PLoS ONEplosplosonePLOS ONE1932-6203Public Library of ScienceSan Francisco, CA USA10.1371/journal.pone.0273897PONE-D-22-07335Research ArticleBiology and life sciencesMarine biologyCoral reefsEarth sciencesMarine and aquatic sciencesMarine biologyCoral reefsEarth sciencesMarine and aquatic sciencesReefsCoral reefsBiology and life sciencesMarine biologyCoralsEarth sciencesMarine and aquatic sciencesMarine biologyCoralsBiology and life sciencesPhysiologyPhysiological parametersBiology and life sciencesOrganismsEukaryotaPlantsAlgaeBiology and life sciencesCell biologyCellular structures and organellesChloroplastsChlorophyllBiology and life sciencesCell biologyPlant cell biologyChloroplastsChlorophyllBiology and life sciencesPlant sciencePlant cell biologyChloroplastsChlorophyllBiology and life sciencesCell biologyCellular typesPlant cellsChloroplastsChlorophyllBiology and life sciencesCell biologyPlant cell biologyPlant cellsChloroplastsChlorophyllBiology and life sciencesPlant sciencePlant cell biologyPlant cellsChloroplastsChlorophyllPhysical sciencesMaterials scienceMaterialsPigmentsOrganic pigmentsChlorophyllPhysical sciencesChemistryChemical compoundsOrganic compoundsCarbohydratesPhysical sciencesChemistryOrganic chemistryOrganic compoundsCarbohydratesEarth sciencesMarine and aquatic sciencesOceanographyOcean acidificationResearch and analysis methodsMathematical and statistical techniquesStatistical methodsMultivariate analysisPrincipal component analysisPhysical sciencesMathematicsStatisticsStatistical methodsMultivariate analysisPrincipal component analysisGlobal change differentially modulates Caribbean coral physiologyGlobal change modulates coral physiologyhttps://orcid.org/0000-0003-0340-1371BoveColleen B.ConceptualizationData curationFormal analysisFunding acquisitionMethodologyVisualizationWriting – original draftWriting – review & editing12*DaviesSarah W.ConceptualizationMethodologySupervisionWriting – review & editing2RiesJustin B.ConceptualizationFunding acquisitionMethodologySupervisionWriting – review & editing3UmbanhowarJamesFormal analysisWriting – review & editing14ThomassonBailey C.Data curationWriting – review & editing45FarquharElizabeth B.Data curationWriting – review & editing16McCoppinJess A.Data curationWriting – review & editing4CastilloKarl D.ConceptualizationFunding acquisitionMethodologySupervisionWriting – review & editing17Environment, Ecology, and Energy Program, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of AmericaThe Department of Biology, Boston University, Boston, Massachusetts, United States of AmericaDepartment of Marine and Environmental Sciences, Northeastern University, Nahant, MA, United States of AmericaThe Department of Biology, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of AmericaCoral Restoration Foundation, Key Largo, Florida, United States of AmericaCenter for Marine Science, University of North Carolina Wilmington, Wilmington, NC, United States of AmericaDepartment of Earth, Marine and Environmental Sciences, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of AmericaMayfieldAnderson B.EditorLiving Oceans Foundation, TAIWAN
The authors have declared that no competing interests exist.
* E-mail: colleenbove@gmail.com2920222022179e0273897113202217820222022Bove et alThis is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Global change driven by anthropogenic carbon emissions is altering ecosystems at unprecedented rates, especially coral reefs, whose symbiosis with algal symbionts is particularly vulnerable to increasing ocean temperatures and altered carbonate chemistry. Here, we assess the physiological responses of three Caribbean coral (animal host + algal symbiont) species from an inshore and offshore reef environment after exposure to simulated ocean warming (28, 31°C), acidification (300–3290 μatm), and the combination of stressors for 93 days. We used multidimensional analyses to assess how a variety of coral physiological parameters respond to ocean acidification and warming. Our results demonstrate reductions in coral health in Siderastrea siderea and Porites astreoides in response to projected ocean acidification, while future warming elicited severe declines in Pseudodiploria strigosa. Offshore S. siderea fragments exhibited higher physiological plasticity than inshore counterparts, suggesting that this offshore population was more susceptible to changing conditions. There were no plasticity differences in P. strigosa and P. astreoides between natal reef environments, however, temperature evoked stronger responses in both species. Interestingly, while each species exhibited unique physiological responses to ocean acidification and warming, when data from all three species are modelled together, convergent stress responses to these conditions are observed, highlighting the overall sensitivities of tropical corals to these stressors. Our results demonstrate that while ocean warming is a severe acute stressor that will have dire consequences for coral reefs globally, chronic exposure to acidification may also impact coral physiology to a greater extent in some species than previously assumed. Further, our study identifies S. siderea and P. astreoides as potential ‘winners’ on future Caribbean coral reefs due to their resilience under projected global change stressors, while P. strigosa will likely be a ‘loser’ due to their sensitivity to thermal stress events. Together, these species-specific responses to global change we observe will likely manifest in altered Caribbean reef assemblages in the future.
http://dx.doi.org/10.13039/100000001National Science Foundation#1437371RiesJustin B.Women Diver Hall of Famehttps://orcid.org/0000-0003-0340-1371BoveColleen B.Lerner-Gray Memorial Fund of the American Museum of Natural Historyhttps://orcid.org/0000-0003-0340-1371BoveColleen B.This research was partially supported by the Women Diver Hall of Fame Sea of Change Foundation Marine Conservation Scholarship (https://www.wdhof.org/scholarship/marine-conservation-scholarship-graduate) and Lerner-Gray Memorial Fund of the American Museum of Natural History Grants for Marine Research (https://www.amnh.org/research/richard-gilder-graduate-school/academics-and-research/fellowship-and-grant-opportunities/research-grants-and-graduate-student-exchange-fellowships/the-lerner-gray-fund-for-marine-research) awarded to CBB. JBR acknowledges support from NSF BIO-OCE award #1437371 (https://www.nsf.gov/geo/oce/programs/biores.jsp). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Data AvailabilityAll data and code used in this manuscript are archived at Zenodo (10.5281/zenodo.5093907) and can be freely accessed on GitHub (github.com/seabove7/Bove_CoralPhysiology). Protocols for host carbohydrate and lipid assays can be accessed on protocols.io (carbohydrate: doi.org/10.17504/protocols.io.bvb9n2r6; lipid: doi.org/10.17504/protocols.io.bvcfn2tn).Introduction
Human-induced global change is driving unprecedented challenges for ecosystems globally, from increases in terrestrial droughts [1] and severe storm activity across lower latitudes [2] to altering species’ distributions globally [3,4]. Coral reefs are a prime example of an ecosystem heavily impacted by global change, particularly by ocean warming and acidification [5–8]. Ocean acidification and warming are predicted to affect many marine ecosystems by reducing ecosystem complexity and function, especially for organisms with longer generational times and thus fewer opportunities to adapt to changing conditions [9]. Therefore, understanding the diversity of responses of tropical reef-building corals at both the species- and population-levels is critical for predicting future impacts of global change.
Previous work assessing tropical reef-building corals under global change has generally focussed on quantifying changes in coral calcification rates owing to the ecological importance of new reef production for the maintenance of these ecosystems [10–15]. These studies demonstrate a diversity of calcification responses under stress, including maintained and suppressed growth rates [12,16,17]. For example, the Caribbean coral species Siderastrea siderea and Porites astreoides have been shown previously to maintain higher growth rates under ocean acidification and/or warming stress, [16–18] and other species, such as Orbicella faveolata and Acropora cervicornis, generally exhibited reduced growth under these same stressors [14,18,19]. While some corals sustain growth rates under stress, these corals may accomplish this at a cost to other metabolic processes [20,21] or through modifications to holobiont (animal host, dinoflagellates, bacteria, viruses, etc.) communities.
Tropical reef-building corals depend on the maintenance of an endosymbiotic relationship with photosynthetic dinoflagellates (family Symbiodiniaceae) for a significant portion of their energetic needs [22]. However, this relationship often breaks down under severe or prolonged stress, especially with increasing seawater temperature, resulting in the phenomenon known as ‘coral bleaching’ [23–25]. Corals bleach in response to ocean acidification, but especially in response to warming, and this loss of symbiosis leads to declines in calcification and gametogenesis [26]. Thus, as the symbiosis between the coral host and algal symbionts breaks down, both components of the coral are likely to exhibit closely integrated physiological responses. Indeed, previous work has observed that greater coral tissue biomass follows increased symbiont density and chlorophyll a content in several Caribbean reef-building coral species [27], highlighting the intrinsic relationship with algal symbionts to support the coral host’s energy budget. Further, previous work has reported the influence of algal symbiont and microbiome communities as mechanisms of improving coral holobiont physiology under environmental stress [28–32]. Overall, it is clear that maintaining healthy symbioses within the coral holobiont is critical for the physiological health of the coral host.
Coral tissue biomass and energy reserves (e.g., lipid, protein, carbohydrate) are important aspects of overall coral health [33,34] that provide insight into resilience and recovery capacity in response to environmental stressors. Although energy reserves are extremely important in understanding the coral host response to stress, few studies have investigated how the combination of ocean acidification and warming influence these traits [34–36]. Coral tissue biomass relies on the equilibrium between energy sources and expenditures; thus, corals with already low biomass (i.e., low energy reserves) may experience heightened vulnerability under environmental stress [37] and may explain some of the variation of physiological responses to stress within and between species [16,17]. However, studies have demonstrated that corals may not always consume energy reserves under environmental stress [34] or increase metabolic processes [38]. Instead, corals may use other physiological mechanisms as coping tools to maintain growth and host energy reserves, such as relying more on algal symbionts whose photosynthesis is fertilised under conditions of elevated pCO2 [39].
Many symbiotic corals also have the capacity to exhibit physiological plasticity (i.e., modification of an organism’s physiology) in response to changing environments that may be employed under global change scenarios [40,41]. While plasticity is often highlighted as a mechanism for rapid response to changing environments, there is debate about whether plasticity alone is enough to ensure species persistence under global change [42]. Indeed, a highly plastic coral may be able to modulate its physiology (e.g., increase chlorophyll a per symbiont cell) under an acute stress event (e.g., low light levels) [43], but this is likely to come at a cost to another metabolic process, such as energy stores. This physiological cost can be beneficial for the coral in the short term, however, may eventually result in a decline in fitness [42,44], especially in long-lived organisms like reef-building corals. These potential trade-offs in reef-building corals remain poorly understood and highlight the complexities of plasticity as a mode of global change resilience.
To assess the physiological responses of Caribbean corals to independent and combined ocean acidification (300–3290 μatm) and warming (28, 31°C), we conducted a 93-day common-garden experiment on 3 species of corals (S. siderea, Pseudodiploria strigosa, P. astreoides) and quantified coral host energy reserves (total protein, carbohydrate, lipid) and algal symbiont physiology (cell density, chlorophyll a concentration, coral colour intensity). These coral species were selected because they represent both weedy (P. astreoides) and stress-tolerant (S. siderea and P. strigosa) life histories [45], possess similar growth morphologies (mounding), and are common throughout the Caribbean across a variety of environmental gradients. Additionally, we included corals from two distinct reef environments to assess how environmental histories impact responses to global change stressors. Overall, we selected these species to better understand how corals that are expected to dominate Caribbean reefs in the future may respond to global change stressors. We hypothesised that (1) corals are more susceptible to thermal stress than acidification, (2) physiological responses are highly species-specific, and (3) physiological plasticity dictates coral resilience under global change. Our results highlight the diversity of physiological responses, from susceptibility to resistance, that Caribbean corals exhibit in response to projected global change, which will ultimately drive changes in community compositions across space.
MethodsExperimental design
Six colonies each of three Caribbean reef-building corals (Siderastrea siderea, Pseudodiploria strigosa, Porites astreoides) were collected from inshore (Port Honduras Marine Reserve; 16°11’23.5314”N, 88°34’21.9360”W) and offshore (Sapodilla Cayes Marine Reserve; 16°07’00.0114”N, 88°15’41.1834”W) reef environments at similar depths (3–5 m) from the southern portion of the Belize Mesoamerican Barrier Reef System. All corals were collected following local laws and regulations with appropriate permits (#5674). These two distinct reef environments are approximately 25 km apart and were selected to explore how environmental history (e.g., temperature, salinity, carbonate chemistry, nutrients, etc.) affects responses to global change. Specifically, the inshore site is known to be more environmentally variable (i.e., diel and seasonal variability) than the offshore location (S1 Fig), potentially diving local adaptation and/or long-term acclimatisation in these species [46–48]. This study further investigates the physiological responses of corals assessed in Bove et al. [17] and detailed descriptions of experimental setup can be found there.
Corals (2 reef environments x 3 species x 6 colonies = 36 colonies) were collected and transported to Northeastern University’s Marine Science Center. Colonies were sectioned into eight equally-sized fragments (8 fragments/colony = 288 total samples) and returned to ambient conditions for a 23-day recovery period, followed by a 20-day acclimation period where tanks were slowly adjusted to target experimental treatment conditions. Corals were maintained in one of eight experimental treatments (three replicate tanks per treatment; see S2 Fig for coral allocation schematic and Table A in S1 Text for sample sizes) for the 93-day experiment. The eight treatments encompassed four pCO2 treatments (Table 1) corresponding to pre-industrial, current-day (pCO2 control), moderate end-of-century, and an extreme pCO2 level all crossed with two temperatures (Table 1) corresponding to the corals’ approximate present-day summer mean and projected end-of-century summer warming[49] that has also been observed to induce bleaching in these species [50]. High-precision digital solenoid-valve mass flow controllers (Aalborg Instruments and Controls; Orangeburg, NY, USA) were used to bubble air alone (control pCO2 conditions), or in combination with CO2-free air (pre-industrial conditions) or CO2 gas (end-of-century and extreme conditions) to achieve gas mixtures of each desired pCO2 condition.
10.1371/journal.pone.0273897.t001
Warming and acidification treatment means and standard deviations.
Temperature Treatment (°C)
pCO2 treatment (μatm)
Pre-industrial
Current-day
End-of-century
Extreme
Control
28 ± 0.4
288 ± 65
447 ± 152
673 ± 104
3285 ± 484
Warming
31 ± 0.4
311 ± 96
405 ± 91
701 ± 94
3309 ± 414
Experimental tanks were filled with 5 μm-filtered natural seawater from Massachusetts Bay with a salinity of 31.7 psu (±0.2) and were illuminated with full spectrum LED lights on a 10:14 light-dark cycle with photosynthetically active radiation of approximately 300 μmol photons m–2 s–1. Corals were fed a combination of ca. 6 g frozen adult Artemia and 250 mL concentrated newly hatched live Artemia (500 mL-1) every other day to satisfy heterotrophic feeding [51,52]. Temperature, salinity and pH were measured at the same time (~1PM) every other day throughout the experiment and total alkalinity (TA) and dissolved inorganic carbon (DIC) were analysed every 10 days with a VINDTA 3C (Marianda Corporation, Kiel, Germany) (S3 Fig). Temperature, salinity, TA, and DIC were used to calculate carbonate parameters using CO2SYS [53] with Roy et al. [54] carbonic acid constants K1 and K2, Mucci’s value for the stoichiometric aragonite solubility product [55], and an atmospheric pressure of 1.015 atm. At the completion of the experimental period, corals were immediately flash-frozen in liquid nitrogen and transported to the University of North Carolina at Chapel Hill. Coral tissue was removed from the skeleton using seawater with an airbrush and stored in 50 mL conical tubes at −80°C until further processing.
Host and symbiont physiological parameter assessments
Preserved coral tissue slurries were homogenised with a Tissue-tearor (BioSpec Products; Bartlesville, Oklahoma, USA) for several minutes and vortexed for 5 seconds, after which 1.0 mL of slurry was aliquoted for algal symbiont density analysis. Algal symbiont aliquots were dyed with 200 μL of a 1:1 Lugol’s iodine and formalin solution and cell densities were quantified by performing at least 3 replicate counts of 10 μL samples using a hemocytometer (1 x 1 mm; Hausser Scientific, Horsham, Pennsylvania, USA) and a compound microscope. Algal symbiont densities were standardised to total tissue volume and previously measured coral surface area (106 cells per cm2) [17]. Remaining tissue slurry was centrifuged at 4400 rpm for 3 minutes to separate the coral host and algal symbiont fractions, and the host fraction was poured off from the symbiont pellet. Chlorophyll a pigment was extracted from the algal pellet by adding 40 mL of 90% acetone to the conical tube at −20°C for 24 hours. Samples were diluted by adding 0.1 mL of extracted chlorophyll a sample to 1.9 mL of 90% acetone. If samples were too high or too low for detection on the fluorometer, samples were reanalysed by either diluting or concentrating the sample, respectively. Extracted chlorophyll a content was measured using a Turner Design 10-AU fluorometer with the acidification method [56] and expressed as the μg of pigment per cm2 of coral tissue surface area.
Coral host supernatant was aliquoted (1 mL each) for total protein, carbohydrate, and lipid analysis, and stored at −80°C. Glass beads were added to total protein aliquots, vortexed for 15 minutes, and centrifuged for 3 minutes at 4000 rpm. Duplicate samples were prepared with 235 μL of seawater, 15 μL of protein aliquot, and 250 μL of Bradford reagent (Thermo Scientific) and left for 20 minutes. Coral host total protein samples were read at 562 nm on a spectrophotometer (Eppendorf BioSpectrometer® basic; Hamburg, Germany) in duplicates and were expressed as mg per cm2 coral tissue surface area. For coral host carbohydrate, 25 μL of phenol was added to 1000 μL of diluted coral host slurry and vortexed for 3 seconds before immediately adding 2.5 mL concentrated sulphuric acid (H2SO4). Samples were incubated at room temperature for 1 minute and then transferred to a room temperature water bath for 30 minutes [57]. Finally, 200 μL of each standard and sample was pipetted into a 96-well plate in triplicate and read on a spectrophotometer at 485 nm (BMG LABTECH POLARstart Omega; Cary, North Carolina, USA). Total carbohydrate was expressed as mg per cm2 coral tissue surface area [58]. Coral host lipids were extracted following the Folch Method [59] by adding 600 μL of chloroform (CHCl3) and methanol (CH3OH) in a 2:1 ratio to 600 μL of host slurry and placed on a plate shaker for 20 minutes before adding 160 μL of 0.05M sodium chloride (NaCl). Tubes were inverted twice and then centrifuged at 3000 rpm for 5 minutes. Finally, the lipid layer was removed and 100 μL was pipetted in triplicate into a 96-well plate for colourimetric assay. The lipid assay was performed by adding 50 μL of CH3OH to each well before evaporating the solvent at 90°C for 10 minutes. Next, 100 μL of H2SO4 was added to every well, incubated at 90°C for 20 minutes, and cooled on ice for 2 minutes before transferring 75 μL of each sample into a new 96-well plate. Background absorbance of the new plate was read at 540 nm on a spectrophotometer before adding 34.5 μL of 0.2 mg/mL vanillin in 17% phosphoric acid to each well. The plate was read again at 540 nm and coral host lipid concentrations were normalised to coral surface area (mg per cm2) [60,61].
Coral colour intensity was also analysed from images of every fragment with standardized colour scales taken at every 30 days throughout the experiment. This assessment complements other algal symbiont physiological assessments as a non-destructive alternative to quantify coral bleaching. Colour balance was adjusted using a custom Python script that took a square of pixels as a white standard (50 x 50) on each image to adjust the colour balance until it was true white. The total red, green, blue, and sum of all colour channel intensities were measured following [62] using the MATLAB macro “AnalyzeIntensity” for either 10 (S. siderea and P. astreoides) or 20 (P. strigosa; 10 in valley and 10 on ridges) quadrats of 25 x 25 pixels on each coral fragment. The resulting values act as a measure of brightness, with higher brightness values correlating with pigment lightening (i.e., coral bleaching); thus, data were inverted so that lower values represent reduced coral pigmentation. The sum of all colour channels (red, green, blue) resulted in a stronger correlation with symbiont physiology (chlorophyll a and cell density) in S. siderea and P. strigosa, while the red channel alone was best in P. astreoides.
Coral physiology analyses
Sample mortality was observed throughout the experimental period across species as described in Bove et al. [17] and thus some treatments resulted in reduced replication for physiological analyses (Table A in S1 Text). Overall, S. siderea exhibited nearly 90% survival (86 total fragments), P. strigosa exhibited 80% survival (77 total fragments), and P. astreoides exhibited 72% survival (69 total fragments) at the end of the experiment [17]. Further, the initial and final control treatment sample size of P. strigosa was lower than other species because this treatment system had to be reconstructed before the start of the experiment and there were only a few reserve genotypes of this species available for the new control system.
Principal component analysis (PCA) (function prcomp) of scaled and centered physiological parameters (host carbohydrate, host lipid, host protein, algal symbiont chlorophyll a, algal symbiont cell density, calcification rate as previously reported for the same samples in Bove et al [17]) were employed to assess the relationship between physiological parameters and treatment conditions for each coral species. Main effects (temperature, pCO2, reef environment) were evaluated with PERMANOVA using the adonis2 function (vegan package; version 2.5.7 [63]). The additive model resulted in a lower AIC than the fully interactive model for all species, so interaction terms were dropped from each model resulting in fully additive models (see Table B in S1 Text).
Correlations of all physiological parameters were assessed to determine the relationships between parameters within each species. The Pearson correlation coefficient (R2) of each comparison was calculated using the corrgram package (version 1.13 [64]) and the significance was calculated using the cor.test function. These relationships were then visualised through simple scatterplots.
Here, we use physiological plasticity to refer to the amount an individual modifies its physiology in response to stress compared to observed physiology under control conditions. Physiological plasticity of each experimental fragment was calculated for each species using all principal components (PCs) calculated above as the distance between an experimental fragment and the control (420 μatm; 28°C) fragment from that same colony [65]. The effects of treatment (pCO2 and temperature) and natal reef environment on calculated distances were assessed using generalised linear mixed effects models (function lmer) with a Gamma distribution and log-link and a random effect for colony (P. strigosa and P. astreoides) or tank crossed with colony (S. siderea). The best-fit model was selected as the model with the lowest AIC for each species (Table C in S1 Text). Natal reef environment was only a significant predictor of plasticity in S. siderea; thus, samples were pooled across reef environments for both P. strigosa and P. astreoides. Parametric bootstraps were performed to model mean response and 95% confidence intervals with 1500 iterations and significant effects were defined as non-overlapping confidence intervals. Marginal and conditional R2 values of the best fit models were calculated using the r2_nakagawa function in the rcompanion package (version 2.4.13 [66]). All figures and statistical analyses were carried out in R version 4.1.2 (R Core Team, 2018) and the accompanying data and code can be freely accessed on GitHub (github.com/seabove7/Bove_CoralPhysiology) and Zenodo (10.5281/zenodo.5093907).
ResultsPrincipal component analysis
Two PCs explained approximately 66% of the variance in physiological responses of S. siderea to ocean acidification and warming treatments (Fig 1A). PC1 was driven by differences in algal symbiont physiology (chlorophyll a, cell density), while PC2 represented an inverse relationship between host energy reserves (lipid, protein, carbohydrate) and calcification rates and colour intensities. Overall, higher pCO2 and temperature resulted in reduced S. siderea physiology (Fig 1A). Treatment pCO2 predominantly drove S. siderea physiological responses (p = 7e-04), while temperature and reef environment did not explain as much variation in physiological responses (p = 0.05 and p = 0.001, respectively; Table D in S1 Text and S4A Fig). These observed responses are driven by declines in total host physiology under warming as well as reduced symbiont physiology with increasing pCO2 (S5A Fig). Further, no significant interactive effect between temperature and pCO2 was detected in S. siderea physiology (S4D Fig).
10.1371/journal.pone.0273897.g001
Principal component analysis (PCA) of all coral physiological parameters for (A) S. siderea, (B) P. strigosa, and (C) P. astreoides after 93 days of exposure to different temperature and pCO2 treatments. PCAs of (A) S. siderea and (C) P. astreoides are depicted by pCO2 in colour (pre industrial [300 μatm], light purple; current day [420 μatm], dark purple; end-of-century [680 μatm], light orange; extreme [3290 μatm], dark orange) and temperature by shape (filled circles 28°C; open circles 31°C). The PCA for (B) P. strigosa is depicted by temperature in colour (28°C blue; 31°C red) and pCO2 by shape (pre industrial, circles; current day, triangles; end-of-century, squares; extreme, stars). Arrows represent significant (p < 0.05) correlation vectors for physiological parameters (rate = calcification rate; den = symbiont density; chla = chlorophyll a; pro = protein; carb = carbohydrate; lipid = lipid; colour = colour intensity) and ellipses represent 95% confidence based on multivariate t-distributions.
For P. strigosa, 74% of the variance in response to treatments was explained by two PCs (Fig 1B). PC1 explained most of the variation of physiological parameters with the exception of host lipid content, which was represented in PC2. Physiology of P. strigosa was reduced under warming (p = 7e-04) and in offshore samples (p = 7e-04; S4B Fig), however, pCO2 did not clearly alter physiology (Fig 1B; p = 0.2; Table D in S1 Text). This clear decline in physiology under warming is driven by declines in symbiont physiology and total host protein content (S5B Fig). Again, no significant interactive effect between temperature and pCO2 was detected (S3E Fig).
For P. astreoides, the first two PCs explained 59% of the total variance in response to treatment (Fig 1C). Samples separated most along PC1 driven primarily by calcification rate and algal symbiont density, while PC2 exhibited an inverse relationship between host total carbohydrate and colour intensity. Overall, higher pCO2 reduced P. astreoides physiology, while elevated temperature resulted in improved physiology (Fig 1C). These patterns are most notable in the reduced host energy reserves in response to increasing pCO2 and higher symbiont physiology and lipid content under warming (S5C Fig). Temperature (p = 0.001) and pCO2 (p = 7e-04) altered P. astreoides physiology, while reef environment was not significant (p = 0.5; Table D in S1 Text and S4C Fig) and there was no significant interactive effect between temperature and pCO2 (S3F Fig).
Correlations of physiological parameters
Coral physiological parameters were generally positively correlated with one another within each of the three species. Correlations between S. siderea physiological parameters identified 15 significant relationships out of all 21 possible comparisons (Fig 2A). Of those significant correlations, six resulted in a Pearson’s correlation coefficient (R2) equal to or greater than 0.5, with the strongest relationship identified between symbiont density and chlorophyll a (R2 = 0.72).
10.1371/journal.pone.0273897.g002
Coral physiological parameter scatter plots (top) and correlation matrices (bottom) for (A) S. siderea, (B) P. strigosa, and (C) P. astreoides showing pairwise comparisons of within each species. Scatter plots of each pairwise combination of physiological parameters are displayed on the top with temperature treatment depicted by shape (28°C closed points; 31°C open points) and pCO2 treatment depicted by colour (pre industrial [300 μatm], light purple; current day [420 μatm], dark purple; end-of-century [680 μatm], light orange; extreme [3290 μatm], dark orange). Strengths of the correlations (R2 via Pearson correlation coefficients) between each pairwise combination of physiological parameters are indicated by darker shades of blue on the bottom with significance depicted by asterisks according to significance level (* p < 0.05; ** p < 0.01; *** p < 0.001). R2 and significance levels correspond to the scatter plot at the intersection between two physiological parameters.
All pairwise physiological parameters were significantly correlated with one another in P. strigosa and, of those, 15 correlations exhibit moderate (R2 > 0.50) positive relationships (Fig 2B). Notably, the two strongest correlations were host carbohydrate vs. host protein (R2 = 0.70) and host carbohydrate vs. chlorophyll a (R2 = 0.76).
Compared to both S. siderea and P. strigosa, fewer physiological traits were significantly (p < 0.05) correlated with one another in P. astreoides (12 significant out of 21 total comparisons; Fig 2C). Of the significant correlations, only two pairwise comparisons resulted in a Pearson’s correlation coefficient greater than 0.5: chlorophyll a vs. colour intensity (R2 = 0.57) and host carbohydrate vs. host protein (R2 = 0.68).
Coral physiological plasticity
Physiological plasticity of offshore S. siderea fragments exhibited a positive linear trend with increasing pCO2, while the inshore fragments appear to respond in a parabolic pattern to pCO2, with the lowest calculated distances occurring at 420 μatm, 31°C and 680 μatm, 28°C (Fig 3A). Further, offshore S. siderea fragments exhibited higher plasticity in the extreme pCO2 treatment than in inshore fragments reared in the pre-industrial, current-day, and extreme pCO2 treatments, regardless of temperature (Fig 3A and Table E in S1 Text).
10.1371/journal.pone.0273897.g003
Physiological plasticity of (A) S. siderea, (B) P. strigosa, and (C) P. astreoides after 93-day exposure to experimental treatments. Higher values represent greater plasticity (stronger response) in coral samples. Natal reef environment is depicted along the x axis for S. siderea, however, P. strigosa and P. astreoides samples were pooled by reef environment. pCO2 treatment is depicted by colour and shape (pre industrial [300 μatm], light purple; current day [420 μatm], dark purple; end-of-century [680 μatm], light orange; extreme [3290 μatm], dark orange) and temperature is represented as either closed (28°C) or open (31°C) symbols. The current day at 28°C treatment is not depicted here since plasticity is represented as the distance from this treatment (420 μatm at 28°C). Symbols and bars indicate modelled means and 95% confidence intervals. Non overlapping confidence intervals were interpreted to be statistically different.
Plasticity of P. strigosa and P. astreoides was not clearly different between colonies based on natal reef environments (see Table C in S1 Text). No clear differences in physiological plasticity in response to treatment were identified in P.strigosa (Fig 3B and Table E in S1 Text), however, this is likely due to reduced sample sizes in this analysis as a result of only five colonies (Noffshore = 3, Ninshore = 2) present in the control treatment for distance calculations.
Elevated temperature generally resulted in higher plasticity of P. astreoides compared to control temperature (Fig 3C and Table E in S1 Text), however, this trend was not clearly different within each pCO2 treatment. Physiological plasticity of P. astreoides was significantly lower in both the pre-industrial and end-of-century pCO2 treatments at control temperature than that measured in the extreme pCO2 treatment combined with the elevated temperature.
Species differences in coral physiology
The first two PCs of coral physiology explained about 62% of the total variance across samples (Fig 4). In general, fragments of S. siderea contained higher chlorophyll a content, host carbohydrate, and host lipid content, while P. strigosa fragments typically had greater host protein content accompanied by higher calcification rates, and fragments of P. astreoides were differentiated by their high symbiont densities (Figs 4A and S6). Despite being different coral species, coral physiology exhibited similar declines in responses to increasing pCO2 treatments (Fig 4B), however, responses to temperature were highly species-specific (Fig 4C and Table F in S1 Text). Furthermore, corals from the inshore reef environment exhibited more constrained physiology than their offshore counterparts (S6 Fig).
10.1371/journal.pone.0273897.g004
Principal component analysis (PCA) comparing the physiology of all three species at the end of the experiment with samples clustered by (A) species, (B) pCO2 treatment, and (C) temperature treatment. Arrows represent significant (p < 0.05) correlation vectors for physiological parameters and ellipses represent 95% confidence based on multivariate t-distributions.
DiscussionCoral physiology highlights sensitivity of Caribbean corals to global change
Caribbean coral reefs have experienced considerable shifts in ecosystem composition since the 1970s defined by declines in several stony coral taxa [67,68], resulting in reefs now dominated by weedy and stress-tolerant species. Ocean acidification, warming, and the combination of the two stressors are expected to further reduce coral abundance throughout the Caribbean by the end of this century [69]. We demonstrate a variety of coral responses to simulated ocean acidification and warming scenarios that provide insight into how multiple stress-tolerant and weedy coral species may respond to global change. Understanding individual physiological responses of coral hosts and their algal symbionts provides valuable insight into the relationship between these partners, especially in these now-dominant species. However, to better predict how corals will respond to global change, it is necessary to assess how the physiological parameters of both partners will respond. For example, we found that pCO2 treatment drove differences in coral physiology of both S. siderea and P. astreoides (Fig 1); however, these effects were not clear when assessing individual physiological parameters on their own within a species (S5 Fig). Indeed, several previous studies have reported mixed physiological responses to elevated pCO2, from no difference in coral host energy reserves [34] to reduced symbiont density and productivity loss [25,38]. These effects of pCO2 highlight the complexity of the responses of corals under stress [34,70,71] and suggest that, by limiting assessments to only a few physiological parameters, studies may miss important changes to the coral’s overall condition.
Coral physiologies of all three species were also modulated by temperature, although these impacts were more variable. Siderastrea siderea and P. strigosa both exhibited declines in physiology under elevated temperature (31°C) (Figs 1 and S5); however, these declines were more pronounced in P. strigosa, especially through time (Figs 1B and S7). Indeed, while P. strigosa was previously classified as a stress-tolerant species based on trait assessment [45], it has more recently been identified as a more thermally sensitive coral species [35,72,73]. This response is likely representative of the overall deterioration of coral condition in response to thermal stress, which may lead to mortality under chronic or extreme exposure as is being seen more frequently on Caribbean coral reefs [5]. Thermal events on coral reefs are generally considered to be acute stress events (on the scale of hours to weeks) [74]. Thus, exposure of these corals to more than 90 days of constant elevated temperature may have elicited a more severe response in P. strigosa as is seen during mass bleaching events in situ for this species [75]. Conversely, elevated temperature corresponded with improved physiological parameters in P. astreoides. These differences in coral thermal responses are not surprising given that P. astreoides is generally considered a more opportunistic coral that can persist in less-desirable conditions, including elevated temperature [18,45,76]. Conversely, S. siderea and P. strigosa are classified as ‘stress tolerant’ species with varying levels of susceptibility and resilience to environmental stress [16,50,77,78]. Despite some similarities in responses to ocean acidification and warming observed here, the different relationships between physiological parameters within each species likely interact to produce the species-specific responses observed in situ.
A major goal of this study was to better understand the combined effects of ocean warming and acidification on coral physiology since these stressors continue to change in lock step. While many studies report synergistic effects (i.e., the effects of both stressors compounding one another) of increasing temperature and pCO2 on coral responses [79–81], the interaction term of these treatments in our study was not significant in any models performed. In fact, the species assessed in our experiments generally exhibited clear responses to either warming (P. strigosa) or acidification (S. siderea and P. astreoides) that was only exacerbated by the other stressor in the high temperature, extreme acidification scenario (S4 Fig). Under the combined acidification and warming scenarios, it is possible that one stressor counteracted the effects of the other to result in marginal physiological changes [82]. Indeed, it has been suggested that CO2 fertilisation of algal symbionts under ocean acidification may improve coral physiology [39], potentially countering the negative effects of associated warming on coral-algal symbiosis. Conversely, metabolic processes generally improve along with increasing temperatures up to an individual’s thermal optimum [83], suggesting that the elevated temperature used here may have supported improved physiology, counteracting any negative effects of ocean acidification. Further, while other studies report synergistic effects on coral physiology, most of these studies only assess a single parameter, potentially missing other key physiological responses that suggest more additive responses like observed here. It is clear that coral responses under global change remain complex and require further investigation using additional multi-stressor, multi-species studies to tease apart these complexities.
Global change and species-specific drivers of physiological plasticity
On shorter ecological time scales–like those employed in this experiment–plasticity may be a coral’s most efficient response to global change, as it permits individual-level acclimatisation to a rapidly changing environment within a generation [40,42]. Plasticity has been identified as an important mechanism in coping with elevated pCO2 conditions in tropical corals [84–86] and may predict how these organisms will perform under global change. However, physiological plasticity may not always be beneficial long term and may instead signal a shift in organism condition [18,42,44]. Organisms exhibiting higher plasticity in response to environmental change (e.g., ocean warming and acidification) may incur a physiological cost in the form of a trade-off that ultimately may impact the population’s ability to resist future change [40–42]. Here we assessed the physiological plasticity of the coral under elevated temperature and pCO2, and compared these responses across two natal reef environments (inshore vs. offshore). We found that S. siderea fragments from the offshore exhibited higher plasticity in response to extreme pCO2 (3290 μatm) compared to the inshore counterparts, and that this pattern differed between the two habitats (Fig 3A). These results suggest that offshore S. siderea fragments modulated their physiology to a greater extent than the inshore corals and this shift in physiological state suggest reduced capacity to persist under future ocean acidification. This higher plasticity likely comes at a fitness trade-off in corals that are experiencing sub-optimum conditions [42,87]. Indeed, a reciprocal transplant experiment in southern Belize identified higher plasticity of offshore colonies of S. siderea compared to those from a nearshore environment [47]. The offshore colonies grew at a much higher rate when transplanted to the nearshore environment than in their natal environment (generally considered more ideal conditions) [47], suggesting that plasticity in these corals may indeed come at the cost of growth in home or more ideal conditions [42].
Varying levels of plasticity in P. strigosa and P. astreoides from different habitats has been previously reported [47,88]; however, natal reef effects were not evident in either species in this study (Fig 3B and 3C). The small sample size of P. strigosa likely contributed to the lack of differences between habitats, while different measures of plasticity–physiological plasticity (present study) vs. gene expression plasticity [88]–may contribute to the inconsistent responses observed in P. astreoides. While neither species exhibited differing levels of plasticity between reef environments, both P. strigosa and P. astreoides appear to exhibit higher plasticity at the elevated temperature, though this is only statistically significant in P. astreoides (Fig 3B and 3C). Interestingly, the higher plasticity at elevated temperatures in P. strigosa was associated with diminished physiological conditions, while higher plasticity in P. astreoides manifested as improved physiology (Fig 1B and 1C). These differences highlight how plasticity may result from physiological trade-offs in response to environmental change in some organisms (i.e., P. strigosa) [42,87], while other organisms (i.e., P. astreoides) may benefit from such plastic responses to match their physiology to their environment [89]. Either way, the role of plasticity in coral responses to global change is complex and merits further investigation to better understand species-specific levels of resilience.
Another explanation for varying susceptibilities across coral species under global change may relate to how physiological parameters are correlated to one another within the coral. For example, all physiological parameters were significantly correlated with one another for P. strigosa (Fig 2B), while only some correlations were significant for S. siderea and P. astreoides (Fig 2). Notably, while symbiont density was significantly correlated with all parameters in P. strigosa, it was least correlated with host lipid content, which was in turn best correlated with host protein and host carbohydrate (Fig 2B). This pattern suggests P. strigosa are consuming carbohydrate and protein stores in response to reduced symbiont density and chlorophyll a content, while lipid stores remain relatively unaltered, in line with previous work on coral energetics [90,91]. Siderastrea siderea exhibited similar relationships between symbiont density and all other physiological parameters; however, calcification rates were more dependent on algal symbiont status than host energy reserves (Fig 2A). Interestingly, P. astreoides symbiont density only resulted in a significant correlation with lipid content, while chlorophyll a was a better predictor of most physiological parameters (Fig 2C). In fact, chlorophyll a and symbiont density resulted in one of the strongest correlations in both S. siderea and P. strigosa, while these two parameters were not correlated in P. astreoides. This suggests that S. siderea and P. strigosa both rely on greater concentrations of algal symbionts with higher chlorophyll a content for autotrophically-derived carbon to support the coral host [22,92], while P. astreoides is dependent on more efficient symbionts alone [93,94]. Additionally, these three species are known to host varying algal symbiont communities (e.g., Siderastrea siderea predominantly hosts Cladocopium; P. strigosa hosts Cladocopium and Breviolum; P. astreoides hosts Breviolum and Symbiodinium [95,96]) that may determine differing carbon allocation to the host as well as different thermal tolerances of the coral [97,98]. Although profiling of the algal symbiont community was outside the scope of the current study, both temperature and pCO2 can modulate the symbiosis between coral hosts and algal symbionts [24,25,99,100]. Therefore, given that algal symbiont community and physiology play a significant role in coral responses to global change stressors, these types of data should be obtained in future experiments to better understand differences between and within tropical coral species.
Interestingly, when comparing PCAs of physiology from host only (lipid, carbohydrate, protein) and symbiont only (chlorophyll a, symbiont density, colour intensity) for each species, algal symbionts were generally more impacted than hosts by increasing pCO2 (i.e., pCO2 significantly drove differences in physiology in algal symbionts, not coral hosts) (S8–S10 Figs and Table G in S1 Text). For example, variance in S. siderea host physiology was not significantly explained by pCO2; however, pCO2 altered symbiont physiology. This result suggests that algal symbiont traits were being negatively impacted under ocean acidification, but that host energy reserves remained unaffected. This pattern contrasts previous work demonstrating no change in symbiont physiology under increased pCO2 [34,101,102] and others highlighting greater transcriptomic plasticity of coral hosts in response to increasing pCO2 relative to their algal symbionts [103]. Davies et al., [103] interpreted this result as the coral host responding poorly to pCO2 stress. However, our results suggest that coral hosts were able to maintain energy reserves despite reductions in symbiont density and chlorophyll a content. There is debate on the exact relationship between the coral host and algal symbionts (i.e., mutualism vs. parasitism) as well as their relative roles in coral bleaching [104–106]. While this symbiotic relationship is largely considered a mutualism, recent work has highlighted that this relationship is context dependent and, under specific circumstances, the algal symbionts may become more parasitic [107]. Regardless, it is clear that understanding the varied responses of the different symbiotic partners is critical for predicting the future of tropical coral reefs.
Global change drives similar physiological responses in Caribbean corals
Our results indicate species-specific relationships between physiological parameters within a coral that dictate responses to global change stressors and these patterns may separate the ‘winners’ from ‘losers’ on future reefs [108,109]. Comparisons across all experimental coral fragments highlight that S. siderea were differentiated by their higher host carbohydrate, host lipid, and chlorophyll a content, while P. strigosa fragments were associated with higher host protein and net calcification rates, and P. astreoides hosted the highest algal symbiont densities (Fig 4A). These physiological differences across species likely correspond to species-specific responses observed in this study and previous work assessing global change on tropical reef-building corals [16,17,48,110], as well as patterns of resilience observed in situ [76,78]. For example, S. siderea has generally been considered a more resilient species in terms of survival and growth when reared under ocean acidification and warming conditions [16,17,48]. This resilience may be associated with this species’ maintenance of higher host carbohydrate reserves as a result of greater chlorophyll a content [111] along with increased host lipids reserves for long-term performance [90,91]. The association of proteins with P. strigosa is also noteworthy given that corals generally obtain proteins from their algal symbionts [112]. However, P. strigosa was the most bleached of the three species (see S5 and S7 Figs), suggesting that this species exhibited the largest variation in protein as a result of the loss of productive symbionts with warming. These differences across species not only highlight differences in the underlying response strategies of Caribbean coral species, but may also assist in predicting responses to environmental stress.
Although the coral species examined here exhibit differing host and symbiont physiological responses, patterns of coral physiology converge under increasing pCO2, but not elevated temperature, regardless of species (Fig 4B and 4C). This pattern observed with increasing pCO2 cautions that the broad classification of coral species as ‘resistant’ or ‘susceptible’ to environmental stressors based on individual physiological responses [16,17,34,45,113] may overgeneralize sensitivity to future reef projections [6,16,69]. For example, recent observations of reduced recruitment and size distributions of P. astreoides, commonly labelled a ‘winning’ coral species across the Caribbean [114], suggest that qualifying the success of a species based on short-term studies or limited data (e.g., only measuring a single response parameter) may misrepresent its long-term trajectory. We are already witnessing species that were previously classified as stress-tolerant (i.e., P. strigosa) [45] shifting into a more susceptible category in the past several years alone [17,72], further highlighting the need to reassess how we label resilience in tropical reef-building corals. Similarly, Caribbean coral reef communities have experienced dramatic shifts in species composition and abundance over the past several decades [68]; therefore, many of the individuals within a species assessed today remain due to some level of resilience to stress. Overall, the susceptibility observed in this study across all species is indicative of future Caribbean coral reef assemblages composed only of the most tolerant individuals within a species, despite some species-level resilience to global change stressors.
Conclusions
As global change continues, it is critical to understand species-specific responses to ocean acidification and warming scenarios to predict the future of Caribbean reef assemblages, especially with a focus on now-dominant coral species explored here. Our results suggest that S. siderea may continue to dominate reefs across the Caribbean due to its maintenance of tissue energy reserves and relatively unaltered symbiosis with their algal symbionts under stress. Conversely, the previously assumed stress-tolerant species P. strigosa was unable to maintain any physiological traits under warming, suggesting that this species is now particularly vulnerable to thermal stress, which will likely lead to widespread bleaching and mortality. Finally, P. astreoides exhibited improved physiology under warming while ocean acidification caused reductions in the same physiological traits, indicating that this species may also fare better than others under global change. Although these species had variable responses under these global change scenarios, all three exhibited physiological deterioration under the effects of ocean acidification. Our results underscore the intricacies of coral physiology, both within and across species, in response to their environment and contribute to our understanding of the many ways that global change affects tropical coral reefs.
Supporting information
In situ satellite sea surface temperature.
Monthly MODIS satellite SST data from 2002 to 2021 for both the inshore (Port Honduras Marine Reserve; yellow) and the offshore (Sapodilla Cayes Marine Reserve; green) coral collection locations. Solid horizontal lines represent corresponding reef environment mean SST across duration. The blue dashed line represents the experimental control treatment temperature (28 C) and the red dashed line represents the experimental elevated temperature treatment (31 C). Note the temperature variability of the inshore site exceeding the offshore location. [Data accessibility: NASA OBPG. 2020. MODIS Aqua Global Level 3 Mapped SST. Ver. 2019.0. PO.DAAC, CA, USA. Dataset accessed [2021-02-02] at https://doi.org/10.5067/MODSA-MO4D9].
(TIFF)
Experimental design layout.
Diagram showing allocation of coral fragments for a single species throughout the experiment. Colour represents a different colony and shape represents reef environment. Four colonies (two from each reef environment) are reared within each tank (grey box), with three tanks comprising a treatment (white box). This is repeated for each pCO2 treatment at both temperatures. This same experimental design was used for all species. This figure is taken from Bove et al. 2019.
(TIFF)
Experimental seawater parameters.
Calculated and measured seawater parameters over the entire experimental period.
(TIFF)
Reef and treatment PCAs by species.
Principal component analysis (PCA) of all coral physiological parameters for S. siderea, P. strigosa, and P. astreoides depicted by natal reef environment (A-C; offshore green, inshore yellow) and the combination of pCO2 and temperature treatment (D-F). Arrows represent significant (p < 0.05) correlation vectors for physiological parameters and ellipses represent 95% confidence based on multivariate t-distributions.
(TIFF)
Measured physiological parameters per species.
Mean (±SE) physiological parameter (each row) measured for (A) S. siderea, (B) P. strigosa, and (C) P. astreoides at the completion of the 93-day experimental period. pCO2 treatment is represented along the x axis and the temperature is depicted by colour (28°C blue; 31°C red).
(TIFF)
PCAs by reef and treatment across all species.
Principal component analysis (PCA) comparing the physiology of all three species at the end of the experiment depicted by (A) reef environment and (B) combined pCO2 and temperature treatment. Arrows represent significant (p < 0.05) correlation vectors for physiological parameters and ellipses represent 95% confidence based on multivariate t-distributions.
(TIFF)
Coral images through time per species.
Coral colour changes over the experimental period. Representative images of fragments of (A) P. astreoides, (B) S. siderea, and (C) P. strigosa from the same colonies demonstrating change in coral colour over time in either control (420 μatm; 28°C) or warming (420 μatm; 31°C) treatments from the start of the experiment (T0) to the end (T90).
(TIFF)
PCAs of S. siderea host or symbiont physiology.
Principal component analysis (PCA) of S. siderea coral host (protein, lipid, carbohydrate; left) or algal symbiont (chlorophyll a, symbiont density, colour intensity; right) physiological parameters by temperature (28°C blue; 31°C red), pCO2 (pre industrial [300 μatm], light purple; current day [420 μatm], dark purple; end-of-century [680 μatm], light orange; extreme [3290 μatm], dark orange), and natal reef environment (offshore green; inshore yellow). Arrows represent significant (p < 0.05) correlation vectors for physiological parameters and ellipses represent 95% confidence based on multivariate t-distributions.
(TIFF)
PCAs of P. strigosa host or symbiont physiology.
Principal component analysis (PCA) of P. strigosa coral host (protein, lipid, carbohydrate; left) or algal symbiont (chlorophyll a, symbiont density, colour intensity; right) physiological parameters by temperature (28°C blue; 31°C red), pCO2 (pre industrial [300 μatm], light purple; current day [420 μatm], dark purple; end-of-century [680 μatm], light orange; extreme [3290 μatm], dark orange), and natal reef environment (offshore green; inshore yellow). Arrows represent significant (p < 0.05) correlation vectors for physiological parameters and ellipses represent 95% confidence based on multivariate t-distributions.
(TIFF)
PCAs of P. astreoides host or symbiont physiology.
Principal component analysis (PCA) of P. asteroides coral host (protein, lipid, carbohydrate; left) or algal symbiont (chlorophyll a, symbiont density, colour intensity; right) physiological parameters by temperature (28°C blue; 31°C red), pCO2 (pre industrial [300 μatm], light purple; current day [420 μatm], dark purple; end-of-century [680 μatm], light orange; extreme [3290 μatm], dark orange), and natal reef environment (offshore green; inshore yellow). Arrows represent significant (p < 0.05) correlation vectors for physiological parameters and ellipses represent 95% confidence based on multivariate t-distributions.
(TIFF)
Document containing supplemental tables A through G with captions referenced in the main text.
(PDF)
We thank the Belize Fisheries Department for all associated permits, the Toledo Institute for Development and Environment (TIDE) and the Southern Environmental Association (SEA) for their support. We also thank S. Patel, S. Swinea, F. Buckthal, J. Townsend, J. Boulton, and C. Lopazanski for assisting with preparing corals for physiological assays and the Marchetti, Septer, and Waters labs at UNC Chapel Hill for equipment and lab space use.
ReferencesGreveP, GudmundssonL, SeneviratneSI. Regional scaling of annual mean precipitation and water availability with global temperature change. . 2018;9: 227–240. doi: 10.5194/esd-9-227-2018DelworthTL, ZengF, VecchiGA, YangX, ZhangL, ZhangR. The North Atlantic Oscillation as a driver of rapid climate change in the Northern Hemisphere. . 2016;9: 509–512. doi: 10.1038/ngeo2738HabaryA, JohansenJL, NayTJ, SteffensenJF, RummerJL. Adapt, move or die–how will tropical coral reef fishes cope with ocean warming? . 2017;23: 566–577. doi: 10.1111/gcb.1348827593976MacLeanSA, BeissingerSR. Species’ traits as predictors of range shifts under contemporary climate change: A review and meta-analysis. . 2017;23: 4094–4105. doi: 10.1111/gcb.1373628449200BoveCB, MudgeL, BrunoJF. A century of warming on Caribbean reefs. . 2022;1: e0000002. doi: 10.1371/journal.pclm.0000002Hoegh-GuldbergO, MumbyPJ, HootenAJ, SteneckRS, GreenfieldP, GomezE, et al. Coral Reefs Under Rapid Climate Change and Ocean Acidification. . 2007;318: 1737–1742. doi: 10.1126/science.115250918079392KleypasJA. Climate change and tropical marine ecosystems: A review with an emphasis on coral reefs. . 2019;11: 24–35.KnowltonN.The future of coral reefs. . 2001;98: 5419–5425. doi: 10.1073/pnas.09109299811344288NagelkerkenI, ConnellSD. Global alteration of ocean ecosystem functioning due to increasing human CO2 emissions. . 2015;112: 13272–13277. doi: 10.1073/pnas.151085611226460052RiesJB, CohenAL, McCorkleDC. A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula. . 2010;29: 661–674. doi: 10.1007/s00338-010-0632-3AllemandD, TambuttéE, ZoccolaD, TambuttéS. Coral Calcification, Cells to Reefs. . 2010. pp. 119–150. doi: 10.1007/978-94-007-0114-4_9ComeauS, EdmundsPJ, SpindelNB, CarpenterRC. The responses of eight coral reef calcifiers to increasing partial pressure of CO2 do not exhibit a tipping point. . 2013;58: 388–398. doi: 10.4319/lo.2013.58.1.0388CrookED, CohenAL, Rebolledo-VieyraM, HernandezL, PaytanA. Reduced calcification and lack of acclimatization by coral colonies growing in areas of persistent natural acidification. . 2013;110: 11044–11049. doi: 10.1073/pnas.130158911023776217EnochsIC, ManzelloDP, CarltonR, SchopmeyerS, van HooidonkR, LirmanD. Effects of light and elevated pCO2 on the growth and photochemical efficiency of Acropora cervicornis. . 2014;33: 477–485. doi: 10.1007/s00338-014-1132-7KenkelCD, AlmanzaAT, MatzMV. Fine-scale environmental specialization of reef-building corals might be limiting reef recovery in the Florida Keys. . 2015;96: 3197–3212. doi: 10.1890/14-2297.126909426OkazakiRR, TowleEK, HooidonkR van, MorC, WinterRN, PiggotAM, et al. Species-specific responses to climate change and community composition determine future calcification rates of Florida Keys reefs. . 2017;23: 1023–1035. doi: 10.1111/gcb.1348127561209BoveCB, RiesJB, DaviesSW, WestfieldIT, UmbanhowarJ, CastilloKD. Common Caribbean corals exhibit highly variable responses to future acidification and warming. . 2019;286: 20182840. doi: 10.1098/rspb.2018.284030940056ManzelloDP, EnochsIC, KolodziejG, CarltonR. Coral growth patterns of Montastraea cavernosa and Porites astreoides in the Florida Keys: The importance of thermal stress and inimical waters. . 2015;471: 198–207. doi: 10.1016/j.jembe.2015.06.010RenegarD, RieglB. Effect of nutrient enrichment and elevated CO2 partial pressure on growth rate of Atlantic scleractinian coral Acropora cervicornis. . 2005;293: 69–76. doi: 10.3354/meps293069CohenA, HolcombM. Why Corals Care About Ocean Acidification: Uncovering the Mechanism. . 2009;22: 118–127. doi: 10.5670/oceanog.2009.102Von EuwS, ZhangQ, ManichevV, MuraliN, GrossJ, FeldmanLC, et al. Biological control of aragonite formation in stony corals. . 2017;356: 933–938. doi: 10.1126/science.aam637128572387MuscatineL, McCloskeyLR, MarianRE. Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration1. . 1981;26: 601–611. doi: 10.4319/lo.1981.26.4.0601GlynnPW. Coral reef bleaching: facts, hypotheses and implications. . 1996;2: 495–509. doi: 10.1111/j.1365-2486.1996.tb00063.xBrownBE. Coral bleaching: causes and consequences. . 1997;16: S129–S138. doi: 10.1007/s003380050249AnthonyKR, KlineDI, Diaz-PulidoG, DoveS, Hoegh-GuldbergO. Ocean acidification causes bleaching and productivity loss in coral reef builders. . 2008;105: 17442–17446. doi: 10.1073/pnas.080447810518988740SzmantAM, GassmanNJ. The effects of prolonged? bleaching? on the tissue biomass and reproduction of the reef coral Montastrea annularis. . 1990;8: 217–224. doi: 10.1007/BF00265014FittWK, McFarlandFK, WarnerME, ChilcoatGC. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. . 2000;45: 677–685. doi: 10.4319/lo.2000.45.3.0677BoveCB, WhiteheadRF, SzmantAM. Responses of coral gastrovascular cavity pH during light and dark incubations to reduced seawater pH suggest species-specific responses to the effects of ocean acidification on calcification. . 2020;39: 1675–1691. doi: 10.1007/s00338-020-01995-7LinZ, WangL, ChenM, ZhengX, ChenJ. Proteome and microbiota analyses characterizing dynamic coral-algae-microbe tripartite interactions under simulated rapid ocean acidification. . 2022;810: 152266. doi: 10.1016/j.scitotenv.2021.15226634896508SpeareL, DaviesSW, BalmonteJP, BaumannJ, CastilloKD. Patterns of environmental variability influence coral-associated bacterial and algal communities on the Mesoamerican Barrier Reef. . 2020;29: 2334–2348. doi: 10.1111/mec.1549732497352ZhangY, YangQ, LingJ, LongL, HuangH, YinJ, et al. Shifting the microbiome of a coral holobiont and improving host physiology by inoculation with a potentially beneficial bacterial consortium. . 2021;21: 130. doi: 10.1186/s12866-021-02167-533910503ZieglerM, SenecaFO, YumLK, PalumbiSR, VoolstraCR. Bacterial community dynamics are linked to patterns of coral heat tolerance. . 2017;8: 14213. doi: 10.1038/ncomms1421328186132RodriguesLJ, GrottoliAG. Energy reserves and metabolism as indicators of coral recovery from bleaching. . 2007;52: 1874–1882. doi: 10.4319/lo.2007.52.5.1874SchoepfV, GrottoliAG, WarnerME, CaiW-J, MelmanTF, HoadleyKD, et al. Coral Energy Reserves and Calcification in a High-CO2 World at Two Temperatures. . 2013;8: e75049. doi: 10.1371/journal.pone.007504924146747AichelmanHE, BoveCB, CastilloKD, BoultonJM, KnowltonAC, NievesOC, et al. Exposure duration modulates the response of Caribbean corals to global change stressors. . 2021;n/a: 1–16. doi: 10.1002/lno.11863TowleEK, EnochsIC, LangdonC. Threatened Caribbean Coral Is Able to Mitigate the Adverse Effects of Ocean Acidification on Calcification by Increasing Feeding Rate. . 2015;10: e0123394. doi: 10.1371/journal.pone.012339425874963ThornhillDJ, RotjanRD, ToddBD, ChilcoatGC, Iglesias-PrietoR, KempDW, et al. A Connection between Colony Biomass and Death in Caribbean Reef-Building Corals. . 2011;6: e29535. doi: 10.1371/journal.pone.002953522216307EdmundsPJ. Effect of pCO2 on the growth, respiration, and photophysiology of massive Porites spp. in Moorea, French Polynesia. . 2012;159: 2149–2160. doi: 10.1007/s00227-012-2001-yGuillermicM, CameronLP, CorteID, MisraS, BijmaJ, Beer D de, et al. Thermal stress reduces pocilloporid coral resilience to ocean acidification by impairing control over calcifying fluid chemistry. . 2021;7: eaba9958. doi: 10.1126/sciadv.aba995833523983FoxRJ, DonelsonJM, SchunterC, RavasiT, Gaitán-EspitiaJD. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. . 2019;374: 20180174. doi: 10.1098/rstb.2018.017430966962WarnerDA, DuW-G, GeorgesA. Introduction to the special issue-Developmental plasticity in reptiles: Physiological mechanisms and ecological consequences. . 2018;329: 153–161. doi: 10.1002/jez.219929956505ChevinL-M, LandeR, MaceGM. Adaptation, Plasticity, and Extinction in a Changing Environment: Towards a Predictive Theory. . 2010;8: e1000357. doi: 10.1371/journal.pbio.100035720463950ZieglerM, RoderCM, BüchelC, VoolstraCR. Limits to physiological plasticity of the coral Pocillopora verrucosa from the central Red Sea. . 2014;33: 1115–1129. doi: 10.1007/s00338-014-1192-8NorinT, MetcalfeNB. Ecological and evolutionary consequences of metabolic rate plasticity in response to environmental change. . 2019;374: 20180180. doi: 10.1098/rstb.2018.018030966964DarlingES, Alvarez‐FilipL, OliverTA, McClanahanTR, CôtéIM. Evaluating life-history strategies of reef corals from species traits. . 2012;15: 1378–1386. doi: 10.1111/j.1461-0248.2012.01861.x22938190BaumannJH, TownsendJE, CourtneyTA, AichelmanHE, DaviesSW, LimaFP, et al. Temperature Regimes Impact Coral Assemblages along Environmental Gradients on Lagoonal Reefs in Belize. PattersonHM, editor. . 2016;11: e0162098. doi: 10.1371/journal.pone.016209827606598BaumannJH, BoveCB, CarneL, GutierrezI, CastilloKD. Two offshore coral species show greater acclimatization capacity to environmental variation than nearshore counterparts in southern Belize. . 2021 [cited 7 Jul 2021]. doi: 10.1007/s00338-021-02124-8CastilloKD, RiesJB, BrunoJF, WestfieldIT. The reef-building coral Siderastrea siderea exhibits parabolic responses to ocean acidification and warming. . 2014;281: 20141856. doi: 10.1098/rspb.2014.185625377455Fox-KemperB, HewittHT, XiaoC, AðalgeirsdóttirG, DrijfhoutSS, EdwardsTL, et al. Ocean, cryosphere, and sea level change. In: Masson-DelmotteV, ZhaiP, PiraniA, ConnorsSL, PéanC, BergerS, et al., editors. . Cambridge University Press; 2021.AlemuJB, ClementY. Mass Coral Bleaching in 2010 in the Southern Caribbean. DiasJM, editor. . 2014;9: e83829. doi: 10.1371/journal.pone.008382924400078LewisJB, PriceWS. Feeding mechanisms and feeding strategies of Atlantic reef corals. . 1975;176: 527–544. doi: 10.1111/j.1469-7998.1975.tb03219.xRützler K, Macintyre IG. The Atlantic barrier reef ecosystem at Carrie Bow Cay, Belize, 1: Structure and Communities. 1982 [cited 19 Jul 2022]. Available: http://repository.si.edu/xmlui/handle/10088/1116.PierrotDE, WallaceDWR, LewisE. . Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tennessee.; 2006. Available: doi: 10.3334/CDIAC/otg.CO2SYS_XLS_CDIAC105aRoyRN, RoyLN, VogelKM, Porter-MooreC, PearsonT, GoodCE, et al. The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperatures 0 to 45°C. . 1993;44: 249–267. doi: 10.1016/0304-4203(93)90207-5MucciA.The solubility of calcite and aragonite in seawater at various salinities, temperatures, and one atmosphere total pressure. . 1983;283: 780–799. doi: 10.2475/ajs.283.7.780ParsonsTR, MaitaY, LalliCM. . 1st edition. Oxford Oxfordshire; New York: Pergamon Press; 1984.MasukoT, MinamiA, IwasakiN, MajimaT, NishimuraS-I, LeeYC. Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. . 2005;339: 69–72. doi: 10.1016/j.ab.2004.12.00115766712Bove CB, Baumann JH. Coral Carbohydrate Assay for 96-well plates. 2021 [cited 16 Jun 2021]. doi: 10.17504/protocols.io.bvb9n2r6FolchJ, LeesM, Sloane StanleyGH. A simple method for the isolation and purification of total lipides from animal tissues. . 1957;226: 497–509. 13428781Bove CB, Baumann JH. Coral Lipid Assay for 96-well plates. 2021 [cited 16 Jun 2021]. doi: 10.17504/protocols.io.bvcfn2tnChengY-S, ZhengY, VanderGheynstJS. Rapid quantitative analysis of lipids using a colorimetric method in a microplate format. . 2011;46: 95–103. doi: 10.1007/s11745-010-3494-021069472WintersG, HolzmanR, BlekhmanA, BeerS, LoyaY. Photographic assessment of coral chlorophyll contents: Implications for ecophysiological studies and coral monitoring. . 2009;380: 25–35. doi: 10.1016/j.jembe.2009.09.004Oksanen J, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package. Comprehensive R Archive Network (CRAN); 2020. Available: https://CRAN.R-project.org/package=vegan.Wright K. corrgram: Plot a Correlogram. Comprehensive R Archive Network (CRAN); 2018. Available: https://CRAN.R-project.org/package=corrgram.BarottKL, HuffmyerAS, DavidsonJM, LenzEA, MatsudaSB, HancockJR, et al. Coral bleaching response is unaltered following acclimatization to reefs with distinct environmental conditions. . 2021;118. doi: 10.1073/pnas.202543511834050025Mangiafico S. rcompanion: Functions to Support Extension Education Program Evaluation. 2021. Available: https://CRAN.R-project.org/package=rcompanion.JacksonEJ, DonovanM, CramerK, LamV. . Global Coral Reef Monitoring Network, IUCN, Gland, Switzerland; 2012 p. 306.AlvesC, ValdiviaA, AronsonRB, BoodN, CastilloKD, CoxC, et al. Twenty years of change in benthic communities across the Belizean Barrier Reef. . 2022;17: e0249155. doi: 10.1371/journal.pone.024915535041688CornwallCE, ComeauS, KornderNA, PerryCT, van HooidonkR, DeCarloTM, et al. Global declines in coral reef calcium carbonate production under ocean acidification and warming. . 2021;118: e2015265118. doi: 10.1073/pnas.201526511833972407WeisVM. The susceptibility and resilience of corals to thermal stress: adaptation, acclimatization or both? . 2010;19: 1515–1517. doi: 10.1111/j.1365-294X.2010.04575.x20456235HoadleyKD, LewisAM, WhamDC, PettayDT, GrassoC, SmithR, et al. Host–symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress. . 2019;9: 9985. doi: 10.1038/s41598-019-46412-431292499RippeJP, BaumannJH, LeenerDND, AichelmanHE, FriedlanderEB, DaviesSW, et al. Corals sustain growth but not skeletal density across the Florida Keys Reef Tract despite ongoing warming. . 2018;24: 5205–5217. doi: 10.1111/gcb.1442230102827ScheufenT, KrämerWE, Iglesias-PrietoR, EnríquezS. Seasonal variation modulates coral sensibility to heat-stress and explains annual changes in coral productivity. . 2017;7: 4937. doi: 10.1038/s41598-017-04927-828694432HughesTP, KerryJT, BairdAH, ConnollySR, DietzelA, EakinCM, et al. Global warming transforms coral reef assemblages. . 2018;556: 492–496. doi: 10.1038/s41586-018-0041-229670282EakinCM, MorganJA, HeronSF, SmithTB, LiuG, Alvarez-FilipL, et al. Caribbean Corals in Crisis: Record Thermal Stress, Bleaching, and Mortality in 2005. . 2010;5. doi: 10.1371/journal.pone.001396921125021GreenD, EdmundsP, CarpenterR. Increasing relative abundance of Porites astreoides on Caribbean reefs mediated by an overall decline in coral cover. . 2008;359: 1–10. doi: 10.3354/meps07454VentiA, AnderssonA, LangdonC. Multiple driving factors explain spatial and temporal variability in coral calcification rates on the Bermuda platform. . 2014;33: 979–997. doi: 10.1007/s00338-014-1191-9NealBP, KhenA, TreibitzT, BeijbomO, O’ConnorG, CoffrothMA, et al. Caribbean massive corals not recovering from repeated thermal stress events during 2005–2013. . 2017;7: 1339–1353. doi: 10.1002/ece3.270628261447EdmundsPJ, BrownD, MoriartyV. Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea, French Polynesia. . 2012;18: 2173–2183. doi: 10.1111/j.1365-2486.2012.02695.xHorvathKM, CastilloKD, ArmstrongP, WestfieldIT, CourtneyT, RiesJB. Next-century ocean acidification and warming both reduce calcification rate, but only acidification alters skeletal morphology of reef-building coral Siderastrea siderea. . 2016;6: 29613. doi: 10.1038/srep2961327470426PradaF, CaroselliE, MengoliS, BriziL, FantazziniP, CapaccioniB, et al. Ocean warming and acidification synergistically increase coral mortality. . 2017;7: 40842. doi: 10.1038/srep4084228102293TimmersMA, JuryCP, VicenteJ, BahrKD, WebbMK, ToonenRJ. Biodiversity of coral reef cryptobiota shuffles but does not decline under the combined stressors of ocean warming and acidification. . 2021;118: e2103275118. doi: 10.1073/pnas.210327511834544862PörtnerHO, BennettAF, BozinovicF, ClarkeA, LardiesMA, LucassenM, et al. Trade-offs in thermal adaptation: the need for a molecular to ecological integration. . 2006;79: 295–313. doi: 10.1086/49998616555189CampEF, SchoepfV, MumbyPJ, HardtkeLA, Rodolfo-MetalpaR, SmithDJ, et al. The Future of Coral Reefs Subject to Rapid Climate Change: Lessons from Natural Extreme Environments. . 2018;5. doi: 10.3389/fmars.2018.00004PutnamHM, DavidsonJM, GatesRD. Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. . 2016;9: 1165–1178. doi: 10.1111/eva.1240827695524TambuttéE, VennAA, HolcombM, SegondsN, TecherN, ZoccolaD, et al. Morphological plasticity of the coral skeleton under CO 2 -driven seawater acidification. . 2015;6: 7368. doi: 10.1038/ncomms836826067341DeWittTJ, SihA, WilsonDS. Costs and limits of phenotypic plasticity. . 1998;13: 77–81. doi: 10.1016/s0169-5347(97)01274-321238209KenkelCD, MatzMV. Gene expression plasticity as a mechanism of coral adaptation to a variable environment. . 2016;1: 1–6. doi: 10.1038/s41559-016-001428812568SeebacherF, DucretV, LittleAG, AdriaenssensB. Generalist–specialist trade-off during thermal acclimation. . 2015;2: 140251. doi: 10.1098/rsos.14025126064581AnthonyKR, ConnollySR, WillisBL. Comparative analysis of energy allocation to tissue and skeletal growth in corals. . 2002;47: 1417–1429. doi: 10.4319/lo.2002.47.5.1417GnaigerE, BitterlichG. Proximate biochemical composition and caloric content calculated from elemental CHN analysis: a stoichiometric concept. . 1984;62: 289–298. doi: 10.1007/BF0038425928310880AnthonyKR, FabriciusKE. Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. . 2000;252: 221–253. doi: 10.1016/s0022-0981(00)00237-910967335JonesR.Changes in zooxanthellar densities and chlorophyll concentrations in corals during and after a bleaching event. . 1997;158: 51–59. doi: 10.3354/meps158051TaylorFJR, editor. Photosynthetic physiology of dinoflagellates. 1st edition. . 1st edition. Oxford; Boston: Wiley-Blackwell; 1991. pp. 174–223.LaJeunesseTC. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. . 2002;141: 387–400. doi: 10.1007/s00227-002-0829-2LaJeunesseTC, ParkinsonJE, GabrielsonPW, JeongHJ, ReimerJD, VoolstraCR, et al. Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts. . 2018;28: 2570–2580.e6. doi: 10.1016/j.cub.2018.07.00830100341SuggettDJ, WarnerME, SmithDJ, DaveyP, HennigeS, BakerNR. Photosynthesis and Production of Hydrogen Peroxide by Symbiodinium (pyrrhophyta) Phylotypes with Different Thermal Tolerances1. . 2008;44: 948–956. doi: 10.1111/j.1529-8817.2008.00537.x27041613GrégoireV, SchmackaF, CoffrothMA, KarstenU. Photophysiological and thermal tolerance of various genotypes of the coral endosymbiont Symbiodinium sp. (Dinophyceae). . 2017;29: 1893–1905. doi: 10.1007/s10811-017-1127-1BairdAH, BhagooliR, RalphPJ, TakahashiS. Coral bleaching: the role of the host. . 2009;24: 16–20. doi: 10.1016/j.tree.2008.09.00519022522ColesSL, BrownBE. Coral bleaching—capacity for acclimatization and adaptation. . 2003;46: 183–223. doi: 10.1016/s0065-2881(03)46004-514601413HiiY-S, Ambok BolongAM, YangT-T, LiewH-C. Effect of Elevated Carbon Dioxide on Two Scleractinian Corals: Porites cylindrica (Dana, 1846) and Galaxea fascicularis (Linnaeus, 1767). . 2009;2009: 1–7. doi: 10.1155/2009/215196CrawleyA, KlineDI, DunnS, AnthonyKR, DoveS. The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. . 2010;16: 851–863. doi: 10.1111/j.1365-2486.2009.01943.xDaviesSW, RiesJB, MarchettiA, CastilloKD. Symbiodinium Functional Diversity in the Coral Siderastrea siderea Is Influenced by Thermal Stress and Reef Environment, but Not Ocean Acidification. . 2018;5. doi: 10.3389/fmars.2018.00150BakerAC. Reef corals bleach to survive change. . 2001;411: 765–766. doi: 10.1038/3508115111459046CunningR, BakerAC. Thermotolerant coral symbionts modulate heat stress-responsive genes in their hosts. . 2020;29: 2940–2950. doi: 10.1111/mec.1552632585772WooldridgeSA. Is the coral-algae symbiosis really ‘mutually beneficial’ for the partners? . 2010;32: 615–625. doi: 10.1002/bies.20090018220517874BakerDM, FreemanCJ, WongJCY, FogelML, KnowltonN. Climate change promotes parasitism in a coral symbiosis. . 2018;12: 921–930. doi: 10.1038/s41396-018-0046-829379177FabriciusK, LangdonC, UthickeS, HumphreyC, NoonanS, De’athG, et al. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. . 2011;1: 165–169. doi: 10.1038/nclimate1122van WoesikR, SakaiK, GanaseA, LoyaY. Revisiting the winners and the losers a decade after coral bleaching. . 2011;434: 67–76. doi: 10.3354/meps09203KenkelCD, MeyerE, MatzMV. Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments. . 2013;22: 4322–4334. doi: 10.1111/mec.1239023899402BurriesciMS, RaabTK, PringleJR. Evidence that glucose is the major transferred metabolite in dinoflagellate–cnidarian symbiosis. . 2012;215: 3467–3477. doi: 10.1242/jeb.07094622956249Young SDO’Connor JD, Muscatine L. Organic material from scleractinian coral skeletons—II. Incorporation of 14C into protein, chitin and lipid. . 1971;40: 945–958. doi: 10.1016/0305-0491(71)90040-XWallCB, MasonRAB, EllisWR, CunningR, GatesRD. Elevated p CO 2 affects tissue biomass composition, but not calcification, in a reef coral under two light regimes. . 2017;4: 170683. doi: 10.1098/rsos.17068329291059EdmundsPJ, DiddenC, FrankK. Over three decades, a classic winner starts to lose in a Caribbean coral community. . 2021;12: e03517. doi: 10.1002/ecs2.351710.1371/journal.pone.0273897.r001Decision Letter 0MayfieldAnderson B.Academic Editor2022Anderson B. MayfieldThis is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Submission Version0
17 May 2022
PONE-D-22-07335Global change differentially modulates Caribbean coral physiology and suggests future ‘winners’ and ‘losers’PLOS ONE
Dear Dr. Bove,
Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.
ACADEMIC EDITOR:Hello,
I have now had this article reviewed by two experts in the field. Although one was more favorable, the other necessitated a "major revision." I think most of the comments can be adequately addressed and so I am optimistic that this work can ultimately be published in PLoS ONE upon accommodating them. Looking forward to seeing the revised version in the coming weeks. Anderson
Please submit your revised manuscript by Jul 01 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.
Please include the following items when submitting your revised manuscript:
A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.
If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.
If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.
We look forward to receiving your revised manuscript.
Kind regards,
Anderson B. Mayfield, Ph.D.
Academic Editor
PLOS ONE
Journal Requirements:
When submitting your revision, we need you to address these additional requirements.
1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at
https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and
2. Thank you for stating the following in the Acknowledgments Section of your manuscript:
“This research was partially supported by the Women Diver Hall of Fame Sea of Change Foundation Marine Conservation Scholarship and Lerner-Gray Memorial Fund of the American Museum of Natural History Grants for Marine Research awarded to CBB. JBR acknowledges support from NSF BIO-OCE award #1437371.”
We note that you have provided additional information within the Acknowledgements Section that is not currently declared in your Funding Statement. Please note that funding information should not appear in the Acknowledgments section or other areas of your manuscript. We will only publish funding information present in the Funding Statement section of the online submission form.
Please remove any funding-related text from the manuscript and let us know how you would like to update your Funding Statement. Currently, your Funding Statement reads as follows:
“This research was partially supported by the Women Diver Hall of Fame Sea of Change Foundation Marine Conservation Scholarship (https://www.wdhof.org/scholarship/marine-conservation-scholarship-graduate) and Lerner-Gray Memorial Fund of the American Museum of Natural History Grants for Marine Research (https://www.amnh.org/research/richard-gilder-graduate-school/academics-and-research/fellowship-and-grant-opportunities/research-grants-and-graduate-student-exchange-fellowships/the-lerner-gray-fund-for-marine-research) awarded to CBB. JBR acknowledges support from NSF BIO-OCE award #1437371 (https://www.nsf.gov/geo/oce/programs/biores.jsp). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.”
Please include your amended statements within your cover letter; we will change the online submission form on your behalf.
3. Your ethics statement should only appear in the Methods section of your manuscript. If your ethics statement is written in any section besides the Methods, please move it to the Methods section and delete it from any other section. Please ensure that your ethics statement is included in your manuscript, as the ethics statement entered into the online submission form will not be published alongside your manuscript.
4. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information.
Additional Editor Comments:
Hello,
I have now had this article reviewed by two experts in the field. Although one was more favorable, the other necessitated a "major revision." I think most of the comments can be adequately addressed and so I am optimistic that this work can ultimately be published in PLoS ONE upon accommodating them. Looking forward to seeing the revised version in the coming weeks. Anderson
[Note: HTML markup is below. Please do not edit.]
Reviewers' comments:
Reviewer's Responses to Questions
Comments to the Author
1. Is the manuscript technically sound, and do the data support the conclusions?
The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.
Reviewer #1: Yes
Reviewer #2: Partly
**********
2. Has the statistical analysis been performed appropriately and rigorously?
Reviewer #1: Yes
Reviewer #2: Yes
**********
3. Have the authors made all data underlying the findings in their manuscript fully available?
The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.
Reviewer #1: Yes
Reviewer #2: Yes
**********
4. Is the manuscript presented in an intelligible fashion and written in standard English?
PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.
Reviewer #1: Yes
Reviewer #2: Yes
**********
5. Review Comments to the Author
Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)
Reviewer #1: Specific comments
It is important to understand the physiological effects of warming and acidification on coral and symbiotic algae. By this way, to understand the varied responses of the different symbiotic partners is critical for predicting the future of tropical coral reefs. This manuscript assess the physiological responses of three species of Caribbean corals come from inshore and offshore environments, and then independent and combined test under four ocean acidification conditions and two warming temperatures, with a long time experiments. These results help us understand the physiological responses and relationship between some species of corals and symbiotic algae under warming and acidification. And it require more investigation in multi-stressor, multi-species studies to explore these complexities of coral responses under global change.
There are still some questions about this manuscript. Are the morphology of the three corals the same (such as massive, branching...)? And will different morphology influences the response of physiological effects of warming and acidification on coral and symbiotic algae? In this experiments, the energy of coral completely came from the symbiotic algae. Will the physiological effects on corals and symbiotic algae keep the same or change if the coral get energy by feeding (heterotroph) under warming and acidification in field?
General comments
Comments while reading
Methods
Page 6. The authors did not describe or cite any references about how to control the PCO2 in the four CO2 treatments. How to create the pre-industrial CO2 condition and maintain it?
Page 9, line 226-228. How to see “no interactions” from S2 Table?
line 237. It suggests to use the full name, not the abbreviation in first time to mention noun. It replaces “ all PCs calculated above as… “ as “all Principal compound analysis (PCs) calculated above as …”.
Results
Page 11, line 266-267, 275, 285-286. How to read no significant interactive effect between temperature and pCO2 from S2 Table? Are the Fig S3D (DIC), S3E (HCO3), and S3F (CO2 seawater) cite here correct?
Page 11-12, line 289-297. The Figure 1 had A to F figures, however, the description only for A to C, without D to F. The figure reveal the symbol “sum”, the figure caption describe as sum/red = colour intensity. It is recommended to use uniform notation.
Discussion
Page 16-17, line 426-427. How to see “no interactions” from S2, S3, S8 Table?
Supplemental Materials for manuscript
S5 Table. I may confuse the results of S. sidera analysis. Did S. sidereal results only in offshore analysis, without any inshore analysis?
Reviewer #2: This paper studies the physiological response of three Caribbean coral species to two individually and combined global stressors (warming and acidification). Multiple physiological parameters in the corals are assessed using multidimensional analysis. Based on these data, the response of the coral species as well as 2 locations (inshore and offshore) are compared. The study includes a comprehensive amount of data on coral physiology that are of great value to understand the physiological response of these coral species to global stressors.
The paper could benefit from addressing in a more clear way (1) the ecological relevance of the experimental treatments and whether they reflect values that are relevant to Caribbean reefs, and (2) what the observed changes in physiology mean for the future of these coral species. In general, my main concern with the study is that the multivariable approach obscures the specific effects of the treatments on these corals species (or the lack of effects) and makes it harder to understand the implication of the stressors on the individual corals species and on the reefs of the future.
Specific comments:
Abstract: It would be useful to immediately introduce what species are considered “winners” or “losers” and why. Since “winners” and “losers” are in the title, it is expected to report this as the main result.
The introduction includes a nice description of the physiological parameters studied and how they have been seen to be affected by environmental stressors. This is very useful.
Results of previous studies about the relative susceptibility of Caribbean coral species to the stressors would be useful to offer some context. What species are becoming less or more abundant in locations that have experienced intense warming or OA?
Also, the introduction could benefit from including some context for the meaning and implications of physiological “plasticity”. In this paper, higher plasticity is assumed to imply higher susceptibility to environmental conditions. This should be better supported by adding some references to understand the results.
Methods: Generally, well organized. The authors provide enough details to understand the study and statistical analysis.
Lines 115 and 116 can be mentioned at the end of the paragraph for people that want more details, but perhaps these are not the best lines to start describing the study.
Lines 135-140 could become a table with the factorial CO2 and temperature conditions. From lines 135 to 138 it is not clear why 2 different values are presented for every CO2 treatment.
Line 200 mentioned that the images were analyzed for each timepoint, but I do not think there is a previous mention of when the time points are.
Lines 215-219. If mortality was 90-72% how many samples per coral species per treatment were actually analyzed? These numbers are more important than the 288 total samples reported in lines 130, if most of these 288 corals died before the physiological data was collected (tissue samples).
Results
The PCA section is clear and well organized. However, better organization of figure 1 is possible. For example, if different shapes are used for the CO2 treatments, colors can be used for the temperature (or vice versa) and then the top and bottom panels do not have to be duplicated. Since this is a fully factorial study it is perhaps better to visualize both treatment levels in one same panel.
In general, there are too many mentions to the supplementary information (Tables and Figures) in the results and discussion section. Is this necessary? It gives the feeling that half of the paper is actually not in the paper.
Lines 305-306. It is expected to have a strong correlation between symbiont density and Chl-a. Even more, I think you can argue that this variables are not independent and therefore you should include only one in your model. A more interesting and less redundant variable could be Chl-a content per Symbiont cell, and drop total Chl-a.
Discussion
Please elaborate some about how the studied treatments reflect the present or future conditions of these Caribbean corals.
Lines 449-450: Please provide some citations and explain how plasticity could be a detrimental response to stressors. Plasticity (Figure 3) is a big part of the discussion, but the negative connotation given to more plastic responses should be explained. Similarly, lines 455-457 could use references that support reduced capacity of corals with higher plasticity to persist under climate change scenarios.
Lines 490 and 524: photosynthetic efficiency was not presented as part of the data. Was it measured?
Small comments:
Writing style: “clearly” is used multiple times across the manuscript. This can be removed from most of the sentences and let the reader decide if something is clear based on the data. e.g., Line 395 could be: “pCO2 treatment drove differences in coral physiology” instead of “pCO2 treatment clearly drove differences in coral physiology”.
Lines 479-481 are repeated in the manuscript.
Thank you for making your data and code available.
**********
6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.
If you choose “no”, your identity will remain anonymous but your review may still be made public.
Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.
Reviewer #1: No
Reviewer #2: No
[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]
While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.
10.1371/journal.pone.0273897.r002Author response to Decision Letter 0Submission Version1
9 Jun 2022
Journal Requirements:
1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at
https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and
Response: We have updated our manuscript to meet PLOS ONE’s style requirements as requested.
2. Thank you for stating the following in the Acknowledgments Section of your manuscript:
“This research was partially supported by the Women Diver Hall of Fame Sea of Change Foundation Marine Conservation Scholarship and Lerner-Gray Memorial Fund of the American Museum of Natural History Grants for Marine Research awarded to CBB. JBR acknowledges support from NSF BIO-OCE award #1437371.”
We note that you have provided additional information within the Acknowledgements Section that is not currently declared in your Funding Statement. Please note that funding information should not appear in the Acknowledgments section or other areas of your manuscript. We will only publish funding information present in the Funding Statement section of the online submission form.
Please remove any funding-related text from the manuscript and let us know how you would like to update your Funding Statement. Currently, your Funding Statement reads as follows:
“This research was partially supported by the Women Diver Hall of Fame Sea of Change Foundation Marine Conservation Scholarship (https://www.wdhof.org/scholarship/marine-conservation-scholarship-graduate) and Lerner-Gray Memorial Fund of the American Museum of Natural History Grants for Marine Research (https://www.amnh.org/research/richard-gilder-graduate-school/academics-and-research/fellowship-and-grant-opportunities/research-grants-and-graduate-student-exchange-fellowships/the-lerner-gray-fund-for-marine-research) awarded to CBB. JBR acknowledges support from NSF BIO-OCE award #1437371 (https://www.nsf.gov/geo/oce/programs/biores.jsp). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.”
Please include your amended statements within your cover letter; we will change the online submission form on your behalf.
Response: We have removed the funding information from the text of the manuscript and the current funding statement should suffice.
3. Your ethics statement should only appear in the Methods section of your manuscript. If your ethics statement is written in any section besides the Methods, please move it to the Methods section and delete it from any other section. Please ensure that your ethics statement is included in your manuscript, as the ethics statement entered into the online submission form will not be published alongside your manuscript.
Response: We have added the following ethics statement to the methods section: “All corals were collected following local laws and regulations with appropriate permits (#5674).”
4. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information.
Response: We have added these captions for all supporting information at the end of the main text as requested and updated the in-text citations.
Review Comments to the Author
Reviewer #1:
Specific comments
It is important to understand the physiological effects of warming and acidification on coral and symbiotic algae. By this way, to understand the varied responses of the different symbiotic partners is critical for predicting the future of tropical coral reefs. This manuscript assess the physiological responses of three species of Caribbean corals come from inshore and offshore environments, and then independent and combined test under four ocean acidification conditions and two warming temperatures, with a long time experiments. These results help us understand the physiological responses and relationship between some species of corals and symbiotic algae under warming and acidification. And it require more investigation in multi-stressor, multi-species studies to explore these complexities of coral responses under global change.
There are still some questions about this manuscript. Are the morphology of the three corals the same (such as massive, branching...)? And will different morphology influences the response of physiological effects of warming and acidification on coral and symbiotic algae? In this experiments, the energy of coral completely came from the symbiotic algae. Will the physiological effects on corals and symbiotic algae keep the same or change if the coral get energy by feeding (heterotroph) under warming and acidification in field?
Response: We thank the reviewer for taking time to review our manuscript and provide helpful feedback to improve it. We have addressed your comments and provided clarity on some of your concerns throughout the manuscript. The morphology of all three coral species can be classified as mounding so we do not anticipate differences in morphology to have an impact on the responses of these species. This is important information and therefore we clarified that these are all mounding coral species in the introduction.
Lines 118-121 now state: “These coral species were selected because they represent both weedy (P. astreoides) and stress-tolerant (S. siderea and P. strigosa) life histories [38], possess similar growth morphologies (mounding), and are common throughout the Caribbean.”
In regards to your comment on feeding of the corals in this experiment, the corals were fed throughout the experiment to support heterotrophy, however, this was not stated in the methods text and we appreciate the reviewer pointing this out. We have now added the following clarifying statement into the Experimental design section of the Methods:
Lines 169-170 now state: “Corals were fed a combination of frozen adult Artemia sp. and newly hatched Artemia sp. every other day to satisfy heterotrophic feeding.”
Methods
Page 6. The authors did not describe or cite any references about how to control the PCO2 in the four CO2 treatments. How to create the pre-industrial CO2 condition and maintain it?
Response: We have now added the following statement into the methods to describe how we achieved pCO2 treatments.
Lines 158-161 now state: “High-precision digital solenoid-valve mass flow controllers (Aalborg Instruments and Controls; Orangeburg, NY, USA) were used to bubble air alone (control pCO2 conditions), or in combination with CO2-free air (pre-industrial conditions) or CO2 gas (end-of-century and extreme conditions) to achieve gas mixtures of each desired pCO2 condition.”
Page 9, line 226-228. How to see “no interactions” from S2 Table?
Response: We agree this was unclear so we have clarified this statement.
Lines 252-254 now state: "The additive model resulted in a lower AIC than the fully interactive model for all species, so interaction terms were dropped from each model resulting in fully additive models (see S2 Table)."
line 237. It suggests to use the full name, not the abbreviation in first time to mention noun. It replaces “ all PCs calculated above as… “ as “all Principal compound analysis (PCs) calculated above as …”.
Response: We have updated this to use the full name (principal components) instead of just the abbreviation here.
Results
Page 11, line 266-267, 275, 285-286. How to read no significant interactive effect between temperature and pCO2 from S2 Table? Are the Fig S3D (DIC), S3E (HCO3), and S3F (CO2 seawater) cite here correct?
Response: We have clarified this statement as recommended above. We did incorrectly reference S3D Fig in the supplements, when we meant to reference S4D and we thank the reviewer for noticing this.
Page 11-12, line 289-297. The Figure 1 had A to F figures, however, the description only for A to C, without D to F. The figure reveal the symbol “sum”, the figure caption describe as sum/red = colour intensity. It is recommended to use uniform notation.
Response: We thank the reviewer for highlighting the mistake in our figure caption, which was missing several labels and we have now fixed the caption text. In addition, we have fixed the colour label as requested so now all PC loadings use 'colour'
Discussion
Page 16-17, line 426-427. How to see “no interactions” from S2, S3, S8 Table?
Response: We reference these tables because these represent our model selection process and highlight that we do not identify significant interaction terms in any of our models. However, at the request of Reviewer 2, we have removed this reference to reduce the number of references to the supplemental materials.
Supplemental Materials for manuscript
S5 Table. I may confuse the results of S. sidera analysis. Did S. sidereal results only in offshore analysis, without any inshore analysis?
Response: The analysis of S. siderea was the only one to include reef environment in the model, but both reef environments were included in the analysis. The intercept coefficient for S. siderea represents inshore fragments for comparison across other coefficients. This is highlighted in the figure caption to assist the reader.
Reviewer #2:
This paper studies the physiological response of three Caribbean coral species to two individually and combined global stressors (warming and acidification). Multiple physiological parameters in the corals are assessed using multidimensional analysis. Based on these data, the response of the coral species as well as 2 locations (inshore and offshore) are compared. The study includes a comprehensive amount of data on coral physiology that are of great value to understand the physiological response of these coral species to global stressors.
The paper could benefit from addressing in a more clear way (1) the ecological relevance of the experimental treatments and whether they reflect values that are relevant to Caribbean reefs, and (2) what the observed changes in physiology mean for the future of these coral species. In general, my main concern with the study is that the multivariable approach obscures the specific effects of the treatments on these corals species (or the lack of effects) and makes it harder to understand the implication of the stressors on the individual corals species and on the reefs of the future.
Response: We thank the reviewer for taking their time to review this manuscript and provide very helpful feedback that has improved our manuscript. We especially thank the reviewer for also highlighting things they appreciated about our manuscript in addition to highlighting areas for improvement.
Specific comments:
Abstract: It would be useful to immediately introduce what species are considered “winners” or “losers” and why. Since “winners” and “losers” are in the title, it is expected to report this as the main result.
Response: We have now added the following statement into the abstract.
Lines 43-46 now state: “Further, our study identifies S. siderea and P. astreoides as potential ‘winners’ on future Caribbean coral reefs due to their resilience under projected global change stressors, while P. strigosa will likely be a ‘loser’ due to their sensitivity to thermal stress events.”
The introduction includes a nice description of the physiological parameters studied and how they have been seen to be affected by environmental stressors. This is very useful.
Response: Thank you!
Results of previous studies about the relative susceptibility of Caribbean coral species to the stressors would be useful to offer some context. What species are becoming less or more abundant in locations that have experienced intense warming or OA?
Response: We have added several statements about Caribbean species under these stressors into the intro:
Lines 63-67 now state: “For example, the Caribbean coral species Siderastrea siderea and Porites astreoides have been shown previously to maintain higher growth rates under ocean acidification and/or warming stress, [16–18] and other species, such as Orbicella faveolata and Acropora cervicornis, generally exhibited reduced growth under these same stressors [14,18,19].”
Lines 118-122 now state: “These coral species were selected because they represent both weedy (P. astreoides) and stress-tolerant (S. siderea and P. strigosa) life histories [45], possess similar growth morphologies (mounding), and are common throughout the Caribbean. These coral species are common throughout the Caribbean and can be found across a variety of environmental gradients.”
Also, the introduction could benefit from including some context for the meaning and implications of physiological “plasticity”. In this paper, higher plasticity is assumed to imply higher susceptibility to environmental conditions. This should be better supported by adding some references to understand the results.
Response: We have now added the following paragraph into the introduction to provide a bit more context about physiological plasticity
Lines 101-112 now state: “Many symbiotic corals also have the capacity to exhibit physiological plasticity (i.e., modification of an organism’s physiology) in response to changing environments that may be employed under global change scenarios [38,39]. While plasticity is often highlighted as a mechanism for rapid response to changing environments, there is still debate about whether plasticity alone is enough to ensure species persistence under global change [40]. Indeed, a highly plastic coral may be able to modulate its physiology (e.g., increase chlorophyll a per symbiont cell) under an acute stress event (e.g., low light levels) [41], but this is likely to come at a cost to another metabolic process, such as energy stores. This physiological cost can be beneficial for the coral in the short term, however, may eventually result in a decline in fitness [40,42], especially in long-lived organisms like reef-building corals. These potential trade-offs in reef-building corals remain poorly understood and highlight the complexities of plasticity as a mode of global change resilience.”
Methods
Generally, well organized. The authors provide enough details to understand the study and statistical analysis.
Response: Thank you!
Lines 115 and 116 can be mentioned at the end of the paragraph for people that want more details, but perhaps these are not the best lines to start describing the study.
Response: We have moved this sentence to the end of the paragraph as requested.
Lines 135-140 could become a table with the factorial CO2 and temperature conditions. From lines 135 to 138 it is not clear why 2 different values are presented for every CO2 treatment.
Response: We have now added the below table to the main text to describe the experimental treatments (Table 1). Regarding the two different values, because temperature affects the solubility of CO2 in seawater, the two temperature treatments averaged different carbonate parameters for each of the pCO2 treatments, despite being sparged with the same gas mixture ratios.
Table 1. Warming and acidification treatment means and standard deviations.
Line 200 mentioned that the images were analyzed for each timepoint, but I do not think there is a previous mention of when the time points are.
Response: Thank you for catching this, we have clarified this statement in the text
Lines 225-226 now state: “Coral color intensity was also analysed from images of every fragment with standardized color scales taken every 30 days throughout the experiment.”
Lines 215-219. If mortality was 90-72% how many samples per coral species per treatment were actually analyzed? These numbers are more important than the 288 total samples reported in lines 130, if most of these 288 corals died before the physiological data was collected (tissue samples).
Response: We have updated this statement to report the total number of analyzed fragments per species.
Lines 241-245 now state: “Sample mortality was observed throughout the experimental period across species as described in Bove et al. [17] and thus some treatments resulted in reduced replication for physiological analyses (Table A in S1 Text). Overall, S. siderea exhibited nearly 90% survival (86 total fragments), P. strigosa exhibited 80% survival (77 total fragments), and P. astreoides exhibited 72% survival (69 total fragments) at the end of the experiment [17].”
Results
The PCA section is clear and well organized. However, better organization of figure 1 is possible. For example, if different shapes are used for the CO2 treatments, colors can be used for the temperature (or vice versa) and then the top and bottom panels do not have to be duplicated. Since this is a fully factorial study it is perhaps better to visualize both treatment levels in one same panel.
Response: We appreciate this recommendation for this figure and have condensed the 6-panel figure into 3 (one PCA per species). Since S. siderea and P. astreoides were mostly explained by pCO2 treatment, these data are coloured by pCO2 treatment, while P. strigosa was driven by temperature treatment so we used colour to represent this pattern.
In general, there are too many mentions to the supplementary information (Tables and Figures) in the results and discussion section. Is this necessary? It gives the feeling that half of the paper is actually not in the paper.
Response: While we understand the reviewer’s comment about referencing the supplemental materials, we feel that the materials in the supplemental document are necessary. These tables and figures represent analyses and visualisations we explored to support our overall conclusions from our study. We want to be transparent about the different ways we explored our data but also maintain the manuscript figures succinct and easy to digest. We have removed some duplicate references to the supplemental materials in an effort to reduce the feeling that most of the paper is missing.
Lines 305-306. It is expected to have a strong correlation between symbiont density and Chl-a. Even more, I think you can argue that this variables are not independent and therefore you should include only one in your model. A more interesting and less redundant variable could be Chl-a content per Symbiont cell, and drop total Chl-a.
Response: We chose to include both symbiont density and chlorophyll a in these correlation analyses to compare the correlations across all parameters to see how they change between species. For example, we report a strong correlation between these parameters in S. siderastrea (R2 = 0.72), while these parameters are not highly correlated in P. astreoides (R2 = 0.20). Further, we considered the chla/cell assessment, however, this metric produces concerning values when measuring low symbiont counts (i.e., in bleached P. strigosa) where chlorophyll a was still present, but counts were very low (see below figure where this is depicted). For this reason, we decided to measure these parameters individually and discuss the implications of high density or chlorophyll content for the coral.
Discussion
Please elaborate some about how the studied treatments reflect the present or future conditions of these Caribbean corals.
Response: We have provided these details within the methods section.
Lines 153-158 now state: “The eight treatments encompassed four pCO2 treatments (Table 1) corresponding to pre-industrial, current-day (pCO2 control), moderate end-of-century, and an extreme pCO2 level all crossed with two temperatures (Table 1) corresponding to the corals’ approximate present-day summer mean (28°C ±0.4) and projected end-of-century summer warming (31°C ±0.4) [49] that has also been observed to induce bleaching in these species [50].”
Lines 449-450: Please provide some citations and explain how plasticity could be a detrimental response to stressors. Plasticity (Figure 3) is a big part of the discussion, but the negative connotation given to more plastic responses should be explained. Similarly, lines 455-457 could use references that support reduced capacity of corals with higher plasticity to persist under climate change scenarios.
Response: We have added additional references to support our statements as requested. Additionally, we have explained our rationale behind our conclusions here further.
Lines 476-480 now state: “However, physiological plasticity may not always be beneficial long term and may instead signal a shift in organism condition [18,42,44]. Organisms exhibiting higher plasticity in response to environmental change (e.g., ocean warming and acidification) may incur a physiological cost in the form of a trade-off that ultimately may impact the population’s ability to resist future change [40–42].”
Lines 490 and 524: photosynthetic efficiency was not presented as part of the data. Was it measured?
Response: This was not assessed here and we have clarified the statement in the text since this was in reference to chlorophyll a content.
Lines 517-520 now state: “This pattern suggests P. strigosa are consuming carbohydrate and protein stores in response to reduced symbiont density and chlorophyll a content, while lipid stores remain relatively unaltered, in line with previous work on coral energetics”
Small comments:
Writing style: “clearly” is used multiple times across the manuscript. This can be removed from most of the sentences and let the reader decide if something is clear based on the data. e.g., Line 395 could be: “pCO2 treatment drove differences in coral physiology” instead of “pCO2 treatment clearly drove differences in coral physiology”.
Response: We have removed many uses of ‘clearly’ from the text per request.
Lines 479-481 are repeated in the manuscript.
Response: We have now modified these statements like so:
Lines 465-467 now state: “It is clear that coral responses under global change remain complex and require further investigation using additional multi-stressor, multi-species studies to tease apart these complexities.”
Lines 508-510 now state: “Either way, the role of plasticity in coral responses to global change is complex and merits further investigation to better understand species-specific levels of resilience.”
Thank you for making your data and code available.
Response: Thank you for the kind comment here, it is a major goal of ours to ensure open and transparent science.
10.1371/journal.pone.0273897.r003Decision Letter 1MayfieldAnderson B.Academic Editor2022Anderson B. MayfieldThis is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Submission Version1
13 Jul 2022
PONE-D-22-07335R1Global change differentially modulates Caribbean coral physiology and suggests future ‘winners’ and ‘losers’PLOS ONE
Dear Dr. Bove,
Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.
Please submit your revised manuscript by Aug 27 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.
Please include the following items when submitting your revised manuscript:
A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.
If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.
If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.
We look forward to receiving your revised manuscript.
Kind regards,
Anderson B. Mayfield, Ph.D.
Academic Editor
PLOS ONE
Journal Requirements:
Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.
Additional Editor Comments :
Hello,
I apologize for this taking so long, but one of the original reviewers was too busy to review it, and then 13 others declined (likely because they were in Bremen)! But I digress. The new reviewer has raised some minor issues, but I don't see them as being an issue. I'll be looking forward to seeing the revised version in a few weeks.
Thanks,
Anderson
[Note: HTML markup is below. Please do not edit.]
Reviewers' comments:
Reviewer's Responses to Questions
Comments to the Author
1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.
Reviewer #1: (No Response)
Reviewer #3: (No Response)
**********
2. Is the manuscript technically sound, and do the data support the conclusions?
The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.
Reviewer #1: (No Response)
Reviewer #3: Yes
**********
3. Has the statistical analysis been performed appropriately and rigorously?
Reviewer #1: (No Response)
Reviewer #3: Yes
**********
4. Have the authors made all data underlying the findings in their manuscript fully available?
The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.
Reviewer #1: (No Response)
Reviewer #3: Yes
**********
5. Is the manuscript presented in an intelligible fashion and written in standard English?
PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.
Reviewer #1: (No Response)
Reviewer #3: Yes
**********
6. Review Comments to the Author
Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)
Reviewer #1: (No Response)
Reviewer #3: Please see the uploaded word document for general comments as well as specific comments to the authors.
**********
7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.
If you choose “no”, your identity will remain anonymous but your review may still be made public.
Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.
Reviewer #1: No
Reviewer #3: No
**********
[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]
While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.
Submitted filename: Review of Bove et al._PLoS One.docx
10.1371/journal.pone.0273897.r004Author response to Decision Letter 1Submission Version2
8 Aug 2022
Review Comments to the Author
General comments:
This paper is a revised version of an initial submission, though this reviewer was not one of the two original reviewers. Overall, I think this paper is improved from its original version based on the previous reviewers’ comments and the tracked changes. I do think this paper deserves to be published in PLoS ONE, but recommend some additional minor revisions prior to acceptance.
I appreciate the Github link for the data and analysis codes used for this paper.
Response: Thank you for the helpful feedback and we appreciate the kind comment regarding the inclusion of the GitHub link to the data and code. We strive for transparency and reproducibility!
Specific comments:
I think the introduction is well-written, especially after seeing the additions made from the first round of review, but I have a few additional comments.
Line 119: I would classify S.sid as “weedy” with P.ast
Response: We are using the classifications for these species based on the study led by Darling in 2012 where they assign these labels across coral species. We agree that S. siderea appears to exhibit weedy traits, but it is classified as a stress-tolerant species based on the referenced work.
Line 119: in reference to line 435 in the discussion – in the discussion the authors write “Indeed, P. strigosa is known to be a more thermally sensitive coral species…” but in line 119 in the intro you write that P.strig was chosen b/c it’s stress-tolerant. This needs to be clarified.
Response: We have left the classification of P. strigosa as ‘stress tolerant’ in the intro because this was our reasoning behind selecting this species. However, recent work has demonstrated the sensitivity of this species in more recent years. We have now updated this portion of the discussion to cover this shift (Lines 463-467): “Indeed, while P. strigosa was previously classified as a stress-tolerant species based on trait assessment [45], it has more recently been identified as a more thermally sensitive coral species [35,68,69]. This response is likely representative of the overall deterioration of coral condition in response to thermal stress, which may lead to mortality under chronic or extreme exposure as is being seen more frequently on Caribbean coral reefs [5].”
Line 119: Maybe the authors could consider expanding upon the framing of the 3 selected species – we know that coral cover has declined rapidly on Caribbean reefs due to a myriad of factors, most recent of which include SCTLD. Perhaps framing the experiment a little more intentionally, e.g., you selected weedy/stress tolerant spp because you wanted to test what the predominant responses of the likely-to-be-dominant corals on reefs of the Caribbean will be… it’s not far off from what you have now, but right now it feels like it’s implied – like you didn’t write that but I’m guessing that’s what you intended. If you’re more intentional with the rationale and the “why it matters”, it just makes the reader more invested in reading on.
Response: We appreciate this suggestion to be more explicit here about the framing of the study and so we have updated this section of the introduction to read (Lines 120-127): “These coral species were selected because they represent both weedy (P. astreoides) and stress-tolerant (S. siderea and P. strigosa) life histories [45], possess similar growth morphologies (mounding), and are common throughout the Caribbean . These coral species are common throughout the Caribbean and can be found across a variety of environmental gradients. Additionally, we included corals from two distinct reef environments to assess how environmental histories impact responses to global change stressors. Overall, we selected these species to better understand how corals that are expected to dominate Caribbean reefs in the future may respond to global change stressors.”
Truthfully, when I first read this paper, my initial thought was this deserves to be published; however, I’m not sure how novel it is. Lots of labs have done cross-factorial TxCO2 work like this to assess physiological responses in corals and their symbionts between 2012-present (other Bove papers, other Castillo lab papers, Baumann, Grottoli, Schoepf, Towle, Okazaki, Manzello, Enochs, Edmunds, and many more…) But the framing of this is what might set this paper apart from the many that came before it.
We know the Caribbean is in trouble. We know we have lost a lot of major reef builders. The question that persists is: for the weedy and stress tolerant spp – is there hope for them under combined and possibly extreme TXCO2 scenarios, and on top of that – at prolonged stress exposure, e.g. 90 days, not just 30 or 60 days? I’d like to see the authors play that up and distinguish how this work is novel compared to the many previous studies that at first glance might seem very similar. Convince us why this experiment matters – why we still need this research as a contribution to the literature. The authors start to get at this in lines 593-599 in the Discussion, but I think expanding it could really strengthen the paper.
Response: We appreciate your support of this work and understand that we need to highlight how this work is unique more throughout the manuscript. We have added several statements throughout to drive this message home to readers, for example:
Lines 438-440: “Caribbean coral reefs have experienced considerable shifts in ecosystem composition since the 1970s defined by declines in several stony coral taxa [67,68], resulting in reefs now dominated by weedy and stress-tolerant species.”
Lines 497-500: “Further, while other studies report synergistic effects on coral physiology, most of these studies only assess a single parameter, potentially missing other key physiological responses that suggest more additive responses like observed here.”
Lines 652-654: “As global change continues, it is critical to understand species-specific responses of coral to ocean acidification and warming scenarios to predict the future of Caribbean coral reef assemblages, especially with a focus on now-dominant coral species explored here. “
Lines 657-660: “Conversely, the previously assumed stress-tolerant species P. strigosa was unable to maintain any physiological traits under warming, suggesting that this species is now particularly vulnerable to thermal stress, which will likely lead to widespread bleaching and mortality.”
Methods:
Line 163, Table 1: Are there two typos?
In the preindustrial CO2 column should the 31 +/- 96 be 301?
Similarly in the current-day CO2 column should the 47 +/- 152 be 407?
Response: Thank you for catching these typos, we have fixed them according to the data (31 should have been 311 and 47 should have been 447).
Line 169-170: Is there a reason why the authors combined frozen artemia and newly hatched artemia? Why not just keep the feedings consistent by using one or the other? Doesn’t that technically introduce another variable? In reality, I’m sure there was no measurable effect on heterotrophy between frozen and freshly hatched, but you never know…? Also – how much artemia were fed to each tank? Quantity is important to mention here when thinking about how feeding affects lipids, etc., even though feeding rate was not tested in this study. In short, I noticed the sentence (line 169-170) was added following the first review, but I still think it could use an additional sentence or two of clarification about amount (quantity) of heterotrophic food offered to the corals in each treatment tank. Do the authors know approximate zooplankton density on the natal reefs in Belize? Or was the amount fed based on previous studies?
Response: We combined the frozen and newly hatched because we wanted to make sure that there were different size classes available to the corals and because there was some concern that freshly-hatched Artemia would not have the same nutritional value to more mature Artemia. The frozen and freshly hatched artemia were combined together into a container before being added to the experimental tanks every time so each system was provided the same mixture every time, making it consistent across treatments and tanks. We have clarified this and the amount fed in the text as requested, as well as included the references that helped us settle on this feeding regime and the section now reads (Lines 175-177): “Corals were fed a combination of ca. 6 g frozen adult Artemia and 250 mL concentrated newly hatched live Artemia (500 mL-1) every other day to satisfy heterotrophic feeding [51,52].”
Results:
I noticed a couple of inconsistencies with italicizing and using the subscript “2” for CO2 so I recommend the authors just do a find and replace for species names and “CO2”. Examples include line 316 (species names not italicized) and line 320 “pCO2”. I also noticed use of the British spelling for “colour”. I think as long as it’s consistent it’s fine, and I’m sure if the journal wants the use of “color” that can be corrected during final formatting/editing, but just flagging that the authors might want to check.
Response: Thank you for catching this inconsistency, we have changed the spelling throughout to use ‘colour’ unless the journal prefers the American English spelling. Additionally, we have fixed the use of CO2 throughout as well!
Line 369: Do you have any ideas about why the P. strigosa controls had low survivorship? Do you attribute it to transfer stress form Belize to Massachusetts? Having low survivorship in the controls is a reason to potentially be more critical (or at least skeptical) of treatment results, so if the authors have any ideas about this, they should be briefly mentioned/discussed.
Response: The starting N for this system was lower at the start of the experiment because of loss of samples through the adjustment period. We noticed this system had been impacted by some microorganisms so we had to construct a new ‘control’ system for all species, however, we had many fewer reserve fragments of these genotypes for this species so lower N to begin with. We have thus added the following sentence into the methods to address this (Lines 260-263): “Further, the initial and final control treatment sample size of P. strigosa was lower than other species because this treatment system had to be reconstructed before the start of the experiment and there were only a few reserve genotypes of this species available for the new control system.”
Line 401: Does “constrained physiology” mean “less plastic”?
Response: Yes, we interpret this constrained physiology to mean these corals are less plastic and that corals under these conditions will exhibit similar responses.
Discussion:
Line 435: see comment above from introduction about the incongruence with the statement in line 119.
Response: We have addressed this comment as requested (detailed above).
Line 494-510: I found this paragraph a little hard to get through. There’s so much use of the word “plasticity” and the positive and negative aspects of how plasticity manifested in P. ast and P. strig in the experiment. Then the authors distinguish between the concept of “physiological plasticity” from the study and genotypic plasticity (not analyzed in this study). I get what the authors are trying to convey, but the wording and flow of this paragraph (at least for me) could be improved to help the reader more quickly grasp the take-home messages.
Response: We have updated the text in this paragraph to improve readability and flow as requested. This section how reads (Lines 529-544): “Varying levels of plasticity in P. strigosa and P. astreoides from different habitats has been previously reported [47,86]; however, natal reef effects were not evident in either species in this study (Fig 3B-C). The small sample size of P. strigosa likely contributed to the lack of differences between habitats, while different measures of plasticity – physiological plasticity (present study) vs. gene expression plasticity [86] – may contribute to the inconsistent responses observed in P. astreoides. While neither species exhibited differing levels of plasticity between reef environments, both P. strigosa and P. astreoides appear to exhibit higher plasticity at the elevated temperature, though this is only statistically significant in P. astreoides (Fig 3B-C). Interestingly, the higher plasticity at elevated temperatures in P. strigosa was associated with diminished physiological conditions, while higher plasticity in P. astreoides manifested as improved physiology (Fig 1B-C). These differences highlight how plasticity may result from physiological trade-offs in response to environmental change in some organisms (i.e., P. strigosa) [42,85], while other organisms (i.e., P. astreoides) may benefit from such plastic responses to match their physiology to their environment [87]. Either way, the role of plasticity in coral responses to global change is complex and merits further investigation to better understand species-specific levels of resilience.”
Line 590-593: I generally agree with this statement. I realize you tested more than one parameter in this study, but you still proceeded to use the “winner” and “loser” terminology in your article title after cautioning others against this (for good reason)…
Response: We agree with your concern about this statement and continuing to use those terms in the title so we have updated the title to be “Global change differentially modulates Caribbean coral physiology”.
Lines 593-599: See earlier comment about expansion of these ideas.
Response: We had expanded the discussion as requested and highlighted some of these areas in our response above.
10.1371/journal.pone.0273897.r005Decision Letter 2MayfieldAnderson B.Academic Editor2022Anderson B. MayfieldThis is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Submission Version2
18 Aug 2022
Global change differentially modulates Caribbean coral physiology
PONE-D-22-07335R2
Dear Dr. Bove,
We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.
Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.
An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.
If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.
Kind regards,
Anderson B. Mayfield, Ph.D.
Academic Editor
PLOS ONE
Additional Editor Comments (optional):
Reviewers' comments:
Reviewer's Responses to Questions
Comments to the Author
1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.
Reviewer #1: All comments have been addressed
Reviewer #3: All comments have been addressed
**********
2. Is the manuscript technically sound, and do the data support the conclusions?
The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.
Reviewer #1: Yes
Reviewer #3: Yes
**********
3. Has the statistical analysis been performed appropriately and rigorously?
Reviewer #1: Yes
Reviewer #3: Yes
**********
4. Have the authors made all data underlying the findings in their manuscript fully available?
The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.
Reviewer #1: Yes
Reviewer #3: Yes
**********
5. Is the manuscript presented in an intelligible fashion and written in standard English?
PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.
Reviewer #1: Yes
Reviewer #3: Yes
**********
6. Review Comments to the Author
Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)
Reviewer #1: (No Response)
Reviewer #3: Thanks for addressing all of the comments in the re- review. I think the authors have done so adequately and appropriately. I think the title change is good, and appreciate the clarifications on the heterotrophic feedings as well as the efforts to distinguish this work from previous, similar studies. I believe this is now suitable for publication in PLoS ONE.
**********
7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.
If you choose “no”, your identity will remain anonymous but your review may still be made public.
Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.
Reviewer #1: No
Reviewer #3: No
**********
10.1371/journal.pone.0273897.r006Acceptance letterMayfieldAnderson B.Academic Editor2022Anderson B. MayfieldThis is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
24 Aug 2022
PONE-D-22-07335R2
Global change differentially modulates Caribbean coral physiology
Dear Dr. Bove:
I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.
If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.
If we can help with anything else, please email us at plosone@plos.org.
Thank you for submitting your work to PLOS ONE and supporting open access.