1. Chen, C.-C., H.-Y. Hsieh, A.B. Mayfield, C.-M. Chang, J.-T. Wang, and P.-J. Meng. The key impact on water quality of coral reefs in Kenting National Park. Journal of Marine Science and Engineering, 10(2):270, https://doi.org/10.3390/jmse10020270 2022

    Abstract:

    Southern Taiwan’s Kenting National Park is a popular retreating place for many domestic and international tourists, with increasing tourist numbers potentially over-burdening the coastal ecosystems. To better understand human impacts, a long-term ecological research program was initiated in 2001 to track water quality at 14 coral reef-abutting sites throughout the park since then. Extracting the data from this 20-year survey, we found that increasing in the nutrient levels during the summer rainy season, together with the drops in salinity led by freshwater inputs (land- and rainfall-derived), was the main impact to coral reef ecosystem of Kenting. Cluster analysis further confirmed the nutrient influx was mainly attributed to the local discharge outlets with dense of villages and hotels at upstream. Therefore, more efforts are needed to input to control tourist number, treat waste water discharge and strengthen land protection facilities.

  2. DeMerlis, A., A. Kirkland, M.L. Kaufman, A.B. Mayfield, N. Formel, G. Kolodziej, D.P. Manzello, D. Lirman, N. Traylor-Knowles, and I.C. Enochs. Pre-exposure to a variable temperature treatment improves the response of Acropora cervicornis to acute thermal stress. Coral Reefs, 41(2):435-445, https://doi.org/10.1007/s00338-022-02232-z 2022

    Abstract:

    Given that global warming is the greatest threat to coral reefs, coral restoration projects have expanded worldwide with the goal of replenishing habitats whose reef-building corals succumbed to various stressors. In many cases, however, these efforts will be futile if outplanted corals are unable to withstand warmer oceans and an increased frequency of extreme temperature events. Stress-hardening is one approach proposed to increase the thermal tolerance of coral genotypes currently grown for restoration. Previous studies have shown that corals from environments with natural temperature variability experience less bleaching when exposed to thermal stress, though it remains unclear if this localized acclimatization or adaptation to variable temperatures can be operationalized for enhancing restoration efforts. To evaluate this approach, fragments from six source colonies of nursery-raised Caribbean staghorn coral (Acropora cervicornis) were treated with a variable temperature regime (oscillating twice per day from 28 to 31°C) or static temperatures (28°C) in the laboratory for 89 d. Following this, fragments were subjected to a heat-stress assay (32°C) for 2 weeks. Corals treated with variable temperatures manifested signs of severe thermal stress later than static temperature laboratory controls as well as untreated field controls collected from the nursery. Furthermore, there was a stark contrast in the physiological response to heat stress, whereby the laboratory and field control groups had a significantly higher incidence of rapid tissue sloughing and necrosis, while the variable temperature-treated corals succumbed to bleaching more gradually. Overall, our data show that pre-acclimation to a variable temperature regime improves acroporid thermotolerance. As corals continue to be outplanted back onto Florida’s changing reef scape, understanding the molecular mechanisms underlying this enhanced thermal tolerance and its endurance in situ will be critical for future research and restoration applications.

  3. Martinez-Castillo, V., A.P. Rodriguez-Troncoso, A.B. Mayfield, F.A. Rodriguez-Zaragoza, and A.L. Cupul-Magana. Coral recovery in the central Mexican Pacific 20 years after the 1997-1998 El Niño event. Oceans, 3(1):48-59, https://doi.org/10.3390/oceans3010005 2022

    Abstract:

    El Niño–Southern Oscillation (ENSO) events are increasing globally in both frequency and strength, and they can elicit coral bleaching events. The 1997–1998 ENSO caused mass coral mortality with a 96% decline in live coral cover along the Central Mexican Pacific. However, in recent years, these sites have shown signs of recovery. We used data collected in 1997 and 2015–2017 to evaluate the coral recovery in this region and coral cover levels have now reached 50% of their pre-1997–1998 El Niño values. Furthermore, a strong 2015–2016 ENSO event did not significantly affect the live coral cover, potentially demonstrating that the local corals have acclimatized or even adapted to higher temperatures. Even though branching species remain the most abundant morphotype, a PERMANOVA revealed significant changes in the coral assemblage. Collectively, this dataset is testament to the fact that corals within this region are capable of resisting or at least partially recovering from thermal anomalies caused by ENSO events.

  4. Mayfield, A.B. Machine-learning-based proteomic predictive modeling with thermally-challenged Caribbean reef corals. Diversity, 14(1):33, https://doi.org/10.3390/d14010033 2022

    Abstract:

    Coral health is currently diagnosed retroactively; colonies are deemed “stressed” upon succumbing to bleaching or disease. Ideally, health inferences would instead be made on a pre-death timescale that would enable, for instance, environmental mitigation that could promote coral resilience. To this end, diverse Caribbean coral (Orbicella faveolata) genotypes of varying resilience to high temperatures along the Florida Reef Tract were exposed herein to elevated temperatures in the laboratory, and a proteomic analysis was taken with a subset of 20 samples via iTRAQ labeling followed by nano-liquid chromatography + mass spectrometry; 46 host coral and 40 Symbiodiniaceae dinoflagellate proteins passed all stringent quality control criteria, and the partial proteomes of biopsies of (1) healthy controls, (2) sub-lethally stressed samples, and (3) actively bleaching corals differed significantly from one another. The proteomic data were then used to train predictive models of coral colony bleaching susceptibility, and both generalized regression and machine-learning-based neural networks were capable of accurately forecasting the bleaching susceptibility of coral samples based on their protein signatures. Successful future testing of the predictive power of these models in situ could establish the capacity to proactively monitor coral health. 

  5. Mayfield, A.B., and A.C. Dempsey. Environmentally-driven variation in the physiology of a New Caledonian reef coral. Oceans, 3(1):15-29, https://doi.org/10.3390/oceans3010002 2022

    Abstract:

    Given the widespread threats to coral reefs, scientists have lost the opportunity to understand the basic biology of “pristine” corals whose physiologies have not been markedly perturbed by human activity. For instance, high temperature-induced bleaching has been occurring annually since 2014 in New Caledonia. Because most corals cannot withstand repeated years when bleaching occurs, an analysis was undertaken to showcase coral behavior in a period just before the onset of “annual severe bleaching” (ASB; November 2013) such that future generations might know how these corals functioned in their last bleaching-free year. Pocillopora damicornis colonies were sampled across a variety of environmental gradients, and a subset was sampled during both day and night to understand how their molecular biology changes upon cessation of dinoflagellate photosynthesis. Of the 13 environmental parameters tested, sampling time (i.e., light) most significantly affected coral molecular physiology, and expression levels of a number of both host and Symbiodiniaceae genes demonstrated significant diel variation; endosymbiont mRNA expression was more temporally variable than that of their anthozoan hosts. Furthermore, expression of all stress-targeted genes in both eukaryotic compartments of the holobiont was high, even in isolated, uninhabited, federally protected atolls of the country’s far northwest. Whether this degree of sub-cellular stress reflects cumulative climate change impacts or, instead, a stress-hardened phenotype, will be unveiled through assessing the fates of these corals in the wake of increasingly frequent marine heatwaves. 

  6. Grottoli, A.G., R.J. Toonen, R. van Woesik, R. Vega Thurber, M.E. Warner, R.H. McLachlan, J.T. Price, K.D. Bahr, I.B. Baums, K.D. Castillo, M.A. Coffroth, R. Cunning, K. Dobson, M.J. Donahue, J.L. Hench, R. Iglesias-Prieto, D.W. Kemp, C.D. Kenkel, D.I. Kline, I.B. Kuffner, J.L. Matthews, A.B. Mayfield, J.L. Padilla-Gamiño, S. Palumbi, C.R. Voolstra, V.M. Weis, and H.C. Wu. Increasing comparability among coral bleaching experiments. Ecological Applications, 31(4):e02262, https://doi.org/10.1002/eap.2262 2021

    Abstract:

    Coral bleaching is the single largest global threat to coral reefs worldwide. Integrating the diverse body of work on coral bleaching is critical to understanding and combating this global problem. Yet investigating the drivers, patterns, and processes of coral bleaching poses a major challenge. A recent review of published experiments revealed a wide range of experimental variables used across studies. Such a wide range of approaches enhances discovery, but without full transparency in the experimental and analytical methods used, can also make comparisons among studies challenging. To increase comparability but not stifle innovation, we propose a common framework for coral bleaching experiments that includes consideration of coral provenance, experimental conditions, and husbandry. For example, reporting the number of genets used, collection site conditions, the experimental temperature offset(s) from the maximum monthly mean (MMM) of the collection site, experimental light conditions, flow, and the feeding regime will greatly facilitate comparability across studies. Similarly, quantifying common response variables of endosymbiont (Symbiodiniaceae) and holobiont phenotypes (i.e., color, chlorophyll, endosymbiont cell density, mortality, and skeletal growth) could further facilitate cross‐study comparisons. While no single bleaching experiment can provide the data necessary to determine global coral responses of all corals to current and future ocean warming, linking studies through a common framework as outlined here, would help increase comparability among experiments, facilitate synthetic insights into the causes and underlying mechanisms of coral bleaching, and reveal unique bleaching responses among genets, species, and regions. Such a collaborative framework that fosters transparency in methods used would strengthen comparisons among studies that can help inform coral reef management and facilitate conservation strategies to mitigate coral bleaching worldwide.

  7. Knowlton, N., A.G. Grottoli, J. Kleypas, D. Obura, E. Corcoran, J. de Goeij, T. Felis, S. Harding, A.B. Mayfield, M. Miller, K. Osuka, R. Peixoto, C.J. Randall, C.R. Voolstra, S. Wells, C. Wild, and S. Ferse. Rebuilding coral reefs: A decadal grand challenge. International Coral Reef Society and Future Earth Coasts, 49 pp., https://doi.org/10.53642/NRKY9386 2021

    Abstract:

    This document is the work of a team assembled by the International Coral Reef Society (ICRS), whose mission is to promote the acquisition and dissemination of scientific knowledge to secure the future of coral reefs, including via relevant policy frameworks and decision-making processes. This document seeks to highlight the urgency of taking action to conserve and restore reefs through protection and management measures, to provide a summary of the most relevant and recent natural and social science that provides guidance on these tasks, and to highlight implications of these findings for the numerous discussions and negotiations taking place at the global level.

  8. Mayfield, A.B., A.C. Dempsey, and C.-S. Chen. Assessing coral health in the Kingdom of Tonga with a coral health index. Platax, 18:53-78, https://doi.org/10.29926/platax.202112_18.0007 2021

    Abstract:

    Reef coral health is currently diagnosed retroactively; once corals bleach or become diseased, we assume they had been experiencing high stress levels. This would be akin to telling one who suffered a cardiac arrest that he/she had high blood pressure; ideally, an individual’s susceptibility to a heart attack would be known in advance of such a late-stage, life-threatening event. However, sub-lethal means of assessing coral health do not yet exist, and the preferred health metric, growth, cannot be reliably measured while on research cruises, where most, if not all, reef sites are surveyed and sampled only once. Since it would be preferable to make diagnostic inferences from a single biopsy, a new parameter known as the “coral health index” (CHI; 氣) was devised herein. The CHI, which represents an amalgamation of several response variables known to scale directly with coral resilience (e.g., dinoflagellate endosymbiont density), was profiled across multiple environmental gradients in the Kingdom of Tonga. Machine learning (i.e., AI) models were developed such that the CHI could be predicted from more commonly assessed environmental (e.g., salinity) and ecological (e.g., coral cover) benchmarks. Models for two pocilloporid coral species were characterized by validation R2 values approaching 1, meaning that this AI could be used to delineate relative levels of coral resilience on a pre-bleaching timescale.

  9. Mayfield, A.B., C. Aguilar, G. Kolodziej, I.C. Enochs, and D.P. Manzello. Shotgun proteomic analysis of thermally challenged reef corals. Frontiers in Marine Science, 8:660153, https://doi.org/10.3389/fmars.2021.660153 2021

    Abstract:

    Although coral reef ecosystems across the globe are in decline due to climate change and other anthropogenic stressors, certain inshore reefs of the Upper Florida Keys reef tract have persisted, with some even thriving, under marginalized conditions. To better understand the molecular basis of the thermotolerance displayed by these corals, a laboratory-based temperature challenge experiment that also featured conspecifics from a more stress-susceptible offshore reef was conducted with the common Caribbean reef-builder Orbicella faveolata, and the proteomes of both the coral hosts and their endosymbiotic dinoflagellate communities were profiled in (1) controls, (2) corals that succumbed to high-temperature stress and bleached, and (3) those that instead acclimated to high temperatures ex situ. Proteomic signatures varied most significantly across temperatures, host genotypes, and Symbiodiniaceae assemblages, and the two eukaryotic compartments of this mutualism exhibited distinct proteomic responses to high temperatures. Both partners maintained high levels of molecular chaperones and other canonical (eukaryotic) stress response (CSR) proteins in all treatments (including controls). Instead, proteins involved in lipid trafficking, metabolism, and photosynthesis played greater roles in the holobionts’ high-temperature responses, and these energy mobilization processes may have sustained the elevated protein turnover rates associated with the constitutively active CSR.

  10. McRae, C.J., A.B. Mayfield, W.B. Huang, I.M. Côte, and T.Y. Fan. Contrasting proteomic responses of adult and larval coral to high temperatures. Frontiers in Marine Science, 8:716124, https://doi.org/10.3389/fmars.2021.716124 2021

    Abstract:

    Climate change-induced increases in seawater temperature continue to impact coral reef ecosystems globally. There is a consequent need to characterize the responses of corals to thermal stress to understand the molecular processes underpinning these responses and identify hallmarks of resilience. Here we used an iTRAQ approach to compare the proteomes of adult corals (Pocillopora acuta) that had been thermally conditioned at a control (26°C) or elevated temperature (29.5°C) for three reproductive cycles, as well as the larvae released by these corals. We found that larvae responded more to high-temperature exposure at the protein level than their parents and that different proteins were affected between life stages; a single protein was up-regulated at high temperatures in both adults and their offspring, and its identity is currently unknown. Similarly, different cellular pathways were affected by high-temperature exposure between the coral hosts and their dinoflagellate endosymbionts; proteins involved in translation and protein trafficking were most likely to be affected by high-temperature exposure in the former, with photosynthesis being the most thermo-sensitive process in the latter. Collectively, these findings highlight the importance of considering both life stage and the composition of the coral holobiont when using molecular-scale data to model cellular processes associated with responses to future ocean warming.

  11. Rubin, E.T., I.C. Enochs, C. Foord, A.B. Mayfield, G. Kolodziej I. Basden, and D.P. Manzello. Molecular mechanisms of coral persistence within highly urbanized locations in the Port of Miami, Florida. Frontiers in Marine Science, 8:695236, https://doi.org/10.3389/fmars.2021.695236 2021

    Abstract:

    Healthy coral communities can be found on artificial structures (concrete walls and riprap) within the Port of Miami (PoM), Florida. These communities feature an unusually high abundance of brain corals, which have almost entirely vanished from nearby offshore reefs. These corals appear to be thriving in very low-quality waters influenced by dense ship and boat traffic, dredging, and numerous residential and industrial developments. The PoM basin is part of Biscayne Bay, an estuarine environment that experiences frequent freshwater input, high nutrient loading, hypoxia, and acidification. To investigate if there is a molecular basis behind the ability of these corals to persist within these highly “urbanized” waters, we compared whole transcriptome expression profiles from 25 PoM Pseudodiploria strigose colonies against six conspecifics from a nearby offshore reef. We found that the urban corals exhibited higher expression of (1) transcripts encoding pattern-recognition receptors which may allow these corals to better sense and detect food particles and pathogenic invaders, (2) digestive and degradation-associated enzymes, which may suggest an elevated capacity for heterotrophy and pathogen digestion, and (3) transcripts related to innate immunity, defense, and cellular detoxification, which may collectively protect against pathogenic organisms and water pollution impacts. Large ribosomal subunit rRNA gene mapping revealed that P. strigose colonies from the PoM sites predominantly hosted heat-tolerant endosymbionts from the genus Durusdinium, while offshore conspecifics’ communities were dominated by symbionts in the genus Breviolum. These findings reveal transcriptomic plasticity and molecular mechanisms contributing to the persistence of these corals within a highly urbanized habitat.

  12. Tew, K.S., J. Kuo, J.O. Cheng, F.C. Ko, P.J. Meng, A.B. Mayfield, and P.J. Liu. Impacts of seagrass on benthic microalgae and phytoplankton communities in a coral reef ecosystem under experimental warming—A mesocosm study. Frontiers in Marine Science, 8:679683, https://doi.org/10.3389/fmars.2021.679683 2021

    Abstract:

    The effects of seagrass on microalgal assemblages under experimentally elevated temperatures (28°C) and CO2 partial pressures (pCO2; 800 μatm) were examined using coral reef mesocosms. Concentrations of nitrate, ammonium, and benthic microalgal chlorophyll a (chl-a) were significantly higher in seagrass mesocosms, whereas phytoplankton chl-a concentrations were similar between seagrass and seagrass-free control mesocosms. In the seagrass group, fewer parasitic dinoflagellate OTUs (e.g., Syndiniales) were found in the benthic microalgal community though more symbiotic dinoflagellates (e.g., Cladocopium spp.) were quantified in the phytoplankton community. Our results suggest that, under ocean acidification conditions, the presence of seagrass nearby coral reefs may (1) enhance benthic primary productivity, (2) decrease parasitic dinoflagellate abundance, and (3) possibly increase the presence of symbiotic dinoflagellates.

  13. Chang, T.-C., A.B. Mayfield, and T.-Y. Fan. Culture systems influence the physiological performance of the soft coral Sarcophyton glaucum. Scientific Reports, 20:20200, https://doi.org/10.1038/s41598-020-77071-5 2020

    Abstract:

    There is an urgent need to develop means of ex situ biobanking and biopreserving corals and other marine organisms whose habitats have been compromised by climate change and other anthropogenic stressors. To optimize laboratory growth of soft corals in a way that could also benefit industry (e.g., aquarium trade), three culture systems were tested herein with Sarcophyton glaucum: (1) a recirculating aquaculture system (RAS) without exogenous biological input (RAS−B), (2) a RAS with “live” rocks and an exogenous food supply (RAS+B), and (3) a simple flow-through system (FTS) featuring partially filtered natural seawater. In each system, the effects of two levels of photosynthetically active radiation (100 or 200 μmol quanta m−2 s−1) and flow velocity (5 or 15 cm s−1) were assessed, and a number of soft coral response variables were measured. All cultured corals survived the multi-month incubation, yet those of the RAS−B grew slowly and even paled; however, once they were fed (RAS−B modified to RAS+B), their pigmentation increased, and their oral discs readily expanded. Light had a more pronounced effect in the RAS−B system, while flow affected certain coral response variables in the FTS tanks; there were few effects of light or flow in the RAS+B system, potentially highlighting the importance of heterotrophy. Unlike the ceramic pedestals of the FTS, those of the RAS+B did not regularly become biofouled by algae. In concert with the aforementioned physiological findings, we therefore recommend RAS+B systems as a superior means of biopreservating and biobanking soft corals.

  14. Cruz-García, R., A.P. Rodríguez-Troncoso, F.A. Rodríguez-Zaragoza, A. Mayfield, and A.L. Cupul-Magaña. Ephemeral effects of El Niño Southern Oscillation events on an eastern tropical Pacific coral community. Marine and Freshwater Research, 71(10):1259-1268, https://doi.org/10.1071/MF18481 2020

    Abstract:

    Coral-reef ecosystems of the central Mexican Pacific have been routinely affected by both moderate and severe El Niño Southern Oscillation (ENSO) events over the past 20 years. Such conditions are associated with abnormally high (1997–1998, 2002–2003, 2009–2010, and 2015–2016; "El Niño") and low (1999–2000, 2008–2009, and 2010–2011; ‘La Niña’) seawater temperatures. Because few studies have documented how ENSO events affect both corals and key coral competitors such as macroalgae, we evaluated the short- and long-term changes in the cover of three reef coral genera, namely, Pocillopora, Pavona and Porites, as well as four coral competitors, namely, macroalgae, turf algae, coralline algae (CCA) and sponges, over a multi-year period that encapsulated two strong ENSO events: the 2010–2011 La Niña and the 2015–2016 El Niño. Such temperature anomalies caused a short-lived decrease in coral cover, alongside a concomitant increase in CCA. The communities eventually returned to their coral-dominated states within several months of the ENSO events, suggesting that these reef habitats can recover from such episodes of anomalous seawater temperatures.

  15. Enochs, I.C., N. Formel, D. Manzello, J. Morris, A.B. Mayfield, A. Boyd, G. Kolodziej, G. Adams, and J. Hendee. Coral persistence despite extreme periodic pH fluctuations at a volcanically acidified Caribbean reef. Coral Reefs, 39(3):523-528, https://doi.org/10.1007/s00338-020-01927-5 2020

    Abstract:

    Naturally acidified environments, such as those caused by volcanic CO2 venting, reveal how complex coral reef ecosystems may respond to future ocean acidification conditions. Few of these sites have been described worldwide, and only a single such site is known from the Caribbean. Herein, we have characterized an area of volcanic acidification at Mayreau Island, St. Vincent and the Grenadines. Despite localized CO2 enrichment and gas venting, the surrounding area has high hard and soft coral cover, as well as extensive carbonate frameworks. Twice daily extremes in acidification, in some cases leading to undersaturation of aragonite, are correlated with tidal fluctuations and are likely related to water flow. Corals persisting despite this periodic acidification can provide insights into mechanisms of resilience and the importance of natural pH variability on coral reefs.

  16. Huang, Y.L., A.B. Mayfield, and T.Y. Fan. Effects of feeding on the physiological performance of the stony coral Pocillopora acuta. Scientific Reports, 10:19988, https://doi.org/10.1038/s41598-020-76451-1 2020

    Abstract:

    Reef-building corals rely on both heterotrophy and endosymbiotic dinoflagellate autotrophy to meet their metabolic needs. Those looking to culture these organisms for scientific or industrial purposes must therefore consider both feeding regimes and the light environment. Herein the effects of three photosynthetically active radiation (PAR) levels were assessed in fed and unfed specimens of the model coral Pocillopora acuta that were cultured in a recirculating aquaculture system (RAS). Half of the corals were fed Artemia sp. brine shrimp in a separate feeding tank to prevent biofouling, and fragments were exposed to PAR levels of 105, 157, or 250 μmol quanta m−2 s−1 over a 12-h period each day. All cultured corals survived the 140-day treatment, and the physiological response variables assessed-buoyant weight, specific growth rate, linear extension, color, and Fv/Fm-were significantly influenced by feeding, and, to a lesser extent, light. Specifically, fed corals grew faster and larger, and presented darker pigmentation; corals fed at the highest light levels grew at the fastest rate (6 cm year−1 or 175 mg g−1 week−1). Given the high physiological performance observed, we advocate the active feeding of brine shrimp in RAS by those looking to cultivate P. acuta, and likely other corals, over long-term timescales.

  17. Mayfield, A.B. Exploiting the power of multivariate statistics for probing the cellular biology of environmentally challenged coral reefs. Platax, 17:27-52, https://doi.org/10.29926/platax.202012_17.0003 2020

    Abstract:

    The coral reef research field has grown markedly in terms of both human power and technological capacity in recent years, a fortuitous occurrence given the rapidly diminishing nature of Earth’s reefs on account of climate change and other anthropogenic stressors. Unfortunately, most coral biologists lack the statistical background to realize the full analytical potential of “big” datasets emerging from (non-exhaustively) 1) expanding reef survey efforts, 2) satellite and in-water (e.g., photomosaic) coral reef imaging projects, and 3) “next-generation” molecular approaches (i.e., ‘OMICs); statistical training has not advanced commensurately with dataset size, a significant short-coming when considering the utility of these data in informing coral reef ecosystem management and conservation. One notably pervasive issue in ‘OMICs research in particular is the general omission of multivariate statistical approaches (MSA), which universally outperform the more commonly employed, less statistically conservative univariate alternatives when attempting to A) model experimental results and B) make predictions about reef coral health and fate. Herein I have attempted to make a case for coral biologists to strongly re-evaluate the merit of MSA, as well as explain why relying on univariate approaches alone may actually lead to spurious findings that do not advance our knowledge of corals and coral reefs.

  18. Mayfield, A.B. Feed your corals. Reef Encounter, 35(1):20-23, 2020

    Abstract:

    No abstract.

  19. Mayfield, A.B. Proteomic signature of corals from thermodynamic reefs. Microorganisms, 8(8):1171, https://doi.org/10.3390/microorganisms8081171 2020

    Abstract:

    Unlike most parts of the world, coral reefs of Taiwan’s deep south have generally been spared from climate change-induced degradation. This has been linked to the oceanographically unique nature of Nanwan Bay, where intense upwelling occurs. Specifically, large-amplitude internal waves cause shifts in temperature of 6–9°C over the course of several hours, and the resident corals not only thrive under such conditions, but they have also been shown to withstand multi-month laboratory incubations at experimentally elevated temperatures. To gain insight into the sub-cellular basis of acclimation to upwelling, proteins isolated from reef corals (Seriatopora hystrix) featured in laboratory-based reciprocal transplant studies in which corals from upwelling and non-upwelling control reefs (<20 km away) were exposed to stable or variable temperature regimes were analyzed via label-based proteomics (iTRAQ). Corals exposed to their “native” temperature conditions for seven days (1) demonstrated highest growth rates and (2) were most distinct from one another with respect to their protein signatures. The latter observation was driven by the fact that two Symbiodiniaceae lipid trafficking proteins, sec1a and sec34, were marginally up-regulated in corals exposed to their native temperature conditions. Alongside the marked degree of proteomic “site fidelity” documented, this dataset sheds light on the molecular mechanisms underlying acclimatization to thermodynamically extreme conditions in situ.

  20. Mayfield, A.B., and C.S. Chen. A coral transcriptome in the Anthropocene as an “alternative stable state.” Platax, 17:1 26, https://doi.org/10.29926/platax.202012_17.0002 2020

    Abstract:

    In contrast to many coral reefs across the globe, those of Taiwan’s deep south had, until the summer of 2020, not generally been greatly affected by climate change-driven seawater temperature rise. This has been attributed to the effects of cold-water upwelling, which naturally cools reefs within Nanwan Bay during the warmest times of the year; episodic upwelling has also thermally “hardened” the resident corals, and prior works sought to uncover the molecular basis of such thermotolerance in colonies of the model coral Pocillopora acuta collected from Nanwan Bay by exposing fragments to sustained high temperatures (30°C) in laboratory mesocosms for nine months. Although all corals ultimately acclimated to this hypothetically stress-inducing temperature ex situ, the dinoflagellate endosymbionts residing within the host corals’ gastrodermal cells collectively displayed a concerted, sustained mRNA-level response to prolonged high-temperature exposure. Herein we used univariate, multivariate, and modeling approaches with the same transcriptomic dataset and identified numerous genes only expressed by corals at high temperatures; although this finding was not generally supported by real-time PCR, these genes may nevertheless be of use to those seeking to develop biomarker assays or molecularly biology-trained predictive models for identifying corals displaying “alternative stable states,” in which their cellular biology has fundamentally changed on account of having acclimatized to chronically high temperatures.

  21. Monteiro, H.J.A., C. Brahmi, A.B. Mayfield, J. Vidal-Dupiol, B. Lapeyre, and J. Le Luyer. Molecular mechanisms of acclimation to long-term elevated temperature exposure in marine symbioses. Global Change Biology, 26(3):1271-1284, https://doi.org/10.1111/gcb.14907 2020

    Abstract:

    Seawater temperature rise in French Polynesia has repeatedly resulted in the bleaching of corals and giant clams. Because giant clams possess distinctive ectosymbiotic features, they represent a unique and powerful model for comparing molecular pathways involved in (a) maintenance of symbiosis and (b) acquisition of thermotolerance among coral reef organisms. Herein, we explored the physiological and transcriptomic responses of the clam hosts and their photosynthetically active symbionts over a 65-day experiment in which clams were exposed to either normal or environmentally relevant elevated seawater temperatures. Additionally, we used metabarcoding data coupled with in situ sampling/survey data to explore the relative importance of holobiont adaptation (i.e., a symbiont community shift) versus acclimation (i.e., physiological changes at the molecular level) in the clams’ responses to environmental change. We finally compared transcriptomic data to publicly available genomic datasets for Symbiodiniaceae dinoflagellates (both cultured and in hospite with the coral Pocillopora damicornis) to better tease apart the responses of both hosts and specific symbiont genotypes in this mutualistic association. Gene module preservation analysis revealed that the function of the symbionts’ photosystem II was impaired at high temperature, and this response was also found across all holobionts and Symbiodiniaceae lineages examined. Similarly, epigenetic modulation appeared to be a key response mechanism for symbionts in hospite with giant clams exposed to high temperatures, and such modulation was able to distinguish thermotolerant from thermosensitive Cladocopium goreaui ecotypes; epigenetic processes may, then, represent a promising research avenue for those interested in coral reef conservation in this era of changing global climate.

  22. Peng, S.E., A. Moret, C. Chang, A.B. Mayfield, Y.-T. Ren, W.-N.U. Chen, M. Giordano, and C.S. Chen. A shift away from mutualism under food-deprived conditions in an anemone-dinoflagellate association. PeerJ, 8:e9745, https://doi.org/10.7717/peerj.9745 2020

    Abstract:

    The mutualistic symbiosis between anthozoans and intra-gastrodermal dinoflagellatesof the family Symbiodiniaceae is the functional basis of all coral reef ecosystems, with the latter providing up to 95% of their fixed photosynthate to their hosts in exchangefor nutrients. However, recent studies of sponges, jellyfish, and anemones have revealed the potential for this mutualistic relationship to shift to parasitism under stressful conditions. Over a period of eight weeks, we compared the physiological conditionsof both inoculated and aposymbiotic anemones (Exaiptasia pallida) that were either fed or starved. By the sixth week, both fed groups of anemones were significantly larger than their starved counterparts. Moreover, inoculated and starved anemones tended to disintegrate into ‘‘tissue balls’’ within eight weeks, and 25% of the samples died; in contrast, starved aposymbiotic anemones required six months to form tissue balls, and no anemones from this group died. Our results show that the dinoflagellates within inoculated anemones may have posed a fatal metabolic burden on their hosts during starvation; this may be because of the need to prioritize their own metabolism and nourishment at the expense of their hosts. Collectively, our study reveals the potential of this dynamic symbiotic association to shift away from mutualism during food-deprived conditions.

  23. Chen, T.-Y., G.-W. Hwang, A.B. Mayfield, C.-P. Chen, and H.-J. Lin. The development of habitat suitability models for fiddler crabs residing in subtropical tidal flats. Ocean and Coastal Management, 182:104931, https://doi.org/10.1016/j.ocecoaman.2019.104931 2019

    Abstract:

    Fiddler crabs are deposit feeders that play critical roles as ecological engineers in tidal flats. Recently, anthropogenic disturbances have led to fiddler crab habitat loss and/or degradation; therefore, we developed a mathematically derived habitat suitability index (HSI) model to aid in habitat assessments of fiddler crabs. Based on what is known about the life histories of fiddler crabs, the variables of an HSI model included submersion time, interstitial salinity, and soil (1) grain size, (2) organic matter content, and (3) heat capacity. We acquired density data from four fiddler crab species—Xeruca formosensis, Tubuca arcuata, Austruca lactea, and Gelasimus borealis— at five sites on the western coast of Taiwan to develop the HSI models. Significant positive correlations existed between the HSI output and fiddler crab density for all target species except for those X. formosensis inhabiting the topsoil layer (0–20 cm). For the deep burrowers X. formosensis, however, a positive linear relationship was documented when only those data from the 40–60 cm layers were considered and if the habitat was a sand-covered mudflat. Mapping for each species was conducted using the HSI models with the highest reliability, and four classification levels were established for the habitat suitability of each species at one of the study sites. Based on this field test of a fiddler crab HSI model, we have developed a platform for the proactive conservation of fiddler crabs inhabiting subtropical tidal flats.

  24. Mayfield, A.B., and C.S. Chen. Enabling coral reef triage via molecular biotechnology and artificial intelligence. Platax, 16:23-47, https://10.29926/PLATAX.201912_2019.002 2019

    Abstract:

    Coral reef ecosystems are threatened by an onslaught of anthropogenic stressors, most notably global climate change (GCC); indeed, no regions have been spared from our wide-ranging human impact. Consequently, there have been urgent pushes to (1) model how marine organisms will respond to changes in their environments and (2) make data-driven predictions as to which populations are most stress sensitive. Given our recently elevated understanding of how GCC affects reef corals, we are now in a position in which it may be possible to make projections as to which corals are most susceptible to GCC, as well as which will demonstrate resilience. Herein we explore the potential for artificial intelligence-based approaches to generate models that can accurately predict coral stress susceptibility (CSS). Specifically, we advocate that coral reef-focused partial least squares and neural networking algorithms should be developed, with their prognostic capability then field-tested at sites spanning a gradient of human impact and ecological resilience in the high-biodiversity “Coral Triangle.” If the developed actuarial models are characterized by the analytical capacity to forecast CSS, we will possess one means of identifying reefs thatshould be prioritized for conservation (i.e., coral reef “triage”).