Measuring multi-year changes in the Symbiodiniaceae algae in Caribbean corals on coral-depleted reefs

Monitoring coral cover can describe the ecology of reef degradation, but rarely can it reveal the proximal mechanisms of change, or achieve its full potential in informing conservation actions. Describing temporal variation in Symbiodiniaceae within corals can help address these limitations, but this is rarely a research priority. Here, we augmented an ecological time series of the coral reefs of St. John, US Virgin Islands, by describing the genetic complement of symbiotic algae in common corals. Seventy-five corals from nine species were marked and sampled in 2017. Of these colonies, 41% were sampled in 2018, and 72% in 2019; 28% could not be found and were assumed to have died. Symbiodiniaceae ITS2 sequencing identified 525 distinct sequences (comprising 42 ITS2 type profiles), and symbiont diversity differed among host species and individuals, but was in most cases preserved within hosts over 3 yrs that were marked by physical disturbances from major hurricanes (2017) and the regional onset of stony coral tissue loss disease (2019). While changes in symbiont communities were slight and stochastic over time within colonies, variation in the dominant symbionts among colonies was observed for all host species. Together, these results indicate that declining host abundances could lead to the loss of rare algal lineages that are found in a low proportion of few coral colonies left on many reefs, especially if coral declines are symbiont-specific. These findings highlight the importance of identifying Symbiodiniaceae as part of a time series of coral communities to support holistic conservation planning. Repeated sampling of tagged corals is unlikely to be viable for this purpose, because many Caribbean corals are dying before they can be sampled multiple times. Instead, random sampling of large numbers of corals may be more effective in capturing the diversity and temporal dynamics of Symbiodiniaceae metacommunities in reef corals

From polyps to pixels: understanding coral reef resilience to local and global change across scales

Abstract Context Coral reef resilience is the product of multiple interacting processes that occur across various interacting scales. This complexity presents challenges for identifying solutions to the ongoing worldwide decline of coral reef ecosystems that are threatened by both local and global human stressors. Objectives We highlight how coral reef resilience is studied at spatial, temporal, and functional scales, and explore emerging technologies that are bringing new insights to our understanding of reef resilience. We then provide a framework for integrating insights across scales by using new and existing technological and analytical tools. We also discuss the implications of scale on both the ecological processes that lead to declines of reefs, and how we study those mechanisms. Methods To illustrate, we present a case study from Kāneʻohe Bay, Hawaiʻi, USA, linking remotely sensed hyperspectral imagery to within-colony symbiont communities that show differential responses to stress. Results In doing so, we transform the scale at which we can study coral resilience from a few individuals to entire ecosystems. Conclusions Together, these perspectives guide best practices for designing management solutions that scale from individuals to ecosystems by integrating multiple levels of biological organization from cellular processes to global patterns of coral degradation and resilience

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.journal articl

Development of Gene Expression Markers of Acute Heat-Light Stress in Reef-Building Corals of the Genus Porites

Coral reefs are declining worldwide due to increased incidence of climate-induced coral bleaching, which will have widespread biodiversity and economic impacts. A simple method to measure the sub-bleaching level of heat-light stress experienced by corals would greatly inform reef management practices by making it possible to assess the distribution of bleaching risks among individual reef sites. Gene expression analysis based on quantitative PCR (qPCR) can be used as a diagnostic tool to determine coral condition in situ. We evaluated the expression of 13 candidate genes during heat-light stress in a common Caribbean coral Porites astreoides, and observed strong and consistent changes in gene expression in two independent experiments. Furthermore, we found that the apparent return to baseline expression levels during a recovery phase was rapid, despite visible signs of colony bleaching. We show that the response to acute heat-light stress in P. astreoides can be monitored by measuring the difference in expression of only two genes: Hsp16 and actin. We demonstrate that this assay discriminates between corals sampled from two field sites experiencing different temperatures. We also show that the assay is applicable to an Indo-Pacific congener, P. lobata, and therefore could potentially be used to diagnose acute heat-light stress on coral reefs worldwide

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships

The Role of Algal Symbiont Community Dynamics in Reef Coral Responses to Global Climate Change

The continued growth and survival of reef-building corals is essential to sustain the goods and services provided by coral reefs, worth billions of dollars annually. However, warming oceans are causing more frequent and severe episodes of coral bleaching, the breakdown of symbiosis between corals and their algal symbionts (Symbiodinium spp.), which threatens corals’ survival unless they can adapt or acclimatize. One way that corals may increase their thermal tolerance is by associating with different Symbiodinium types. Changes in partner abundance may also have functional consequences, but these symbiont dynamics are poorly understood. This dissertation aims to provide a clearer understanding of Symbiodinium community dynamics in corals by investigating changes in both partner identity and abundance over time, the factors driving these changes, and their functional consequences. First, I developed methods to analyze Symbiodinium community structure based on quantitative PCR, overcoming limitations of other techniques while providing a more physiologically relevant metric of symbiont density – the symbiont to host cell ratio. I then applied these techniques to simultaneously assay symbiont identity and abundance in corals under fluctuating environmental conditions. I show that naturally-variable symbiont densities converged under constant conditions to clade-specific equilibria and readjusted to new equilibria when conditions change. To explain these patterns, I used a mathematical  model to show that corals maintain an “optimal” symbiont abundance in a given environment that maximizes the net benefit of the symbiosis, suggesting that partner density regulation facilitates coral acclimatization in a dynamic environment. While symbiont abundance in the Pacific coral Pocillopora damicornis increased under warmer temperatures, corals with more symbionts were more susceptible to thermal bleaching, establishing a quantitative mechanistic link between symbiont abundance and the molecular basis for coral bleaching. Higher symbiont abundance also caused more severe bleaching in the Caribbean corals Orbicella faveolata and Siderastraea siderea, confirming the generality of this phenomenon and indicating that environmental conditions that increase symbiont densities, such as nutrient pollution, may exacerbate climate change-induced coral bleaching. However, corals may resist bleaching by increasing the relative proportion of thermally tolerant symbionts, which I show is more likely to occur when corals bleach more severely and recover at higher temperatures. These findings reconcile conflicting reports over whether corals change their symbionts in response to environmental stress by showing that the magnitude of symbiont shuffling is determined within an ecological framework by disturbance, niche differentiation, and competition among symbiont types. However, species-specific influences also determine symbiont community trajectories, evidenced by greater shifts to thermally tolerant communities in S. siderea compared to O. faveolata. To investigate potential tradeoffs associated with thermally tolerant symbionts, I measured growth rates of P. damicornis with different symbionts at three temperatures and found that while thermally tolerant symbionts reduced coral growth at cool temperatures, this disadvantage was ameliorated by warming, suggesting that in warmer oceans, these symbionts will benefit reefs by enhancing coral survival at no cost to growth. Finally, a survey of thermally tolerant symbionts in different Pocillopora lineages revealed common associations across host taxa, indicating the widespread relevance of symbiont community variation and dynamics. In summary, this dissertation illustrates that coral performance and stress- tolerance are influenced by both symbiont identity and abundance, which are highly dynamic and change in accordance with principles of community ecology. These findings illustrate the importance of symbiotic dynamism in adaptation and acclimatization in diverse biological systems, while highlighting the major role that Symbiodinium community ecology may play in determining the future of coral reefs.</p

shaylematsuda/Mcap_CD_growth: Symbiont growth trade-offs

&lt;p&gt;Data and scripts for the &quot;Symbiont-mediated tradeoffs between growth and heat tolerance are modulated by light and temperature in the coral &lt;em&gt;Montipora capitata&lt;/em&gt;&quot; manuscript. Shayle Matsuda, Mariah Opalek, Raphael Ritson-Williams, Ruth Gates, Ross Cunning&lt;/p&gt

Symbiont community structure in Orbicella faveolata from Mermaid Reef and Sandy Cay Reef in Abaco, The Bahamas in January 2019

Dataset: Symbiont community structure in Orbicella faveolataThis dataset contains results from genus-specific qPCR assays to quantify the abundance of Symbiodinium, Breviolum, Cladocopium, and Durusdinium symbionts relative to coral cells in Orbicella faveolata from Abaco, The Bahamas in January 2019. Bulk genomic DNA was extracted from tissue scrapings collected by SCUBA divers, and used as a template for qPCR assays. Resulting CT values were used to calculate symbiont to host cell ratios for each symbiont genus within each coral. The publication based on these data can be found here: http://dx.doi.org/10.1007/s00338-020-01948-0. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/855439NSF Division of Ocean Sciences (NSF OCE) OCE-185130

Thermotolerant coral symbionts modulate heat stress‐responsive genes in their hosts

Some corals may become more resistant to bleaching by shuffling their Symbiodiniaceae communities toward thermally tolerant species, and manipulations to boost the abundance of these symbionts in corals may increase resilience in warming oceans. However, the thermotolerant symbiont Durusdinium trenchii may reduce growth and fecundity in Caribbean corals, and these tradeoffs need to be better understood as this symbiont spreads through the region. We sought to understand how D. trenchii modulates coral gene expression by manipulating symbiont communities in Montastraea cavernosa to produce replicate ramets containing D. trenchii together with paired ramets of these same genets (n = 3) containing Cladocopium C3 symbionts. We then examined differences in global gene expression between corals hosting Durusdinium and Cladocopium under control temperatures, and in response to short‐term heat stress. We identified numerous transcriptional differences associated with symbiont identity, which explained 2%–14% of the transcriptional variance. Corals with D. trenchii upregulated genes related to translation, ribosomal structure and biogenesis, and downregulated genes related to extracellular structures, and carbohydrate and lipid transport and metabolism, relative to corals with Cladocopium. Unexpectedly, these changes were similar to those observed in Cladocopium‐dominated corals in response to heat stress, suggesting that thermotolerant D. trenchii may cause corals to increase expression of heat stress‐responsive genes, explaining both the increased heat tolerance and the associated energetic tradeoffs in corals containing D. trenchii. These findings provide insight into the ecological changes occurring on contemporary coral reefs in response to climate change, and the diverse ways in which different symbionts modulate emergent phenotypes of their hosts