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Gates, R. D.

Publications and source records attributed to Gates, R. D..

11 recordsLinked to original sources

Coral environmental history is primary driver of algal symbiont composition, despite a mass bleaching event

Coral reefs are iconic examples of climate change impacts because climate-induced heat stress causes the breakdown of the coral-algal symbiosis leading to a spectacular loss of color, termed coral bleaching. To examine the fine-scale dynamics of this process, we re-sampled 600 individually marked Montipora capitata colonies from across K[a]ne ohe Bay, Hawaii and compared the algal symbiont composition before and after the 2019 bleaching event. The relative proportion of the heat-tolerant symbiont Durusdinium in corals increased in most parts of the bay following the bleaching event. Despite this widespread increase in abundance of Durusdinium, the overall algal symbiont community composition was largely unchanged, and hydrodynamically defined regions of the bay retained their distinct pre-bleaching compositions. Furthermore, depth and temperature variability were the most significant drivers of Symbiodiniaceae community composition by site regardless of bleaching intensity or change in relative proportion of Durusdinium. Our results suggest that the plasticity of symbiont composition in corals may be constrained to adaptively match the long-term environmental conditions surrounding the holobiont, independent of an individual corals stress and bleaching response.

ecology↗

Community composition of coral associated Symbiodiniaceae is driven by fine scale environmental gradients

The survival of reef-building corals is dependent upon a symbiosis between the coral and the community of Symbiodiniaceae. Montipora capitata, one of the main reef building coral species in Hawaii, is known to host a diversity of symbionts, but it remains unclear how they change spatially and whether environmental factors drive those changes. Here, we surveyed the Symbiodiniaceae community in 600 M. capitata colonies from 30 sites across K[a]neohe Bay and tested for host specificity and environmental gradients driving spatial patterns of algal symbiont distribution. We found that the Symbiodiniaceae community differed markedly across sites, with M. capitata in the most open-ocean (northern) site hosting few or none of the genus Durusdinium, whereas individuals at other sites had a mix of Durusdinium and Cladocopium. Our study shows that the algal symbiont community composition responds to fine-scale differences in environmental gradients; depth and temperature variability were the most significant predictor of Symbiodiniaceae community, although environmental factors measured in the study explained only about 20% of observed variation. Identifying and mapping Symbiodiniaceae community distribution at multiple scales is an important step in advancing our understanding of algal symbiont diversity, distribution and evolution, and the potential responses of corals to future environmental change.

ecology↗

Genetic patterns in Montipora capitata across an environmental mosaic in Kaneohe Bay

Spatial genetic structure (SGS) is important to a populations ability to adapt to environmental change. For species that reproduce both sexually and asexually, the relative contribution of each reproductive mode has important ecological and evolutionary implications because asexual reproduction can have a strong effect on SGS. Reef building corals reproduce sexually, but many species also propagate asexually under certain conditions. In order to understand SGS and the relative importance of reproductive mode across environmental gradients, we evaluated genetic relatedness in almost 600 colonies of Montipora capitata across 30 environmentally characterized sites in K[a]neohe Bay, Oahu, Hawaii using low-depth restriction digest associated sequencing. Clonal colonies were relatively rare overall but influenced SGS. Clones were located significantly closer to one another spatially than average colonies and were more frequent on sites where wave energy was relatively high, suggesting a strong role of mechanical breakage in their formation. Excluding clones, we found no evidence of isolation by distance within sites or across the bay. Several environmental characteristics were significant predictors of the underlying genetic variation (including degree heating weeks, time spent above 30{degrees}C, depth, sedimentation rate and wave height); however, they only explained 5% of this genetic variation. Our results show that colony fragmentation contributes to the ecology of M. capitata at local scales and that genetic diversity is maintained despite strong environmental gradients in a highly impacted ecosystem, suggesting potential for broad adaptation or acclimatization in this population.

ecology↗

Intrapopulation adaptive variance supports selective breeding in a reef-building coral

The long-term persistence of coral reefs under climate change requires heritable drivers of thermal tolerance which support adaptation. The genomic basis of thermal tolerance has been evaluated across strong spatial and environmental gradients, but this variation also exists within populations due to neutral evolutionary processes. Small scale heterogeneity in coral bleaching is ubiquitous, so we used corals from a single reef to examine genomic signatures of bleaching performance, their biochemical correlates and the downstream consequences of selective breeding. In the absence of directional selection due to environmental differences, adult corals from a single population exhibit strong genomic patterns related to natural bleaching tolerance and symbiosis state, including functional differentiation in signaling pathways, protein and amino acid modification and metabolism. Conversely, growth, development and innate immune responses did not distinguish bleaching tolerance in adult corals. The genomic signatures of these gene ontologies influence biochemical patterns in healthy corals, primarily via cell-signaling pathway impacts on peptides and amino acids. Thermal tolerance in this population is highly heritable, with significantly higher survivorship under temperature stress in larvae and juveniles reared from thermally tolerant parents than those from sensitive parents. Using a select and re-sequence approach, certain gene ontologies were reproducibly impacted, while antioxidant activity and cell signaling ontologies were disproportionately selected in thermally tolerant corals, demonstrating the genomic drivers of successful selective breeding. These data show that intrapopulation variance in the absence of historical selection supports the adaptive capacity of coral reefs under climate change.

ecology↗

Bleaching resistant corals retain heat tolerance following acclimatization to environmentally distinct reefs

Urgent action is needed to prevent the demise of coral reefs as the climate crisis leads to an increasingly warmer and more acidic ocean. Propagating climate change resistant corals to restore degraded reefs is one promising strategy; however, empirical evidence is needed to determine if resistance is retained following transplantation within or beyond a corals natal reef. Here we assessed the performance of bleaching-resistant individuals of two coral species following reciprocal transplantation between environmentally distinct reefs (low vs high diel variability) to determine if stress resistance is retained following transplantation. Critically, transplantation to either environment had no influence on coral bleaching resistance, indicating that this trait was relatively fixed and is thus a useful metric for selecting corals for reef restoration within their native range. In contrast, growth was highly plastic, and native performance was not predictive of performance in the novel environment. Coral metabolism was also plastic, with cross transplants of both species matching the performance of native corals at both reefs within three months. Coral physiology (autotrophy, heterotrophy, and metabolism) and overall fitness (survival, growth, and reproduction) were higher at the reef with higher flow and fluctuations in diel pH and dissolved oxygen, and did not differ between native corals and cross-transplants. Conversely, cross-transplants at the low-variability reef had higher fitness than native corals, thus increasing overall fitness of the recipient population. This experiment was conducted during a non-bleaching year, which suggests that introduction of these bleaching-resistant individuals will provide even greater fitness benefits to recipient populations during bleaching years. In summary, this study demonstrates that propagating and transplanting bleaching-resistant corals can elevate the resistance of coral populations to ocean warming while simultaneously maintaining reef function as the climate crisis worsens.

ecology↗

Shifting Baselines: Repeat bleaching drives coral physiotypes through environmental legacy and cellular memory

O_LIGlobal climate change is altering coral reef ecosystems. Notably, marine heat waves are producing widespread coral bleaching events that are increasing in frequency, with projections for annual bleaching events on reefs worldwide by mid-century. C_LIO_LIThe response of corals to elevated seawater temperatures can be modulated by abiotic factors at site of origin and dominant endosymbiont type, which can result in a shift in multiple coral traits and drive physiological legacy effects that influence the trajectory of reef corals under subsequent thermal stress events. It is critical, therefore, to evaluate the potential for shifting physiological and cellular baselines driven by these factors in in situ bleaching (and recovery) events. Here, we use the back-to-back regional bleaching events of 2014 and 2015 in the Hawaiian Islands and subsequent recovery periods to test the hypothesis that coral multivariate trait space (here termed physiotype, sensu (Van Straalen, 2003) shift in multiple bleaching events, modulated by both environmental histories and symbiotic partnerships (Symbiodiniaceae). C_LIO_LIDespite fewer degree heating weeks in the first-bleaching event relative to the second (7 vs. 10), bleaching severity in a dominant reef building coral on Hawaiian reefs, Montipora capitata, was greater (~70% vs. 50% bleached cover) and differences due to environmental history (reef site) were more pronounced. Melanin, an immune cytotoxic response, provided an initial defense during the first event, potentially priming antioxidant activity, which peaked in the second-bleaching event (i.e., a legacy effect). While magnitude of bleaching differed, immune response patterns were shared among corals harboring heat-sensitive and heat-tolerant Symbiodiniaceae. This supports a pattern of increased constitutive immunity in corals resulting from repeat bleaching events, with greater specialized enzymes (catalase, peroxidase, superoxide dismutase) and attenuated melanin synthesis. C_LIO_LIThis study demonstrates bleaching events have implications for reef corals beyond shaping their ecological assemblages. These events can change the magnitude and/or identity of response variables contributing to physiotype, thus generating physiological legacies carried over into the future. Quantifying baseline coral physiotypes and tracking their shifts will be critical to understanding and forecasting the effects of increased bleaching frequency on coral biology and ecology in the Anthropocene. C_LI

ecology↗

Coral bleaching susceptibility is predictive of subsequent mortality within but not between coral species

Marine heat waves instigated by anthropogenic climate change are causing increasingly frequent and severe coral bleaching events that often lead to widespread coral mortality. While community-wide increases in coral mortality following bleaching events have been documented on reefs around the world, the ecological consequences for conspecific individual colonies exhibiting contrasting phenotypes during thermal stress (e.g. bleached vs. not bleached) are not well understood. Here we describe the ecological outcomes of colonies of the two dominant reef-building coral species in K[a]ne{square}ohe Bay, Hawai{square}i, Montipora capitata and Porites compressa, that exhibited either a bleaching susceptible phenotype (bleached) or resistant phenotype (non-bleached) following the second of two consecutive coral bleaching events in Hawai{square}i in 2015. Conspecific pairs of adjacent bleaching susceptible vs. resistant corals were tagged on patch reefs in two regions of K[a]ne{square}ohe Bay with different seawater residence times and terrestrial influence. The ecological consequences (symbiont recovery and mortality) were monitored for two years following the peak of the bleaching event. Bleaching susceptible corals suffered higher partial mortality than bleaching resistant corals of the same species in the first 6 months following thermal stress. Surprisingly, P. compressa had greater resilience following bleaching (faster pigment recovery and lower post-bleaching mortality) than M. capitata, despite having less resistance to bleaching (higher bleaching prevalence and severity). These differences indicate that bleaching susceptibility of a species is not always a good predictor of mortality following a bleaching event. By tracking the fate of individual colonies of resistant and susceptible phenotypes, contrasting ecological consequences of thermal stress were revealed that were undetectable at the population level. Furthermore, this approach revealed individuals that underwent particularly rapid recovery from mortality, including some colonies over a meter in diameter that recovered all live tissue cover from >60% partial mortality within just one year. These coral pairs continue to be maintained and monitored in the field, serving as a "living library" for future investigations on the ecology and physiology of coral bleaching.

ecology↗

Spatial variation in the biochemical and isotopic composition of corals during bleaching and recovery

Ocean warming and the increased prevalence of coral bleaching events threaten coral reefs. However, the biology of corals during and following bleaching events under field conditions is poorly understood. We examined bleaching and post-bleaching recovery in Montipora capitata and Porites compressa corals that either bleached or did not bleach during a 2014 bleaching event at three reef locations in K[a]ne ohe Bay, O ahu. We measured changes in chlorophylls, biomass, and nutritional plasticity using stable isotopes ({delta}13C, {delta}15N). Coral traits showed significant variation among bleaching conditions, reef sites, time periods, and their interactions. Bleached colonies of both species had lower chlorophyll and total biomass. While M. capitata chlorophyll and biomass recovered three months later, P. compressa chlorophyll recovery was location-dependent and total biomass of previously bleached colonies remained low. Biomass energy reserves were not affected by bleaching, instead M. capitata proteins and P. compressa biomass energy declined over time, and P. compressa lipid biomass was site-specific. Stable isotope analyses of host and symbiont tissues did not indicate increased heterotrophic nutrition in bleached colonies of either species, during or after thermal stress. Instead, mass balance calculations revealed variance in {delta}13C values was best explained by augmented biomass composition, whereas {delta}15N values reflected spatial and temporal variability in nitrogen sources in addition to bleaching effects on symbiont nitrogen demand. These results emphasize total biomass quantity may change substantially during bleaching and recovery. Consequently, there is a need to consider the influence of biomass composition in the interpretation of isotopic values in corals.

physiology↗

High-frequency temperature variability mirrors fixed differences in thermal limits of the massive coral Porites lobata (Dana, 1846)

Spatial heterogeneity in environmental characteristics can drive adaptive differentiation when contrasting environments exert divergent selection pressures. This environmental and genetic heterogeneity can substantially influence population and community resilience to disturbance events. Here, we investigated corals from the highly variable back reef habitats of Ofu Island in American Samoa that thrive in thermal conditions known to elicit widespread bleaching and mortality elsewhere. To investigate the hypothesis that thermal variability is the driving force shaping previously observed differences in coral tolerance limits in Ofu, specimens of the common Indo-Pacific coral Porites lobata (Dana, 1846) from locations with differing levels of thermal variability were acclimated to low and high thermal variation in controlled common garden experimental aquaria. Overall, there was minimal effect of the acclimation exposure. Corals native to the site with the highest level of daily variability grew fastest, regardless of acclimation treatment. When exposed to lethal thermal stress, corals native to both variable sites contained elevated levels of heat shock proteins and maintained photosynthetic performance for 1-2 days longer than corals from the stable environment. Despite being separated by < 5 km, there was significant genetic differentiation among coral colonies (FST = 0.206, p < 0.0001; nuclear ribosomal DNA), while Symbiodinium phylotypes were all ITS2-type C15. Our study demonstrates consistent signatures of adaptation in growth and stress resistance in corals from naturally thermally variable habitats, emphasizing that existing genetic diversity of corals is an important asset in strategies to protect and manage coral reef ecosystems in the face of global change.\n\nSummary StatementCorals native to highly variable habitats demonstrate greater thermal tolerance than corals from less variable habitats after 36-days of acclimation to thermally stable or variable common garden treatments.

evolutionary biology↗

Nurtured by nature: Considering the role of environmental and parental legacies in coral ecological performance

The persistence of reef building corals is threatened by human-induced environmental change. Maintaining coral reefs into the future requires not only the survival of adults, but also the influx of recruits to promote genetic diversity and retain cover following adult mortality. Few studies examine the linkages among multiple life stages of corals, despite a growing knowledge of carryover effects in other systems. We provide a novel test of coral parental preconditioning to ocean acidification (OA) to better understand impacts on the processes of offspring recruitment and growth. Coral planulation was tracked for three months following adult exposure to high pCO2 and offspring from the second month were reciprocally exposed to ambient and high pCO2. Offspring of parents exposed to high pCO2 had greater settlement and survivorship immediately following release, retained survivorship benefits during one and six months of continued exposure, and further displayed growth benefits to at least one month post release. Enhanced performance of offspring from parents exposed to high conditions was maintained despite the survivorship in both treatments declining in continued exposure to OA. Preconditioning of the adults while they brood their larvae may provide a form of hormetic conditioning, or environmental priming that elicits stimulatory effects. Defining mechanisms of positive carryover effects, or positive trans-generational plasticity, is critical to better understanding ecological and evolutionary dynamics of corals under regimes of increasing environmental disturbance. Considering parental and environmental legacies in ecological and evolutionary projections may better account for coral reef response to the chronic stress regimes characteristic of climate change.

physiology↗

A Dynamic Bioenergetic Model For Coral-Symbiodinium Symbioses And Coral Bleaching As An Alternate Stable State

Coral reef ecosystems owe their ecological success-and vulnerability to climate change-to the symbiotic metabolism of corals and Symbiodinium spp. The urgency to understand and predict the stability and breakdown of these symbioses (i.e., coral bleaching) demands the development and application of theoretical tools. Here, we develop a dynamic bioenergetic model of coral-Symbiodinium symbioses that demonstrates realistic steady-state patterns in coral growth and symbiont abundance across gradients of light, nutrients, and feeding. Furthermore, by including a mechanistic treatment of photo-oxidative stress, the model displays dynamics of bleaching and recovery that can be explained as transitions between alternate stable states. These dynamics reveal that healthy and bleached states correspond broadly to nitrogen- and carbon-limitation in the system, with transitions between them occurring as integrated responses to multiple environmental factors. Indeed, a suite of complex emergent behaviors reproduced by the model (e.g., bleaching is exacerbated by nutrients and attenuated by feeding) suggests it captures many important attributes of the system; meanwhile, its modular framework and open source R code are designed to facilitate further problem-specific development. We see significant potential for this modeling framework to generate testable hypotheses and predict integrated, mechanistic responses of corals to environmental change, with important implications for understanding the performance and maintenance of symbiotic systems.

systems biology↗