent stressors on Caribbean reef systems. As a fundament, we provide the first comprehensive ecological study on principle characteristics of the corallivore H. carunculata. Using multiple approaches including in situ experiments, quantitative analytical tools and molecular techniques, we investigated its ecological role within coral reefs and determined its origin and distribution based on its phylogeny. Then, we explored the specific effects of macroalgal competition and corallivory on the major reef building coral in Curaçaoan reefs. Supplementary in situ and laboratory experimental studies provided detailed information on the kind, diversity and severity of their detrimental impacts for scleractinian coral communities. Ultimately, potentially synergistic effects of both stressors for Curaçao s major reef building coral were identified under natural conditions and discerned using specific laboratory experiments.
    doctoral thesis
      360  189