Benthic Cyanobacterial Diversity and Antagonistic Interactions in Abrolhos Bank: Allelopathy, Susceptibility to Herbivory, and Toxicity

Benthic cyanobacterial mats (BCMs) are conspicuous components of coral reef communities, where they play key ecological roles as primary producers among others. BCMs often bloom and might outcompete neighboring benthic organisms, including reef-building corals. We investigated the cyanobacterial species composition of three BCMs morphotypes from the marginal reef complex of Abrolhos Bank (Southeastern Brazil). Also, we assessed their allelopathic effects on coral zooxanthellae, their susceptibility to herbivory by fish, and their toxicity to brine shrimp nauplii. Morphology and 16S rDNA sequencing unveiled the cyanobacteria Moorena bouillonii, Okeania erythroflocculosa, Adonisia turfae, Leptolyngbya sp., and Halomicronema sp. as components of BCMs from Abrolhos. BCMs cell-free filtrates and extracts exerted an allelopathic effect by reducing the growth of the ex hospite Symbiodinium sp. in culture. BCMs-only treatments remained untouched in field susceptibility assays in contrast to macroalgae only and mixed BCMs-macroalgae treatments that had the macroalgae fully removed by reef fish. Crude aqueous extracts from BCMs were toxic to brine shrimps in acute assays. Besides unveiling the diversity of BCMs consortia in Abrolhos, our results cast some light on their allelopathy, antiherbivory, and toxicity properties. These antagonistic interactions might promote adverse cascading effects during benthic cyanobacteria blooms and in gradual shifts to BCMs-dominated states.

Coral reef biofilm bacterial diversity and successional trajectories are structured by reef benthic organisms and shift under chronic nutrient enrichment

Work on marine biofilms has primarily focused on host-associated habitats for their roles in larval recruitment and disease dynamics; little is known about the factors regulating the composition of reef environmental biofilms. To contrast the roles of succession, benthic communities and nutrients in structuring marine biofilms, we surveyed bacteria communities in biofilms through a six-week succession in aquaria containing macroalgae, coral, or reef sand factorially crossed with three levels of continuous nutrient enrichment. Our findings demonstrate how biofilm successional trajectories diverge from temporal dynamics of the bacterioplankton and how biofilms are structured by the surrounding benthic organisms and nutrient enrichment. We identify a suite of biofilm-associated bacteria linked with the orthogonal influences of corals, algae and nutrients and distinct from the overlying water. Our results provide a comprehensive characterization of marine biofilm successional dynamics and contextualize the impact of widespread changes in reef community composition and nutrient pollution on biofilm community structure.

EVIDENCE OF MASS MORTALITY OF THE LONG-LIVED BIVALVE MERCENARIA STIMPSONI CAUSED BY A CATASTROPHIC TSUNAMI

ABSTRACT Tsunamis are huge disasters that can significantly damage benthic organisms and the sea-bottom environment in coastal areas. It is of great ecological importance to understand how benthic ecosystems respond to such destructive forces and how individual species are affected. Investigating the effect of such disasters on animals that are seldom caught alive is particularly difficult. Bivalve mollusks are especially suitable for investigating how a tsunami affects coastal benthic species because they preserve an environmental record in their shells that can be extended back in time by crossdating the records of multiple individuals. Here we studied dead shells of Mercenaria stimpsoni, a long-lived clam, and precisely determined the time of death by using nuclear bomb–induced radiocarbon (bomb-14C) and by counting annual growth increments. First, a quasi-continuous, regional bomb-14C record was created by analyzing the shells of 6 live-caught M. stimpsoni individuals. Then 27 dead shells collected from the seafloor of Funakoshi Bay were 14C-dated and analyzed. The results showed that the huge tsunami that struck northeastern Japan on 11 March 2011 caused mass mortality of this bivalve in Funakoshi Bay. Nine of the 27 clams died during the March 2011 tsunami, probably by starvation after burial by tsunami deposits or exposure above the seafloor as a result of sediment liquefaction during the earthquake. The dating method used in this study can help us understand how long-lived marine organisms with low population density are affected by huge natural disasters such as a tsunami.

Factors Affecting Coral Recruitment and Calcium Carbonate Accretion Rates on a Central Pacific Coral Reef

<p>Coral recruitment and calcium carbonate (CaCO₃) accretion are fundamental processes that help maintain coral reefs. Many reefs worldwide have experienced degradation, including a decrease in coral cover and biodiversity. Successful coral recruitment helps degraded reefs to recover, while CaCO₃ accretion by early successional benthic organisms maintains the topographic complexity of a coral reef system. It is therefore important to understand the processes that affect coral recruitment and CaCO₃ accretion rates in order to understand how coral reefs recover from disturbances. The aim of this thesis was to determine how biophysical forcing factors affect coral recruitment, calcification and bioerosion on a pristine coral reef. I used artificial settlement tiles to measure coral recruitment and CaCO₃ accretion at ten sites (four on the fore reef, four on the Western Reef Terrace and two at the Entrance Channel) at Palmyra Atoll. Fungia skeletons and pieces of dead coral rock were used to measure bioerosion rates, which were combined with the CaCO₃ accretion rates to obtain a net CaCO₃ budget of the reef substratum. Interactions between coral recruits and other benthic organisms on the settlement tiles were recorded to determine the settlement preferences and competitive strength of coral recruits. The settlement preference of Pocillopora damicornis for divots shaped like steephead and bumphead parrotfish bites marks was determined by adding P. damicornis larvae to a container with a settlement tile with the aforementioned divots. I found that coral recruitment and CaCO₃ accretion are influenced by biophysical forcing factors. Most pocilloporids likely recruit close to their parents while the origin of poritid larvae is much more distant. Pocilloporid recruitment rates were also significantly correlated with the successional stage of the benthic community on the settlement tiles, especially the cover of biofilm and bryozoa. Biofilm and crustose coralline algae (CCA) were preferred as settlement substrata by coral larvae, however both pocilloporids and poritids settled on a large number of different benthic substrata. P. damicornis larvae showed a significant settlement preference for divots shaped like parrotfish bite marks over a flat settlement surface. Coral recruits were good competitors against encrusting algae but were often outcompeted by filamentous and upright algae. Settlement tiles were almost entirely colonised by benthic organisms within three to twelve months of deployment. The mass of CaCO₃ deposited onto the settlement tiles negatively correlated with herbivore grazing pressure on the benthic community. Bioerosion rates within pieces of coral (internal bioerosion) increased over time but overall bioerosion rates (internal and external) rarely exceeded CaCO₃ deposition by CCA. My results show how variability in biophysical forcing factors leads to natural variation in coral recruitment and CaCO₃ accretion. This thesis highlights the importance of measuring herbivore grazing, CCA and turf algae cover to gain a better understanding of reef resilience. I conclude that models constructed for Caribbean reefs may not be suited to predict resilience in Pacific reefs and that within the Pacific, two different kinds of resilience models need to be constructed, one for human-inhabited coral reefs and one for uninhabited coral reefs.</p>

Factors Affecting Coral Recruitment and Calcium Carbonate Accretion Rates on a Central Pacific Coral Reef

<p>Coral recruitment and calcium carbonate (CaCO₃) accretion are fundamental processes that help maintain coral reefs. Many reefs worldwide have experienced degradation, including a decrease in coral cover and biodiversity. Successful coral recruitment helps degraded reefs to recover, while CaCO₃ accretion by early successional benthic organisms maintains the topographic complexity of a coral reef system. It is therefore important to understand the processes that affect coral recruitment and CaCO₃ accretion rates in order to understand how coral reefs recover from disturbances. The aim of this thesis was to determine how biophysical forcing factors affect coral recruitment, calcification and bioerosion on a pristine coral reef. I used artificial settlement tiles to measure coral recruitment and CaCO₃ accretion at ten sites (four on the fore reef, four on the Western Reef Terrace and two at the Entrance Channel) at Palmyra Atoll. Fungia skeletons and pieces of dead coral rock were used to measure bioerosion rates, which were combined with the CaCO₃ accretion rates to obtain a net CaCO₃ budget of the reef substratum. Interactions between coral recruits and other benthic organisms on the settlement tiles were recorded to determine the settlement preferences and competitive strength of coral recruits. The settlement preference of Pocillopora damicornis for divots shaped like steephead and bumphead parrotfish bites marks was determined by adding P. damicornis larvae to a container with a settlement tile with the aforementioned divots. I found that coral recruitment and CaCO₃ accretion are influenced by biophysical forcing factors. Most pocilloporids likely recruit close to their parents while the origin of poritid larvae is much more distant. Pocilloporid recruitment rates were also significantly correlated with the successional stage of the benthic community on the settlement tiles, especially the cover of biofilm and bryozoa. Biofilm and crustose coralline algae (CCA) were preferred as settlement substrata by coral larvae, however both pocilloporids and poritids settled on a large number of different benthic substrata. P. damicornis larvae showed a significant settlement preference for divots shaped like parrotfish bite marks over a flat settlement surface. Coral recruits were good competitors against encrusting algae but were often outcompeted by filamentous and upright algae. Settlement tiles were almost entirely colonised by benthic organisms within three to twelve months of deployment. The mass of CaCO₃ deposited onto the settlement tiles negatively correlated with herbivore grazing pressure on the benthic community. Bioerosion rates within pieces of coral (internal bioerosion) increased over time but overall bioerosion rates (internal and external) rarely exceeded CaCO₃ deposition by CCA. My results show how variability in biophysical forcing factors leads to natural variation in coral recruitment and CaCO₃ accretion. This thesis highlights the importance of measuring herbivore grazing, CCA and turf algae cover to gain a better understanding of reef resilience. I conclude that models constructed for Caribbean reefs may not be suited to predict resilience in Pacific reefs and that within the Pacific, two different kinds of resilience models need to be constructed, one for human-inhabited coral reefs and one for uninhabited coral reefs.</p>

Impact of the local environmental variability on the patterns of coral recruitment on Indo-Pacific reefs

<p>Coral reefs are threatened by a range of human activities at both local and global scales. The result of these impacts has resulted in a worldwide decline in the coral reef ecosystems. Corals are the principle reef builders and the maintenance of their populations is fundamental for healthy reef ecosystems. Local environmental factors are critically important in shaping coral populations, particularly at the post-settlement phase, when young coral colonies are most vulnerable to disturbances. In this context, understanding the environmental factors that drive coral recruitment and affect coral survivorship in the early life history stages is vital to effectively manage coral reefs. In this thesis I began by investigating the effect of abiotic and biological factors on coral recruitment and juvenile coral life history stages using settlement panels deployed in the Wakatobi Marine National Park (SE Sulawesi, Indonesia). My objectives were to assess the spatio-temporal variability in coral recruitment rates and juvenile abundance. I used a modelling approach to identify the environmental factors that affected the distribution and abundance patterns of corals. Then, I focused on the main environmental factors, identified from previously published research, affecting coral recruitment. I conducted a caging experiment to assess the impact of fish predation on coral juveniles. Finally, I analysed the development of the benthic community and the interactions between corals and benthic organisms in the first two years of colonisation of artificial bare surfaces. I found high spatial and temporal variability in recruitment rates over seven years of data, values were lower than on other Indo-Pacific reefs and ranged from 9.6 (±8.21 SE) to 317.19 (±12.76 SE) rec. m⁻²; while juvenile abundance ranged from 4.2 (±1.49 SE) to 33 (±6.36 SE) juv. m⁻². The local characteristics of the sites, such as coral cover, influenced the distribution of coral colonies in early life history stages; furthermore differences in coral density between the two life history stages (juvenile and recruits) were consistent over time. However, no single or combination of factors adequately explained abundance patterns for either recruits or juveniles. Fish predation did not appear to be the main cause of coral post-settlement mortality in the Wakatobi and it affected only 10.8% of the coral juveniles in the experiment. In contrast, 58.51% of the coral juveniles were found to be overgrown by algae and other invertebrates, however only turf and green encrusting algae affected coral survivorship. Coral colony abundance and the number of interactions with other benthic organisms, especially crustose coralline algae (CCA) and sponges, increased over time on panels and they were different between the front and back side of the panels, which was attributed to differences in light and predation regimes. Coral recruitment was higher on older benthic communities, although none of the known coral recruitment promoters, such as CCA, or competitors, such as turf algae, were correlated with coral abundance. My results show that changes in coral populations between the recruit and juvenile stages are likely driven by small-scale processes. The site characteristics determine the final patterns, which vary over time following temporal fluctuations in environmental factors. The effect of the interactions between algae and sponges with coral recruits and their influence on juvenile survivorship suggests these organisms having a role in coral recruitment success and highlight their importance as a focus for reef management. Furthermore, the use of long term studies allowed a better understanding of the high variability present in coral recruitment and the trends of the recruitment process, which are useful information for conservative purposes.</p>

Impact of the local environmental variability on the patterns of coral recruitment on Indo-Pacific reefs

<p>Coral reefs are threatened by a range of human activities at both local and global scales. The result of these impacts has resulted in a worldwide decline in the coral reef ecosystems. Corals are the principle reef builders and the maintenance of their populations is fundamental for healthy reef ecosystems. Local environmental factors are critically important in shaping coral populations, particularly at the post-settlement phase, when young coral colonies are most vulnerable to disturbances. In this context, understanding the environmental factors that drive coral recruitment and affect coral survivorship in the early life history stages is vital to effectively manage coral reefs. In this thesis I began by investigating the effect of abiotic and biological factors on coral recruitment and juvenile coral life history stages using settlement panels deployed in the Wakatobi Marine National Park (SE Sulawesi, Indonesia). My objectives were to assess the spatio-temporal variability in coral recruitment rates and juvenile abundance. I used a modelling approach to identify the environmental factors that affected the distribution and abundance patterns of corals. Then, I focused on the main environmental factors, identified from previously published research, affecting coral recruitment. I conducted a caging experiment to assess the impact of fish predation on coral juveniles. Finally, I analysed the development of the benthic community and the interactions between corals and benthic organisms in the first two years of colonisation of artificial bare surfaces. I found high spatial and temporal variability in recruitment rates over seven years of data, values were lower than on other Indo-Pacific reefs and ranged from 9.6 (±8.21 SE) to 317.19 (±12.76 SE) rec. m⁻²; while juvenile abundance ranged from 4.2 (±1.49 SE) to 33 (±6.36 SE) juv. m⁻². The local characteristics of the sites, such as coral cover, influenced the distribution of coral colonies in early life history stages; furthermore differences in coral density between the two life history stages (juvenile and recruits) were consistent over time. However, no single or combination of factors adequately explained abundance patterns for either recruits or juveniles. Fish predation did not appear to be the main cause of coral post-settlement mortality in the Wakatobi and it affected only 10.8% of the coral juveniles in the experiment. In contrast, 58.51% of the coral juveniles were found to be overgrown by algae and other invertebrates, however only turf and green encrusting algae affected coral survivorship. Coral colony abundance and the number of interactions with other benthic organisms, especially crustose coralline algae (CCA) and sponges, increased over time on panels and they were different between the front and back side of the panels, which was attributed to differences in light and predation regimes. Coral recruitment was higher on older benthic communities, although none of the known coral recruitment promoters, such as CCA, or competitors, such as turf algae, were correlated with coral abundance. My results show that changes in coral populations between the recruit and juvenile stages are likely driven by small-scale processes. The site characteristics determine the final patterns, which vary over time following temporal fluctuations in environmental factors. The effect of the interactions between algae and sponges with coral recruits and their influence on juvenile survivorship suggests these organisms having a role in coral recruitment success and highlight their importance as a focus for reef management. Furthermore, the use of long term studies allowed a better understanding of the high variability present in coral recruitment and the trends of the recruitment process, which are useful information for conservative purposes.</p>