Production and accumulation of reef framework by calcifying corals and macroalgae on a remote Indian Ocean Cay

McLaughlin, M. James; Bessey, Cindy; Kendrick, Gary A.; Keesing, John; Olsen, Ylva S.

doi:https://doi.org/10.5194/egusphere-2022-467

Preprints

https://doi.org/10.5194/egusphere-2022-467

Preprints

28 Jun 2022

| 28 Jun 2022

Production and accumulation of reef framework by calcifying corals and macroalgae on a remote Indian Ocean Cay

M. James McLaughlin, Cindy Bessey, Gary A. Kendrick, John Keesing, and Ylva S. Olsen

Abstract. Coral reefs face increasing pressures in response to unprecedented rates of environmental change at present. The coral reef physical framework is formed through the production of calcium carbonate (CaCO₃) and maintained by marine organisms, primarily hermatypic corals, crustose coralline algae (CCA), and other calcifying algae. The Kimberley bioregion, located in the northern part of Western Australia, has largely escaped land-based anthropogenic impacts and this study provides important metabolic data we are lacking on reef-building calcifying corals and macrophytes from an undisturbed set of marine habitats. Specimens of the dominant coral and algal taxa were collected from the reef platform of Browse Island located on the mid-shelf just inside the 200 m isobath off the Kimberley coast. During experimental light/dark incubations, all algae were net autotrophic producing 6–111 mmol O₂ m⁻² day⁻¹. In contrast, most corals were net consumers of O₂ with average net fluxes ranging from −42 to 47 mmol O₂ m⁻² day⁻¹. The net change in pH was generally negative for corals and calcifying algae (−0.01 to −0.08 h−1). Corals, Halimeda (a calcifying green algae) and Galaxaura (a calcifying red algae) had positive calcification rates in light ranging from 4.2 to 18.4 g CaCO₃ m⁻² d⁻¹. Resulting net calcification rates were all positive and ranged from 1.9 to 9.9 g CaCO₃ m⁻² d⁻¹ and were strongly correlated to net O₂ production. In intertidal habitats around Browse Island, estimated relative contributions of coral and Halimeda to the reef production of CaCO₃ were similar at around 600–840 g m⁻² year⁻¹. The low reef platform had very low coral cover of < 3 % which made a smaller contribution to calcification of ~240 g CaCO₃ m⁻² year⁻¹. Calcification on the subtidal reef slope was predominantly from corals, producing ~1540 g CaCO₃ m⁻² year⁻¹, twice that of Halimeda. The relative contributions of the main reef builders, in these undisturbed areas, to net community metabolism and CaCO₃ production and reef metabolism is important to understand exclusively climate-driven coral bleaching and mortality.

Received: 15 Jun 2022 – Discussion started: 28 Jun 2022

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Journal article(s) based on this preprint

15 Mar 2023

Production and accumulation of reef framework by calcifying corals and macroalgae on a remote Indian Ocean cay

M. James McLaughlin, Cindy Bessey, Gary A. Kendrick, John Keesing, and Ylva S. Olsen

Biogeosciences, 20, 1011–1026, https://doi.org/10.5194/bg-20-1011-2023,https://doi.org/10.5194/bg-20-1011-2023, 2023

Short summary

M. James McLaughlin, Cindy Bessey, Gary A. Kendrick, John Keesing, and Ylva S. Olsen

Interactive discussion

Status: closed

RC1:
'Comment on egusphere-2022-467', Anonymous Referee #1, 18 Jul 2022

General Comments:

This study assessed the metabolic and calcification rates of a variety of cultured, reef-dwelling marine calcifiers and algal taxa found in the anthropogenically-pristine Kimberley bioregion of Western Australia. The values measured were then related to the areal extent of benthic coverage across the various local reef habitats and further argued to provide a baseline for understanding shifts in metabolic and calcification rates in this region in response to environmental stressors (i.e. those that induce bleaching and mortality). While the results presented are surely significant in that they represent novel and important reef metabolic data from a unique location, more time/space could be spent discussing the methods used, assumptions made, and data generated in relation to previously published studies and long outstanding questions in the field (particularly with relation to future impacts of anthropogenic change). The authors should potentially consider reorganizing the key takeaways of the article - particularly in the Discussion section - around these topics as they are currently lacking and/or given short shrift. As it is currently presented, the Discussion section reads as a series of descriptive statements rather than a connected narrative that binds the manuscript together, interprets and provides context for the results of the study, and proposes potential mechanisms and future directions. Overall, I think spending a little more time thinking about the selected location, taxa, observed rates of metabolism/calcification, and trends in O2, pH, and TA in relation to future projected impacts of environmental change in this region (quantitatively, if possible) is a worthwhile endeavor and will only strengthen the impact of this work.

Specific Comments/Questions:

Lines 52 - 61: Just to clarify, it is commonly argued that net community productivity (NCP) rates in many reef ecosystems, while certainly variable over the course of a diel cycle, tend to balance out over longer temporal scales such that nearly all of the organic carbon produced during periods of high photosynthesis is consumed on annual timescales or greater (i.e. Ware et al., 1992; Frankignoulle and Gattuso, 1993; Gattuso et al., 1999; Bates, 2002 and others). Thus, while it is true that CO2 source/sink behavior is possible in coral reefs on short timescales, overall they are believed to be net sources because of high calcification rates.

Lines 123 - 125: I’d argue it’s more the magnitude and the net effect of these changes that is difficult to predict rather than conceptually reasoning through the effects themselves. We know the respective impacts of photosynthesis/respiration and calcification/dissolution on many parameters of carbonate chemistry very well, but “hybrid” organisms that have both NCP and NCC rates (like corals and calcifying algae) make predicting the values of these rates difficult.

Section 2.2: What is the rationale/motivation for selecting these particular taxa for incubations - both abundance-wise and otherwise?

Lines 131 - 134: Include citations for those that do exist and potentially some discussion on what has been learned and/or what is left to explore or challenge?

Section 2.3: In the “real” world, PAR has a more parabolic shape with time over the course of a day than the more step-wise shifts induced by the incubation setup. It follows that photosynthesis vs irradiance is often modeled as a hyperbolic tangent function (i.e. Atkinson and Grigg, 1984; Langdon and Atkinson, 2005; Bouman et al., 2018; Bolden et al., 2019). Has any thought been given to what artifacts the simplified 4-hour approach (2 hours light - 2 hours dark) to incubations presented here may have on measured and scaled-up metabolic and calcification rates?

Lines 231 - 242: Is this instrument/method calibrated using any kind of standard (such as the Dickson CRMs or another internal standard)?

Section 2.6: This is an interesting approach. To clarify, there are four total incubation periods: two, 1-hour light periods and two, 1-hour dark periods. The per-hour rates of O2 (or alkalinity) production or consumption are then multiplied by 24 to get respective light or dark “daily” rates of net productivity (and calcification). However, why is expressing light and dark incubation results in terms of *daily* fluxes valuable? Photosynthesis only occurs during sunlight hours; in your assumptions, there are only 12 hours of photosynthesis and 24 of respiration in a day. Not that these are invalid assumptions, but would it not make more sense to express the light and dark rates on hourly scales *or* do the calculation for the net flux (GPP - R) and express this as 1 daily value for each light+dark pair?

Lines 280 - 284 (and Table 2): Any comment on why this may be and/or what it implies about seasonal/interannual variability of carbonate chemistry in the offshore waters that are assumed to supply the reef ecosystem?

Section 3.2: I think this goes back to my earlier comment - I would think about expressing the respective light and dark fluxes in hourly units rather than daily. I am guessing that the calculations of net autotrophy/heterotrophy are based on light rates minus dark rates. *However* I would double-check to make sure the equations used are consistent with a 12-hour photoperiod and 24-hours of respiration. Including the equations used in the text would be a valuable addition.

Lines 315 - 318: How are the r2 values “adjusted”?

Lines 365 - 369: Why is the alkalinity anomaly technique prone to overestimates of calcification rates? A small clause (and citation?) for this would balance the underestimate assertion for the CaCO3 content/growth method.

Lines 373 - 386: Out of curiosity, to measured pH and alkalinity values produce calculated DIC values (using CO2SYS or seacarb) consistent with the trends in O2 in terms of the magnitude of heterotrophic/autotrophic behavior across taxa?

Lines 422 - 430: Are there any hypothesized observations/mechanisms for explaining why the calcification rates here are lower than other reported values - particularly as they relate to local open ocean chemistry variability and/or artificats introduced in the incubation + scaling approach?

Lines 460 - 462: Why were CCA species not included in this incubation study?

Technical Comments/Questions:

Line 69 - No need for possessive. “Coral skeletons are…” is fine.

Lines 84 - 85: This concluding sentence reads as a bit of a non sequitur, and this paragraph overall could use some refocusing. I would suggest taking a step back and thinking about the key points the reader is meant to take away from this section. It seems like it’s about scleractinian coral contributions to the reef framework and threats to that contribution (based on lines 65-80, but lines 80 - 85 suddenly shift focus to metabolism.

Line 87 - I think this first sentence could be stated more concisely. “Reef algae are also an important structural component of coral reef ecosystems. Their morphological diversity provides…”

Line 95 - Sentence could be more concise. “Calcified macroalgae can also contribute significantly to the deposition of carbonates in coral reef environments.”

Line 99 - “make it a major contributor”.

Lines 99 - 102: Here and throughout, be careful and consistent with the use of the term “production” to refer to organic carbon/oxygen production vs CaCO3 precipitation.

Line 277 (and elsewhere): Consider expressing O2 concentration in molar units (as you do in subsequent discussions). It would be more consistent with the other measured chemical constituents and allow readers to think about potential stoichiometric relationships between variables more easily.

Lines 290 - 292: This sentence could be more concise and clear (I think). “In light incubations, O2 productivity fluxes were postitive across all taxa.”

Lines 395 - 398: This is repeated at line 364.

Citation: https://doi.org/10.5194/egusphere-2022-467-RC1
- AC1: 'Reply on RC1', James Mclaughlin, 28 Nov 2022
  
  We thank reviewer RC1 for their insightful and considered comments and suggestions. We have made significant changes to the introduction and discussions sections to address some of the constructive criticisms provided by RC1, which we think adds considerable value and strengthens our manuscript. We have sought to address all of the specific comments and questions that RC1 has provided in the supplemental document attached.
  
  Citation: https://doi.org/10.5194/egusphere-2022-467-AC1
RC2:
'Comment on egusphere-2022-467', Anonymous Referee #2, 26 Jul 2022

The comment was uploaded in the form of a supplement: https://egusphere.copernicus.org/preprints/2022/egusphere-2022-467/egusphere-2022-467-RC2-supplement.pdf

Citation: https://doi.org/10.5194/egusphere-2022-467-RC2
- AC2: 'Reply on RC2', James Mclaughlin, 28 Nov 2022
  
  We thank reviewer RC2 for the time spent providing constructive criticism and comments on our manuscript. We greatly appreciate the reviewers suggested additional reference material for us to consider implementing into this manuscript. We feel in addressing the comments, the effort has added considerable value to our work resulting in a much more impactful summation for our study of the reef at Browse Island. Please find our responses to RC2's specific comments in the supplemental document attached.
  
  Citation: https://doi.org/10.5194/egusphere-2022-467-AC2

Interactive discussion

Status: closed

RC1:
'Comment on egusphere-2022-467', Anonymous Referee #1, 18 Jul 2022

General Comments:

This study assessed the metabolic and calcification rates of a variety of cultured, reef-dwelling marine calcifiers and algal taxa found in the anthropogenically-pristine Kimberley bioregion of Western Australia. The values measured were then related to the areal extent of benthic coverage across the various local reef habitats and further argued to provide a baseline for understanding shifts in metabolic and calcification rates in this region in response to environmental stressors (i.e. those that induce bleaching and mortality). While the results presented are surely significant in that they represent novel and important reef metabolic data from a unique location, more time/space could be spent discussing the methods used, assumptions made, and data generated in relation to previously published studies and long outstanding questions in the field (particularly with relation to future impacts of anthropogenic change). The authors should potentially consider reorganizing the key takeaways of the article - particularly in the Discussion section - around these topics as they are currently lacking and/or given short shrift. As it is currently presented, the Discussion section reads as a series of descriptive statements rather than a connected narrative that binds the manuscript together, interprets and provides context for the results of the study, and proposes potential mechanisms and future directions. Overall, I think spending a little more time thinking about the selected location, taxa, observed rates of metabolism/calcification, and trends in O2, pH, and TA in relation to future projected impacts of environmental change in this region (quantitatively, if possible) is a worthwhile endeavor and will only strengthen the impact of this work.

Specific Comments/Questions:

Lines 52 - 61: Just to clarify, it is commonly argued that net community productivity (NCP) rates in many reef ecosystems, while certainly variable over the course of a diel cycle, tend to balance out over longer temporal scales such that nearly all of the organic carbon produced during periods of high photosynthesis is consumed on annual timescales or greater (i.e. Ware et al., 1992; Frankignoulle and Gattuso, 1993; Gattuso et al., 1999; Bates, 2002 and others). Thus, while it is true that CO2 source/sink behavior is possible in coral reefs on short timescales, overall they are believed to be net sources because of high calcification rates.

Lines 123 - 125: I’d argue it’s more the magnitude and the net effect of these changes that is difficult to predict rather than conceptually reasoning through the effects themselves. We know the respective impacts of photosynthesis/respiration and calcification/dissolution on many parameters of carbonate chemistry very well, but “hybrid” organisms that have both NCP and NCC rates (like corals and calcifying algae) make predicting the values of these rates difficult.

Section 2.2: What is the rationale/motivation for selecting these particular taxa for incubations - both abundance-wise and otherwise?

Lines 131 - 134: Include citations for those that do exist and potentially some discussion on what has been learned and/or what is left to explore or challenge?

Section 2.3: In the “real” world, PAR has a more parabolic shape with time over the course of a day than the more step-wise shifts induced by the incubation setup. It follows that photosynthesis vs irradiance is often modeled as a hyperbolic tangent function (i.e. Atkinson and Grigg, 1984; Langdon and Atkinson, 2005; Bouman et al., 2018; Bolden et al., 2019). Has any thought been given to what artifacts the simplified 4-hour approach (2 hours light - 2 hours dark) to incubations presented here may have on measured and scaled-up metabolic and calcification rates?

Lines 231 - 242: Is this instrument/method calibrated using any kind of standard (such as the Dickson CRMs or another internal standard)?

Section 2.6: This is an interesting approach. To clarify, there are four total incubation periods: two, 1-hour light periods and two, 1-hour dark periods. The per-hour rates of O2 (or alkalinity) production or consumption are then multiplied by 24 to get respective light or dark “daily” rates of net productivity (and calcification). However, why is expressing light and dark incubation results in terms of *daily* fluxes valuable? Photosynthesis only occurs during sunlight hours; in your assumptions, there are only 12 hours of photosynthesis and 24 of respiration in a day. Not that these are invalid assumptions, but would it not make more sense to express the light and dark rates on hourly scales *or* do the calculation for the net flux (GPP - R) and express this as 1 daily value for each light+dark pair?

Lines 280 - 284 (and Table 2): Any comment on why this may be and/or what it implies about seasonal/interannual variability of carbonate chemistry in the offshore waters that are assumed to supply the reef ecosystem?

Section 3.2: I think this goes back to my earlier comment - I would think about expressing the respective light and dark fluxes in hourly units rather than daily. I am guessing that the calculations of net autotrophy/heterotrophy are based on light rates minus dark rates. *However* I would double-check to make sure the equations used are consistent with a 12-hour photoperiod and 24-hours of respiration. Including the equations used in the text would be a valuable addition.

Lines 315 - 318: How are the r2 values “adjusted”?

Lines 365 - 369: Why is the alkalinity anomaly technique prone to overestimates of calcification rates? A small clause (and citation?) for this would balance the underestimate assertion for the CaCO3 content/growth method.

Lines 373 - 386: Out of curiosity, to measured pH and alkalinity values produce calculated DIC values (using CO2SYS or seacarb) consistent with the trends in O2 in terms of the magnitude of heterotrophic/autotrophic behavior across taxa?

Lines 422 - 430: Are there any hypothesized observations/mechanisms for explaining why the calcification rates here are lower than other reported values - particularly as they relate to local open ocean chemistry variability and/or artificats introduced in the incubation + scaling approach?

Lines 460 - 462: Why were CCA species not included in this incubation study?

Technical Comments/Questions:

Line 69 - No need for possessive. “Coral skeletons are…” is fine.

Lines 84 - 85: This concluding sentence reads as a bit of a non sequitur, and this paragraph overall could use some refocusing. I would suggest taking a step back and thinking about the key points the reader is meant to take away from this section. It seems like it’s about scleractinian coral contributions to the reef framework and threats to that contribution (based on lines 65-80, but lines 80 - 85 suddenly shift focus to metabolism.

Line 87 - I think this first sentence could be stated more concisely. “Reef algae are also an important structural component of coral reef ecosystems. Their morphological diversity provides…”

Line 95 - Sentence could be more concise. “Calcified macroalgae can also contribute significantly to the deposition of carbonates in coral reef environments.”

Line 99 - “make it a major contributor”.

Lines 99 - 102: Here and throughout, be careful and consistent with the use of the term “production” to refer to organic carbon/oxygen production vs CaCO3 precipitation.

Line 277 (and elsewhere): Consider expressing O2 concentration in molar units (as you do in subsequent discussions). It would be more consistent with the other measured chemical constituents and allow readers to think about potential stoichiometric relationships between variables more easily.

Lines 290 - 292: This sentence could be more concise and clear (I think). “In light incubations, O2 productivity fluxes were postitive across all taxa.”

Lines 395 - 398: This is repeated at line 364.

Citation: https://doi.org/10.5194/egusphere-2022-467-RC1
- AC1: 'Reply on RC1', James Mclaughlin, 28 Nov 2022
  
  We thank reviewer RC1 for their insightful and considered comments and suggestions. We have made significant changes to the introduction and discussions sections to address some of the constructive criticisms provided by RC1, which we think adds considerable value and strengthens our manuscript. We have sought to address all of the specific comments and questions that RC1 has provided in the supplemental document attached.
  
  Citation: https://doi.org/10.5194/egusphere-2022-467-AC1
RC2:
'Comment on egusphere-2022-467', Anonymous Referee #2, 26 Jul 2022

The comment was uploaded in the form of a supplement: https://egusphere.copernicus.org/preprints/2022/egusphere-2022-467/egusphere-2022-467-RC2-supplement.pdf

Citation: https://doi.org/10.5194/egusphere-2022-467-RC2
- AC2: 'Reply on RC2', James Mclaughlin, 28 Nov 2022
  
  We thank reviewer RC2 for the time spent providing constructive criticism and comments on our manuscript. We greatly appreciate the reviewers suggested additional reference material for us to consider implementing into this manuscript. We feel in addressing the comments, the effort has added considerable value to our work resulting in a much more impactful summation for our study of the reef at Browse Island. Please find our responses to RC2's specific comments in the supplemental document attached.
  
  Citation: https://doi.org/10.5194/egusphere-2022-467-AC2

Peer review completion

AR: Author's response | RR: Referee report | ED: Editor decision | EF: Editorial file upload

ED: Reconsider after major revisions (29 Nov 2022) by Tyler Cyronak

AR by James Mclaughlin on behalf of the Authors (30 Nov 2022) Author's response Author's tracked changes Manuscript

ED: Referee Nomination & Report Request started (06 Dec 2022) by Tyler Cyronak

RR by Anonymous Referee #1 (12 Dec 2022)

Suggestions for revision or reasons for rejection

I highly suggest the authors consider re-outlining the Introduction as it will help focus the details of this key section of the manuscript and further highlight the significance of their work. Many of the paragraphs in this section currently read as though they are each the "first" paragraph in an Introduction, rather than a series of connected ideas. I wholeheartedly agree with the authors that having baseline metabolic and benthic community composition data from a relatively pristine coral reef ecosystem is important, but the "why" in relation to compounding environmental/climate stressors and/or the need to compare to ecosystems with different benthic community composition is somewhat lost when interpreting through these seemingly disjointed paragraphs and often repeated but vague statements about biogeochemical cycling and metabolism within reef ecosystems. That said, clarity and details in the Methods, Experimental Results, and Discussion sections are much improved and provide an appropriate level context for the study.

Line Edits/Comments/Technical Corrections
Summary of Intro P1: Stressors causing changes in reef ecosystems?

Summary of Intro P2: Ecosystem services provided by modern reefs?

Summary of Intro P3: Capturing metabolism in coral reef ecosystems?

Summary of Intro P4: Calcification on reefs and the threat of OA?

Summary of Intro P5: Back to metabolism on reefs?

Summary of Intro P6: The important roles of benthic algae in reef ecosystems?

Summary of Intro P7: Influence of reef metabolism on seawater chemistry?

Summary of Intro P8: Uniqueness of the opportunity to study the Kimberley Bioregion of NW Australia?

Line 41: “current” rather than “currently”?

Line 43: Citation for the impacts of “recurrent large scale weather events”?

Lines 41 - 47: A lot packed into this sentence; consider breaking up and refocusing. Also, a bit unclear on the link between eutrophication, sedimentation, and increasing SST and OA. I think breaking this sentence up could help with this though.

Lines 52 - 57: Shouldn’t these sentences come before ecosystem services are introduced in the last sentence of the preceding paragraph?

Lines 64 - 66: The way this sentence is written is counter to lines 71 - 75.

Lines 71 - 75: Adding the timescales (i.e. seasonal, annual, etc.) over which reef flats are generalized to be net sources of CO2 to the atmosphere may help reconcile this statement with the “high” calcification and production rates mentioned above.

Line 306: Rogue comma.

Line 309: Space needed between 34.8 and ppt.

Lines 313 - 314: Check subscripts and superscripts.

Line 355: Rogue underscore?

Lines 378 - 396: Not sure if this paragraph is well-positioned here. A lot of the statements in this paragraph read as site descriptions that may serve a stronger role in the Methods section when introducing Browse Island. Additionally, the “general” discussion of the influences of production and calcification on ambient seawater chemistry has already been brought up in the Introduction.

Lines 398 - 417: I think this is a much stronger starting paragraph for the Discussion section.

Lines 413 - 417: Run-on sentence. Consider a full stop after “elsewhere” and starting a new sentence with “For example…”

Line 415: Rogue space after O2.

Lines 448 - 453 (and throughout): Be mindful of run-on sentences.

Lines 453 - 455: “… or use of radioisotopes *was* limited.”

Lines 584 - 586: Repeated in 586 - 587.

Figures 3, 4, and 6: Axes are unreadable/corrupted.

Hide

ED: Publish subject to minor revisions (review by editor) (20 Jan 2023) by Tyler Cyronak

AR by James Mclaughlin on behalf of the Authors (02 Feb 2023) Author's response Author's tracked changes Manuscript

ED: Publish subject to technical corrections (17 Feb 2023) by Tyler Cyronak

AR by James Mclaughlin on behalf of the Authors (20 Feb 2023) Manuscript

Journal article(s) based on this preprint

15 Mar 2023

Production and accumulation of reef framework by calcifying corals and macroalgae on a remote Indian Ocean cay

M. James McLaughlin, Cindy Bessey, Gary A. Kendrick, John Keesing, and Ylva S. Olsen

Biogeosciences, 20, 1011–1026, https://doi.org/10.5194/bg-20-1011-2023,https://doi.org/10.5194/bg-20-1011-2023, 2023

Short summary

M. James McLaughlin, Cindy Bessey, Gary A. Kendrick, John Keesing, and Ylva S. Olsen

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Short summary

Coral reefs face increasing pressures from environmental change at present. The coral reef physical framework is formed through the production of calcium carbonate by corals, crustose coralline algae (CCA), and other calcifying algae. The Kimberley bioregion, located in the northern part of Western Australia, has largely escaped land-based anthropogenic impacts and this study provides important data on reef building processes we are lacking from an undisturbed set of marine habitats.


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