Investigating the photosynthesis of Symbiodinium in Caribbean gorgonian corals

Symbiodinium photosynthesis fuels the growth of an array of marine invertebrates, including scleractinian corals and octocorals. Studies examining the symbiosis between Caribbean octocorals and Symbiodinium are sparse, even though octocorals blanket the landscape of Caribbean coral reefs. Here, I compared the photosynthetic characteristics of Symbiodinium in four comCaribbean octocoral species (Pseudoplexaura porosa, Pseudoplexaura wagenaari, Eunicea tourneforti, and Pterogorgia anceps) in outdoor aquaria at ambient temperature. The four octocoral species exhibited similar photochemical efficiencies despite significant differences in Symbiodinium density, chlorophyll a per cell, light absorption by chlorophyll a, and rates of photosynthetic oxygen evolution. Differences in photosynthetic performance between octocoral species could not be easily attributed to the physiology of either symbiotic partner, as the four octocoral species associated with one of three Symbiodinium internal transcribed spacer 2 (ITS2) types. P. porosa and P. anceps harbored the same Symbiodinium type but exhibited markedly different photosynthetic characteristics, which highlights the importance of host morphology on Symbiodinium performance. I also compared the photosynthetic performance of Symbiodinium in discrete growth forms of Briareum asbestinum at ambient and at elevated temperature. B. asbestinum grows in either an encrusting or branching morphology, each of which co-occurs and associates with distinct Symbiodinium types (B19 in encrusting, B21 in branching). The two morphologies had different symbiotic characteristics at ambient temperature, as encrusting fragments had greater Symbiodinium and chlorophyll densities cm-2; however, photosynthetic oxygen evolution was not significantly different. In addition, branches had higher photochemical and light absorption efficiencies than encrusting fragments. At elevated temperature, more negative impacts were seen in branches than in encrusting fragments, including impaired photochemical efficiency and a decreased ratio of photosynthesis to respiration. Neither morphology exhibited coral bleaching at elevated temperature, despite negative effects of elevated temperature on photosynthesis by Symbiodinium. A decreased ratio of photosynthesis to respiration represents a potential fitness cost to branches, as the energetic contribution of their Symbiodinium may be reduced at elevated temperature. Understanding the symbioses between gorgonian corals and Symbiodinium and how they respond to elevated temperature will aid in understanding why gorgonian corals dominate many Caribbean reefs

The effects of a changing marine environment on the bioeroding sponge Cliona orientalis

Bioeroding sponges are a unique group of coral reef sponges. They transform dissolved nutrients into particulate nutrients via active filter feeding whilst also eroding the coral reef framework that they inhabit. Despite their ecological importance, we know little about their distribution or abundance, especially along the inshore Great Barrier Reef (GBR). In addition, bioeroding sponges are often considered to be thermally tolerant, even though their thermal thresholds are unknown. Bioeroding sponges also occur in high abundance in polluted or eutrophic habitats, but it is unclear whether these conditions directly benefit sponges through accelerated growth or improved condition or benefit bioeroding sponges indirectly via negative effects on corals. To address these knowledge gaps, this thesis investigated whether bioeroding sponges and their photosynthetic symbionts can tolerate changing environmental conditions on coral reefs. Research focused on Cliona orientalis as it is a conspicuous bioeroding sponge on the GBR. Field surveys were used to measure the abundance of C. orientalis on the inshore GBR and laboratory experiments were performed to investigate the response of C. orientalis to ocean warming and nutrient enrichment. Decreasing coral cover on the GBR may provide opportunities for rapid growth and expansion of other taxa. The bioeroding sponges Cliona spp. may increase in abundance after coral bleaching, damage, and mortality as they withstand elevated temperatures without bleaching. In Chapter 2, I analysed benthic surveys of the inshore GBR (2005–2014) which revealed that the percent cover of C. orientalis has not increased in the past decade, as would be expected if the sponge benefited from coral bleaching or mortality. I found that the proportion of fine particles in benthic sediments was negatively associated with the presence-absence and the percent cover of this sponge, indicating that C. orientalis requires wave-exposed habitats where fine sediments are absent. The fastest increases in C. orientalis cover coincided with the lowest macroalgal cover and chlorophyll a concentration, highlighting the importance of macroalgal competition and local environmental conditions for this sponge. Given the observed distribution and habitat preferences of C. orientalis, bioeroding sponges likely represent site-specific rather than regional threats to corals and reef accretion. Coral reefs face many stressors associated with global climate change, including increasing sea surface temperature and ocean acidification. In Chapters 3 and 4, I exposed C. orientalis to temperature increments increasing from 23 to 32 °C to define the thermal tolerance threshold of the sponge and its associated microbiome. At 32 °C, or 3 °C above the maximum monthly mean (MMM) temperature, sponges bleached and the photosynthetic capacity of Symbiodinium was compromised, consistent with sympatric corals. Cliona orientalis demonstrated little capacity to recover from thermal stress, remaining bleached with reduced Symbiodinium density and energy reserves after one month at reduced temperature. While C. orientalis can withstand current temperature extremes (<3 °C above MMM) under laboratory and natural conditions, this species would not survive ocean temperatures projected for 2100 without acclimatisation or adaptation (≥3 °C above MMM). In Chapter 4, I demonstrated that bleaching of C. orientalis is preceded by a change in its microbial community, which is not restored after the thermal stress is removed. In Chapter 5, I investigated the effects of dissolved inorganic nutrients and light intensity on the growth and condition of five common Great Barrier Reef sponges, including C. orientalis, to test whether C. orientalis responds differently than other sponge species. Dissolved nutrients up to 7 μM total DIN did not significantly affect the growth, condition, or chlorophyll content of any sponge species after 10 weeks of exposure. Light (80 vs 160 μmol quanta m⁻²-2 s⁻¹) did not affect four of the five sponge species, but higher irradiance resulted in higher organic content and chlorophyll levels in C. orientalis. Hence, as ocean temperatures increase above local thermal thresholds, C. orientalis will have a negligible impact on reef erosion, and nutrient enrichment is unlikely to alter these effects

Symbioses are restructured by repeated mass coral bleaching

Survival of symbiotic reef-building corals under global warming requires rapid acclimation or adaptation. The impact of accumulated heat stress was compared across 1643 symbiont communities before and after the 2016 mass bleaching in three coral species and free-living in the environment across ~900 kilometers of the Great Barrier Reef. Resilient reefs (less aerial bleaching than predicted from high satellite sea temperatures) showed low variation in symbioses. Before 2016, heat-tolerant environmental symbionts were common in ~98% of samples and moderately abundant (9 to 40% in samples). In corals, heat-tolerant symbionts were at low abundances (0 to 7.3%) but only in a minority (13 to 27%) of colonies. Following bleaching, environmental diversity doubled (including heat-tolerant symbionts) and increased in one coral species. Communities were dynamic (Acropora millepora) and conserved (Acropora hyacinthus and Acropora tenuis), including symbiont community turnover and redistribution. Symbiotic restructuring after bleaching occurs but is a taxon-specific ecological opportunity

Climate Change and Student Behavior: Recommendations for the University of Richmond

We, the Environmental Studies Senior Seminar Class of 2008, choose to recognize climate change as an imminent threat. After rigorous examination of the scientific, social, and political aspects of climate change, we initially wanted to help construct the carbon emissions inventory required in the PCC. However, citing their ability to build the inventory through existing University institutions, our administration steered us towards the Scope 3 emissions inventory, a component which focuses on student behavior. While we found Scope 3 too limiting, we decided our goal as a class was to impact student climate change awareness on campus. Therefore, we separated into three “working groups” and developed three distinct projects to meet our goal: 1) develop a database of projects and initiatives other universities have implemented to address climate change; 2) execute a comprehensive survey of the student body’s understanding of global climate change and energy consumption patterns and; 3) present the University of Richmond with options and recommendations for addressing climate change on campus. Our goal is to inspire individual responses to climate change. Raising awareness does not indicate everyone will or should agree with our beliefs and convictions, but it will enable individuals to come to their own conclusions. We wholeheartedly believe climate change is an issue we cannot disregard and we stand by the belief that the risk of doing nothing is the biggest danger of them all. Paper prepared for the Environmental Studies Senior Seminar Faculty Advisor: Dr. David Salisbur

Environmental drivers of variation in bleaching severity of Acropora species during an extreme thermal anomaly

High sea surface temperatures caused global coral bleaching during 2015–2016. During this thermal stress event, we quantified within- and among-species variability in bleaching severity for critical habitat-forming Acropora corals. The objective of this study was to understand the drivers of spatial and species-specific variation in the bleaching susceptibility of these corals, and to evaluate whether bleaching susceptibility under extreme thermal stress was consistent with that observed during less severe bleaching events. We surveyed and mapped Acropora corals at 10 sites (N = 596) around the Lizard Island group on the northern Great Barrier Reef. For each colony, bleaching severity was quantified using a new image analysis technique, and we assessed whether small-scale environmental variables (depth, microhabitat, competition intensity) and species traits (colony morphology, colony size, known symbiont clade association) explained variation in bleaching. Results showed that during severe thermal stress, bleaching of branching corals was linked to microhabitat features, and was more severe at reef edge compared with lagoonal sites. Bleaching severity worsened over a very short time-frame (∼1 week), but did not differ systematically with water depth, competition intensity, or colony size. At our study location, within- and among-species variation in bleaching severity was relatively low compared to the level of variation reported in the literature. More broadly, our results indicate that variability in bleaching susceptibility during extreme thermal stress is not consistent with that observed during previous bleaching events that have ranged in severity among globally dispersed sites, with fewer species escaping bleaching during severe thermal stress. In addition, shaded microhabitats can provide a refuge from bleaching which provides further evidence of the importance of topographic complexity for maintaining the biodiversity and ecosystem functioning of coral reefs

Symbiosis and host morphological variation: Symbiodiniaceae photosynthesis in the octocoral Briareum asbestinum at ambient and elevated temperatures

Intra-species morphological variation may occur in sessile organisms, such as corals, living in different habitats. Conversely, the octocoral Briareum asbestinum exhibits both encrusting and upright branching morphologies at the same shallow water habitat, enabling studying physiological differences uncoupled from habitat variation due to depth or reef location. We investigated the mutualism between endosymbiotic dinoflagellate algae, Breviolum spp. (previously clade B Symbiodinium), and these B. asbestinum morphologies at ambient and elevated temperatures. Based on msh1 gene sequences, the host morphologies were genetically similar although they differed in protein content, polyp expansion behavior, and associated Breviolum (B19 for encrusting and B21 for branching B. asbestinum). Due to colony orientation, polyps in encrusting B. asbestinum experienced irradiance levels nearly three times higher than polyps in the branching morph, which probably contributed to the lower photochemical and light absorption efficiencies of the Breviolum in encrusting fragments. The light-limited portion of photosynthesis-irradiance curves and the intracellular chlorophyll concentrations, however, indicated that Breviolum in both morphologies were acclimated to similar internal irradiances. Encrusting B. asbestinum exhibited higher Breviolum density, areal chlorophyll a, and greater photosynthetic rates cm(-2) compared to branching B. asbestinum. Notably, elevated temperature did not cause bleaching in either morphology, as Breviolum and chlorophyll densities did not differ significantly from ambient temperature, although the two morphologies adjusted some of the measured parameters, indicating coping with the stressor. In the face of continued ocean warming, the high thermal tolerance of octocorals may reinforce the shift of Caribbean reefs from scleractinian coral to octocoral dominance

Elevated seawater temperature disrupts the microbiome of an ecologically important bioeroding sponge

Bioeroding sponges break down calcium carbonate substratum, including coral skeleton, and their capacity for reef erosion is expected to increase in warmer and more acidic oceans. However, elevated temperature can disrupt the functionally important microbial symbionts of some sponge species, often with adverse consequences for host health. Here, we provide the first detailed description of the microbial community of the bioeroding sponge Cliona orientalis and assess how the community responds to seawater temperatures incrementally increasing from 23°C to 32°C. The microbiome, identified using 16S rRNA gene sequencing, was dominated by Alphaproteobacteria, including a single OTU (Rhodothalassium sp.) that represented 21% of all sequences. The 'core' microbial community (taxa present in >80% of samples) included putative nitrogen fixers and ammonia oxidizers, suggesting that symbiotic nitrogen metabolism may be a key function of the C. orientalis holobiont. The C. orientalis microbiome was generally stable at temperatures up to 27°C, however a community shift occurred at 29°C, including changes in the relative abundance and turnover of microbial OTUs. Notably, this microbial shift occurred at a lower temperature than the 32°C threshold that induced sponge bleaching, indicating that changes in the microbiome may play a role in the destabilisation of the C. orientalis holobiont. C. orientalis failed to regain Symbiodinium or restore its baseline microbial community following bleaching, suggesting that the sponge has limited ability to recover from extreme thermal exposure, at least under aquarium conditions. This article is protected by copyright. All rights reserved

Dissolved inorganic nutrient enrichment does not affect sponge growth or condition

Changing land use and an increasing human population have led to increased terrestrial runoff, which delivers nutrients, pesticides, and heavy metals into aquatic ecosystems. Elevated nutrient levels can adversely affect nearshore corals by reducing the amount of light reaching the benthos, exacerbating coral disease and bleaching, as well as stimulating algal growth, but the effects on other reef taxa are poorly understood. We investigated the effects of dissolved inorganic nutrient enrichment and changes in irradiance on the growth and condition of 5 common Great Barrier Reef sponges: 4 sponges with photosynthetic symbionts and 1 lacking photosynthetic symbionts. Concentrations of up to 7 µM total dissolved inorganic nitrogen (DIN) did not significantly affect the growth, condition, or chl a content of any sponge species after 10 wk exposure. However, 2 species lost >20% volume across all nutrient treatments, suggesting that aquarium conditions may have been suboptimal for these species. Irradiance (80 vs. 160 µmol quanta m s) did not affect 4 of the 5 sponge species; however, higher irradiance resulted in higher organic content and chl a levels in the bioeroding sponge Cliona orientalis, the only studied species that associates with the photosynthetic dinoflagellate Symbiodinium, suggesting that sponge-Symbiodinium associations may be more sensitive to irradiance levels than sponge- Cyanobacteria associations. While elevated nutrient levels are exacerbating the decline of reef-building corals, exposure to the average DIN levels within flood plumes that reach inshore reefs appears to have negligible effects on reef sponges

A decadal analysis of bioeroding sponge cover on the inshore Great Barrier Reef

Decreasing coral cover on the Great Barrier Reef (GBR) may provide opportunities for rapid growth and expansion of other taxa. The bioeroding sponges Cliona spp. are strong competitors for space and may take advantage of coral bleaching, damage, and mortality. Benthic surveys of the inshore GBR (2005–2014) revealed that the percent cover of the most abundant bioeroding sponge species, Cliona orientalis, has not increased. However, considerable variation in C. orientalis cover, and change in cover over time, was evident between survey locations. We assessed whether biotic or environmental characteristics were associated with variation in C. orientalis distribution and abundance. The proportion of fine particles in the sediments was negatively associated with the presence-absence and the percent cover of C. orientalis, indicating that the sponge requires exposed habitat. The cover of corals and other sponges explained little variation in C. orientalis cover or distribution. The fastest increases in C. orientalis cover coincided with the lowest macroalgal cover and chlorophyll a concentration, highlighting the importance of macroalgal competition and local environmental conditions for this bioeroding sponge. Given the observed distribution and habitat preferences of C. orientalis, bioeroding sponges likely represent site-specific – rather than regional – threats to corals and reef accretion

Zooxanthellar Symbionts Shape Host Sponge Trophic Status through Translocation of Carbon

Sponges belonging to the genus Cliona are common inhabitants of many coral reefs, and as bioeroders, they play an important role in the carbonate cycle of the reef. Several Cliona species maintain intracellular populations of dinoflagellate zooxanthellae (i.e., Symbiodinium spp.), which also form symbioses with a variety of other invertebrates and protists (e.g., corals, molluscs, foraminifera). Unlike the case of coral symbioses, however, almost nothing is known of the metabolic interaction between sponges and their zooxanthella symbionts. To assess this interaction, we performed a tracer experiment to follow C and N in the system, performed a reciprocal transplant experiment, and measured the stable carbon isotope ratio of Cliona spp. with and without zooxanthellae to study the influence of environment on the interaction. We found strong evidence of a transfer of C from zooxanthellae to their sponge hosts but no evidence of a transfer of N from sponge to zooxanthellae. We also saw significant influences of the environment on the metabolism of the sponges. Finally, we observed significant differences in carbon metabolism of sponge species with and without symbionts. These data strongly support hypotheses of metabolic integration between zooxanthellae and their sponge host and extend our understanding of basic aspects of benthic-pelagic coupling in shallow-water marine environments