The overgrowing, boring sponge Cliona viridis was studied on the Southwest coast of Grand Cayman Island, British West Indies. The surface area covered by the sponge was estimated using transect and quadrat surveys. Between 1 and 8 m depth, the average substrate coverage was 5%. Smaller sponge colonies were usually subcircular and larger colonies more dendritic. This change in shape may aid in exploiting new substrate. The sponge removes between 13.9% and 32.2% of the substrate as it expands laterally and produces an average erosional rate of 0.6 mm yr ⁻¹. Average sediment production rate is 1 kg m ⁻² yr ⁻¹. The chips produced by the sponge comprised only 0.0122% to 1.250% of the bottom sediments. Presumably, the majority of the sponge-produced sediments were transported out by water currents. / Thesis / Bachelor of Science (BSc)

Sponges contribute to large number of functions in coral reef ecosystems. Among these, bioerosion is perhaps one of the most widely studied, largely due to the important contribution of excavating sponges to the carbonate budget on coral reefs (up to 95 % of the total internal bioerosion). Despite our current knowledge, much of the literature is centred on individual-based observations, and little is known about their ecological role and interactions with other reef taxa in complex coral reef systems. The aim of this thesis was to quantify the ecological interactions of bioeroding sponges with major reef taxa by scaling up individual observations to population and ecosystem-based approaches. A cosmopolitan, abundant and highly competitive bioeroding sponge from Glover’s Atoll, Belize (Cliona tenuis) was used as model species. Monitoring of C. tenuis populations throughout 2009 indicated a trade-off between reproduction and growth, with the highest growth rates (31.4 ± 5.6 mm.y–1) occurring in summer, and a peak in reproductive output during winter. Populations typically show strong left-skewed size frequency distributions, mostly represented by juvenile-size individuals (46%), suggesting that regulating mechanisms (e.g. competition and predation) may be acting in constraining the transition of juveniles to adult sizes. Long-term in situ manipulations showed no effect of predation, yet competition with macroalgae significantly reduced the size of the sponge by 38% ± 11% (SE). While C. tenuis exhibit high growth and recruitment rates that could theoretically result in rapid population growth, the likelihood of sponges forming an alternative stable state as reefs sustain greater levels of disturbance is unclear. An analytical modelling approach of the interplay between macroalgae, coral and sponge was used to explore the likelihood of alternate stable states. The results show that irrespective of successful sponge invasion, inclusion of this third antagonist (in the interplay between coral and macroalgae) can qualitatively affect the likelihood of alternative stable state. The model exhibits emergent properties suggestive of intransitivity between the three competing taxa. Despite the potential of C. tenuis to benefit from disturbance, there are few cases in the literature reporting increases in bioeroding sponge abundance followed disturbance. Therefore, regulating mechanisms such as competition with other taxa, recruitment limitation or mortality are expected to exert demographic control on the populations of bioeroding sponges when space limitation is relaxed due to coral mortality. To determine processes regulating sponge populations, an individual-based spatial modelling approach was used to simulate the population dynamics of C. tenuis in a dynamic ecosystem environment. Using an orthogonal hypothesis testing approach, it was found that competition, and to a lesser extend partial mortality of the sponge tissue, largely regulate the population structure of C. tenuis. While reductions in coral cover may temporarily favour the rapid colonization by sponges, the competitive superiority of macroalgae may steal the opportunity from the opportunists.

In 2001, the Coral Reef Evaluation and Monitoring Program (CREMP) began monitoring the abundance and area covered by three clionid sponges (Cliona delitrix, C. lampa, and C. caribbaea). Subsequently, monitoring has been conducted annually at all 40 CREMP sites throughout the Florida Keys National Marine Sanctuary (FKNMS) and the Dry Tortugas. Between 2001 and 2002, mean clionid area decreased significantly from 7.6 cm2/m2 to 4.6 cm2/m2 (Wilcoxon; p= 0.035). Between 2002 and 2003, the decline to 4.5 cm2/m2 was not significant. Approximately 80% of all clionid colonies recorded at the CREMP stations covered less than 50 cm2. Among all recorded stony coral species, Montastraea annularis, M. cavernosa, and Siderastrea siderea were the most frequently and extensively invaded by clionid colonies. However, the vast majority of clionid colonies occurred in substrata not associated with a live coral colony. The mean percent cover for the four coral species identified to be most susceptible to clionid invasion had the greatest decline in the Dry Tortugas deep stations between 2001 and 2003. At Lower Keys patch-reef stations, mean percent cover showed a small, steady decrease, while at Upper Keys patch-reef stations, a small steady increase occurred. Fifteen water-quality parameters collected by the Water Quality Monitoring Network (WQMN) were analyzed to determine if clionid distributions correlated with water quality. When patch-reef sites were analyzed as a subset of sites, clionid area and abundance correlated strongly ( 0.65) with water-quality parameters that indicated higher nutrient flux and food resources. However, the correlation was weak when all 39 CREMP sites were considered ( 0.10). Clionid sponges are well known to be aggressive and successful bioeroders on coral reefs.

abstract: Some cyanobacteria, referred to as boring or euendolithic, are capable of excavating tunnels into calcareous substrates, both mineral and biogenic. The erosive activity of these cyanobacteria results in the destruction of coastal limestones and dead corals, the reworking of carbonate sands, and the cementation of microbialites. They thus link the biological and mineral parts of the global carbon cycle directly. They are also relevant for marine aquaculture as pests of mollusk populations. In spite of their importance, the mechanism by which these cyanobacteria bore remains unknown. In fact, boring by phototrophs is geochemically paradoxical, in that they should promote precipitation of carbonates, not dissolution. To approach this paradox experimentally, I developed an empirical model based on a newly isolated euendolith, which I characterized physiologically, ultrastructurally and phylogenetically (Mastigocoleus testarum BC008); it bores on pure calcite in the laboratory under controlled conditions. Mechanistic hypotheses suggesting the aid of accompanying heterotrophic bacteria, or the spatial/temporal separation of photosynthesis and boring could be readily rejected. Real-time Ca2+ mapping by laser scanning confocal microscopy of boring BC008 cells showed that boring resulted in undersaturation at the boring front and supersaturation in and around boreholes. This is consistent with a process of uptake of Ca2+ from the boring front, trans-cellular mobilization, and extrusion at the distal end of the filaments (borehole entrance). Ca2+ disequilibrium could be inhibited by ceasing illumination, preventing ATP generation, and, more specifically, by blocking P-type Ca2+ ATPase transporters. This demonstrates that BC008 bores by promoting calcite dissolution locally at the boring front through Ca2+ uptake, an unprecedented capacity among living organisms. Parallel studies using mixed microbial assemblages of euendoliths boring into Caribbean, Mediterranean, North and South Pacific marine carbonates, demonstrate that the mechanism operating in BC008 is widespread, but perhaps not universal. / Dissertation/Thesis / Ph.D. Microbiology 2010

Caribbean coral reefs have undergone changes in coral cover, structural complexity and assemblage composition since the 1970s. Although some of the ecological consequences associated with these changes have been well documented, the consequences for ecosystem functions dependent on reef structure are less well understood. In particular, there has been little research into the effects of change, on carbonate production and bioerosion; both are critical controls of structural complexity. Currently, there is only a very limited understanding of how both processes vary within and between different habitat types and what this means for ecosystem functioning. Carbonate framework production and bioerosion were investigated within three habitat types (hardgrounds, Acropora palmata reef and Orbicella reef) under sheltered and exposed wave energy regimes on Grand Cayman. Census based assessments were used, allowing the identification of functionally important species. Additionally, habitat specific calcification rates were measured for calcareous encruster communities to improve estimations of carbonate production; mean rates of calcification ranged from 0.19 to 1.14 G (1G = 1 kg CaCO3 m-2 yr-1) within hardgrounds (4–7 m), Acropora palmata reef (1–8 m) and Orbicella reef habitats (8–15 m) and were significantly higher at wave exposed sites. The rates of bioerosion for two sponge species, Siphonodictyon brevitubulatum and Cliona tenuis, were also measured and new approaches to estimating excavating sponge community bioerosion were developed to improves bioerosion estimates. Mean carbonate framework production was 0.38 G within hardgrounds, 2.65 G within Acropora palmata reef habitat and 3.54 G within Orbicella reef habitat but not significantly different between wave exposure regimes. Calcareous encruster communities, dominated by coralline algae, were identified as key carbonate producers within shallow reef habitats on the exposed south coast. They may be important to the maintenance of reef structure in these degraded reef habitats. Orbicella species were the most important carbonate producers within all reef habitats. Mean total bioerosion was 1.32, 2.27 and 2.28 G within hardgrounds, Acropora palmata reef and Orbicella reef habitats respectively. 4 Total bioerosion was not significantly different between wave exposure regimes for any habitat type, but almost completely dominated by parrotfish (29–86 %). On Grand Cayman, both carbonate framework production and bioerosion were less than that measured in comparative habitats, across the Caribbean, despite the presence of a well-managed marine protected area on the sheltered west coast. The highest rates of net carbonate production occurred in the deepest habitat - Orbicella reef (exposed: +1.45 G, sheltered: +1.07 G). Sheltered and exposed Acropora palmata reef habitat had net production rates of +0.53 and +0.30 G respectively. Hardgrounds were net erosional (-0.94 G). Overall the results suggest a change in the focal point for reef accumulation on Grand Cayman that may alter geomorphology over time. Additionally, Acropora palmata reef habitats are likely to be in a state of accretionary stasis, which may have shutdown reef growth in reef crest environments as carbonate framework produced within these habitats is a major contributor to reef accumulation at the reef crest.

The dermestid beetle (Dermestes maculatus) has become renowned in the laboratory as an aid to skeletonization of remains, both for the zoologist and the anthropologist. However, little attention has been paid to the potential effects these insects can have on hard tissues and whether their traces may be mistaken for trauma or the effects of taphonomic processes. The use of dermestid beetles in the anthropology laboratory was tested by a choice experiment based on ASTM D3345-17, examining the behavior of D. maculatus regarding Styrofoam, wood, and two types of bone. Specifically, this project tested 1.) whether the beetles showed preference for a particular material (of wood, Styrofoam, dry bone, or green bone), 2.) whether material(s) had an impact on survivorship from the larval to adult stages, and 3.) what traces dermestids leave on skeletal remains and the variation in form of those traces. Results suggest dermestid beetles will preferentially bore pupal chambers in softer materials (Styrofoam > wood > dry bone > green bone), but preference is not absolute, as pits appear in dry bone even when softer materials are present. Preference did not appear to impact survivorship. Information on the “typical” form of dermestid trace on materials is presented, as an aid to identifying these features as resulting from taphonomic processes, as opposed to ante- or perimortem processes/events.

Caribbean coral reefs are in crisis. Degradation of living coral and fish assemblages has accelerated during the past half century, with a suite of anthropogenic drivers –from local fishing pressure to unprecedented global scale climate change– implicated. Accompanying these losses is the physical disintegration of the three-dimensional calcium carbonate reef structure. Flattening of reefs, synonymous with loss of ecosystem function and provision of services, is caused by an imbalance in the carbonate budget: a trade-off between carbonate production and consolidation by calcifying organisms (principally coral-algal symbioses) and framework breakdown by bioeroding organisms and storms. This thesis focuses on expanding our understanding of two functionally critical issues that strongly influence Caribbean coral reef community composition and dynamics, and which look likely to have a key bearing on the future state of reefs in the region: coral photosynthetic endosymbionts, and carbonate budgets. The former exert an important role in the production of the coral carbonate framework, whilst the latter reflect the dynamics of reef carbonate production and erosion. In the first part of the thesis, existing information on rates of carbonate production and erosion on Caribbean reefs is utilised to construct a detailed theoretical carbonate budget model. The model is used to chart historic changes in Caribbean carbonate budgets, tracking reef flattening across time and identifying key ecological drivers of these changes. This “eco-geomorphic” model is then coupled with state-of-the-art climate and ecological models, to project reef processes to the end of the century, asking the question ‘at what point will Caribbean reefs shift to net erosional regimes?’. The models are also used to explore the efficacy of local management and climate mitigation in altering the negative trajectory of reefs under projected warming and ocean acidification. In the second part of the thesis, 632 corals from across the wider Caribbean are screened, to construct the largest recorded baseline of symbiont biogeography for the region’s key remaining reef framework builder, Montastraea annularis. Spatial patterns of symbiont diversity are explored in terms of environmental, geographic and genetic factors, contributing to the growing body of work currently in the early stages of cataloguing symbiont diversity and its ecological significance. Although carbonate budget models forecast a bleak outlook for the Caribbean, detection of widespread low-level prevalence of thermally-tolerant endosymbionts in M. annularis provides a weak ‘nugget of hope’ for potential coral acclimation. Combined local management and aggressive mitigative action on carbon emissions are pre-requisites for maintenance of functioning reefs into the next century. Coral reef conservation efforts can be improved if we fully appreciate the contributions of all reef components –not just the enigmatic ones– to healthy reef functioning.

Parrotfish are a diverse and ubiquitous group found on coral reefs worldwide. They are categorised into three main feeding modes; the browsers, scrapers and excavators, which together perform a number of important functional roles on coral reefs. Scraper and excavator parrotfish are common on most Indo-Pacific coral reefs where their roles in bioerosion, sediment production, grazing pressure and sediment reworking have been shown to influence benthic community composition, reef growth potential and sediment supply to reef habitats and reef associated sedimentary landforms. However, despite the widely known importance of parrotfish on coral reefs, our understanding of how their roles in carbonate cycling vary among species and among whole parrotfish communities in different reef habitats remains limited. This thesis produces original contributions to knowledge in the areas of species specific bioerosion estimates for the central Indian Ocean, bottom-up controls of habitat type on parrotfish assemblages and how variations in parrotfish assemblages translate to contributions to carbonate cycling processes among different reef habitats. The study was carried out across eight habitats on an atoll-edge reef platform in the central Maldives, where it was found that parrotfish community composition was driven by reef structural complexity and substrate type. Parrotfish occurred in six of the eight habitats, comprising ~44% of the platform area. Among these habitats, overall grazing pressure, bioerosion rates, sediment reworking and sediment production varied markedly. These processes were also found to have different spatial patterns over the reef platform, showing that they are not necessarily tightly coupled. In addition, reef habitats can vary in their importance for both sediment supply, and the relative importance of reworked sediment. Parrotfish produced a wide range of sediment size fractions, from < 32 to 2000 μm and produced predominantly coral sands (>80%) between 125 and 1000 μm in diameter. This is comparable to the grain types found on local reef islands, and it is likely that the most significant supply of this material is from habitats on the atoll-edge side of the platform (which make up ~20% of the total platform area). Quantifying parrotfish functional roles and understanding the drivers behind these processes is important for informing future empirical and modelling studies, particularly as coral reefs undergo a time of dramatic environmental change.

Resource managers need inexpensive bioindicators to evaluate the health of coral reef ecosystems and to inform decisions on when and where to utilize more expensive assessment techniques. Following USEPA Guidelines for Evaluating Ecological Indicators, I developed the SEDCON Index (SI), a rapid-assessment protocol whichutilizes reef sediment composition to assess the integrity of coral-reef communities. Keyadvantages of this index are that it entails non-destructive sampling and is applicable to reefs worldwide. The underlying assumption of the index is that community structure is reflected by proportions of recognizable remnants of calcareous shells and skeletal remains of mixotrophic (zooxanthellate corals and larger foraminifers), autotrophic (calcareous and coralline algae), and heterotrophic (e.g., bryozoans, molluscs, smaller foraminifers) benthic organisms, as well as unrecognizable debris as a proxy for bioerosion.

abstract: Euendolithic cyanobacteria have the remarkable ability to actively excavate and grow within certain minerals. Their activity leads to increased erosion of marine and terrestrial carbonates, negatively affecting coral reef and bivalve ecology. Despite their environmental relevance, the boring mechanism has remained elusive and paradoxical, in that cyanobacteria alkalinize their surroundings, typically leading to carbonate precipitation, not dissolution. Thus, euendoliths must rely on unique adaptations to bore. Recent work using the filamentous model euendolith Mastigocoleus testarum strain BC008 indicated that excavation relied on transcellular calcium transport mediated by P-type ATPases, but the phenomenon remained unclear. Here I present evidence that excavation in M. testarum involves an unprecedented set of adaptations. Long-range calcium transport is achieved through the coordinated pumping of multiple cells, orchestrated by the localization of calcium ATPases in a repeating annular pattern, positioned at a single cell pole, adjacent to each cell septum along the filament. Additionally, specialized chlorotic cells that I named calcicytes, differentiate and accumulate calcium at concentrations more than 500 fold those of canonical cells, likely allowing for fast calcium flow at non-toxic concentrations through undifferentiated cells. I also show, using 13C stable isotope tracers and NanoSIMS imaging, that endolithic M. testarum derives most of its carbon from the mineral carbonates it dissolves, the first autotroph ever shown to fix mineral carbon, confirming the existence of a direct link between oxidized solid carbon pools and reduced organic pools in the biosphere. Finally, using genomic and transcriptomic approaches, I analyze gene expression searching for additional adaptations related to the endolithic lifestyle. A large and diverse set of genes (24% of 6917 genes) were significantly differentially regulated while boring, including several master regulators and genes expectedly needed under this condition (such as transport, nutrient scavenging, oxidative stress, and calcium-binding protein genes). However, I also discovered the up-regulation of several puzzling gene sets involved in alternative carbon fixation pathways, anaerobic metabolism, and some related to photosynthesis and respiration. This transcriptomic data provides us with several new, readily testable hypotheses regarding adaptations to the endolithic lifestyle. In all, my data clearly show that boring organisms show extraordinarily interesting adaptations. / Dissertation/Thesis / Doctoral Dissertation Microbiology 2016