Simulated terrestrial runoff shifts the metabolic balance of a coastal Mediterranean plankton community toward heterotrophy

Soulié, Tanguy; Vidussi, Francesca; Courboulès, Justine; Heydon, Marie; Mas, Sébastien; Voron, Florian; Cantoni, Carolina; Joux, Fabien; Mostajir, Behzad

doi:https://doi.org/10.5194/egusphere-2023-2782

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https://doi.org/10.5194/egusphere-2023-2782

Preprints

24 Nov 2023

| 24 Nov 2023

Simulated terrestrial runoff shifts the metabolic balance of a coastal Mediterranean plankton community toward heterotrophy

Tanguy Soulié, Francesca Vidussi, Justine Courboulès, Marie Heydon, Sébastien Mas, Florian Voron, Carolina Cantoni, Fabien Joux, and Behzad Mostajir

Abstract. Climate change is projected to increase the frequency and intensity of extreme rainfall events in the Mediterranean region, increasing runoffs of terrestrial matter into coastal waters. To evaluate the consequences of terrestrial runoff on plankton key processes, an in situ mesocosm experiment was conducted for 18 days in the spring of 2021 in the coastal Mediterranean Thau Lagoon. Terrestrial runoff was simulated in replicate mesocosms by adding soil from an adjacent oak forest that had matured in water from the main river tributary of the lagoon. Automated high-frequency monitoring of dissolved oxygen, chlorophyll-a fluorescence, salinity, light, and temperature was combined with manual sampling of organic and inorganic nutrient pools, pH, carbonate chemistry and maximum quantum yield (Fv:Fm) of photosystem II (PSII). High-frequency data were used to estimate gross oxygen primary production (GPP), respiration (R), and phytoplankton growth (µ) and loss (L) rates. During the first half of the experiment (d2–d11), the simulated runoff reduced light availability (-52 %), chlorophyll-a concentrations (-70 %) and phytoplankton growth rates (-53 %). However, phytoplankton maintained a certain level of primary production by increasing its photosynthetic efficiency. Meanwhile, the runoff enhanced R (+53 %), shifting the metabolic status (GPP:R) of the system toward heterotrophy and increasing the partial pressure of carbon dioxide (pCO₂), potentially switching the direction of the air-sea CO₂ exchange. However, during the second part of the experiment (d11–d17), remineralised nutrients boosted phytoplankton growth (+299 %) in the terrestrial runoff treatment, but not its loss rates, leading to phytoplankton biomass accumulation and suggesting a mismatch between phytoplankton and its predators. Our study showed that a simulated terrestrial runoff significantly affected key plankton processes, suggesting that climate change-related increases in runoff frequency and intensity can shift the metabolic balance of Mediterranean coastal lagoons toward heterotrophy.

Received: 22 Nov 2023 – Discussion started: 24 Nov 2023

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Journal article(s) based on this preprint

17 Apr 2024

Simulated terrestrial runoff shifts the metabolic balance of a coastal Mediterranean plankton community towards heterotrophy

Tanguy Soulié, Francesca Vidussi, Justine Courboulès, Marie Heydon, Sébastien Mas, Florian Voron, Carolina Cantoni, Fabien Joux, and Behzad Mostajir

Biogeosciences, 21, 1887–1902, https://doi.org/10.5194/bg-21-1887-2024,https://doi.org/10.5194/bg-21-1887-2024, 2024

Short summary

Tanguy Soulié, Francesca Vidussi, Justine Courboulès, Marie Heydon, Sébastien Mas, Florian Voron, Carolina Cantoni, Fabien Joux, and Behzad Mostajir

Interactive discussion

Status: closed

CC1: 'Comment on egusphere-2023-2782', A. Regaudie-de-Gioux, 30 Nov 2023

Publisher’s note: this comment is a copy of RC1 and its content was therefore removed.

Citation: https://doi.org/10.5194/egusphere-2023-2782-CC1
RC1:
'Comment on egusphere-2023-2782', Aurore Regaudie de Gioux, 01 Dec 2023
The manuscript « Simulated terrestrial runoff shifts the metabolic balance of a coastal Mediterranean plankton community toward heterotrophy” evaluates the consequences of terrestrial runoff on planktonic communities in the coastal Mediterranean Thau Lagoon. For that the authors conducted in situ mesocosms experiment simulating terrestrial runoff by adding soil and measuring several chemical and biological parameters during almost 3 weeks.
The paper is easy to read, interesting and, I believe, deserve to be published in Biogeosciences.

Please find following some minor comments.

M&Ms
L76: Experiments were performed during 18 days, why?
L87: Turn-over rate of 3.5d-1. Does that mean that every 3.5 days water from the surface goes down to the bottom of the mesocosm and goes then up to the surface?
L92: The data that you presented here are the average of 2 mesocosms for the control and 2 mesocosms for the treatment. It is quite critical to use these data with so few replicates…
L101: “The mixture was left to mature for two weeks”. Any refs? Why 2 weeks?
119: “Winkler Chl-a” , I think this is a typo error.

L121: You said that you left at least during 6 h the DO bottle of fixation. This is quite a lot. Normally, we should leave the DO bottles, once fixed with R1 and R2, to settle the precipitate until reaching 1/3 of the bottle volume. If, for any logistical reason, we have to analyze latter the fixed DO bottles, It is advised to be kept in the dark and under water. Was that the case here?
L135: Nutrient samples were stored at -20°C until analyses. However it is not recommended to keep samples for silicate analyses at -20°C but rather at 4°C. Indeed, freezing can cause polymerization that can biased the analyses and specifically for samples from coastal, estuarine waters and with lower salinity (cf. Aminot and Kerouel). Considering that, I think the silicate data has to be analyzed with great precaution.

How do you think, by the end of the experiment, the diminution of mesocosms volume can affect planktonic communities and thus your analyses?

L175-185: What is the % of error of this method? Its reproducibility and inter-repeatability?

Results
Figure 1: How do you explain the great drop of DLI at day 12 and 13?

Figure 2: BA had opposite trends between control and treatment. How do you explain it? Why did you not analyze the phytoplanktonic abundance?

Figure4: Did you check CR/Chl or CR/BA?

Discussion
L382-387: Considering the mixing of the mesocosms waters (turn-over of 3.5 days), do you think that sedimentation is important?
L390: There is no relationship between CR and BA, so we cannot think that planktonic bacterial respiration represent a major part of community respiration here.
L407: Do you think that Mediterranean coastal lagoons are really net O2 producers today? Any refs?

Supplement information
Rnight = (mean of NCP during night period)*duration of night period*60 (Soulié et al. 2021.
Citation: https://doi.org/10.5194/egusphere-2023-2782-RC1
- AC1: 'Reply on RC1', Tanguy Soulié, 14 Dec 2023
  
  Response to Referee Comment 1
  Dear Dr. Regaudie-de-Gioux,
  We deeply thank you for your helpful comments, improving the quality and accuracy of the manuscript. Please find in the attached document detailed explanations about how we have considered and answered each comment.
  Concerning the modifications made on the revised version of the manuscript explained in the present document, please note that:
  - additional sentences or words were highlighted in yellow
  - deleted sentences or words were written in red and crossed out
  
  Citation: https://doi.org/10.5194/egusphere-2023-2782-AC1
RC2:
'Comment on egusphere-2023-2782', Tamara Cibic, 04 Jan 2024

The work by Soulié et al. “Simulated terrestrial runoff shifts the metabolic balance of a coastal Mediterranean plankton community toward heterotrophy” investigated the consequences of terrestrial runoff on plankton communities and some biological processes in the Thau lagoon on the Mediterranean coast. The results come from an in situ mesocosm experiment in which terrestrial runoff was simulated by adding soil and various chemical and biological variables were analyzed for 18 days.
The paper is well written, focused and interesting and should be published in Biogeosciences after revision.
A major criticism of this work is the fact that no real phytoplankton data are presented. All results were derived from Chl-a sensor data, including phytoplankton growth and loss rates. I know this is becoming more common and accepted lately, but similarly to Chl-a fluorescence and oxygen sensors data, for which some calibrations were done, actual phytoplankton counts and identifications should have been done on at least some samples to check if there is a match between Chl-a and microphytoplankton. Since flow cytometry was used in the paper to estimate heterotrophic bacterial abundance, the same method could have been used to assess the smaller phototrophic picoplankton. It is a pity that there is no information on the actual composition of the phytoplankton, as this is the topic of the article. If the authors have these (already published or unpublished) results, I think it would be a great addition to this publication to at least mention them in the discussion.
Introduction
I think it would be easier for the reader if some scientific questions or hypotheses were added at the end of the introduction section to structure the discussion.
M&Ms
Experimental design
It is not stated what the final volume in each mesocosm is. It is also not clear if the mesocosms are sealed at the top and what the bottom is like. Are the mesocosms open or sealed at the bottom? Are they floating? Please add this information.
L76: The experiments were conducted for 18 days. In my opinion, this is a very long time to test the effects of a flash flood on the coastal area. There is a strong mixing effect by the seawater, and even in a confined area like a lagoon, the terrestrial runoff will eventually be diluted in a few days. The choice of the duration of the experiment should be discussed.
L104: Why was the sampled soil left to mature for two weeks? Why was this step necessary? In a flash flood there is no such step, the soil is washed away directly by the heavy rain and transported into a river and eventually into an estuary. Flash floods do not last 14 days, this is unclear and should be better explained.
Discussion
What I miss here is a discussion of the ecological implications of these results at the lagoon mesoscale. In particular, a detailed discussion of the trophic state of the lagoon and a comparison with other Mediterranean lagoons.

Citation: https://doi.org/10.5194/egusphere-2023-2782-RC2
- AC2:
  'Reply on RC2', Tanguy Soulié, 17 Jan 2024
  
  Dear Dr. Cibic,
  We deeply thank you for your helpful comments, improving the quality and accuracy of the manuscript. Please find in the attached document detailed explanations about how we have considered and answered each comment.
  Concerning the modifications made on the revised version of the manuscript explained in the present document, please note that:
  - additional sentences or words were highlighted in light blue
  - deleted sentences or words were written in purple and crossed out
  
  Citation: https://doi.org/10.5194/egusphere-2023-2782-AC2
  - AC3: 'Reply on AC2', Tanguy Soulié, 17 Jan 2024
    
    The comment was uploaded in the form of a supplement: https://egusphere.copernicus.org/preprints/2023/egusphere-2023-2782/egusphere-2023-2782-AC3-supplement.pdf
    
    Citation: https://doi.org/10.5194/egusphere-2023-2782-AC3

Interactive discussion

Status: closed

CC1: 'Comment on egusphere-2023-2782', A. Regaudie-de-Gioux, 30 Nov 2023

Publisher’s note: this comment is a copy of RC1 and its content was therefore removed.

Citation: https://doi.org/10.5194/egusphere-2023-2782-CC1
RC1:
'Comment on egusphere-2023-2782', Aurore Regaudie de Gioux, 01 Dec 2023
The manuscript « Simulated terrestrial runoff shifts the metabolic balance of a coastal Mediterranean plankton community toward heterotrophy” evaluates the consequences of terrestrial runoff on planktonic communities in the coastal Mediterranean Thau Lagoon. For that the authors conducted in situ mesocosms experiment simulating terrestrial runoff by adding soil and measuring several chemical and biological parameters during almost 3 weeks.
The paper is easy to read, interesting and, I believe, deserve to be published in Biogeosciences.

Please find following some minor comments.

M&Ms
L76: Experiments were performed during 18 days, why?
L87: Turn-over rate of 3.5d-1. Does that mean that every 3.5 days water from the surface goes down to the bottom of the mesocosm and goes then up to the surface?
L92: The data that you presented here are the average of 2 mesocosms for the control and 2 mesocosms for the treatment. It is quite critical to use these data with so few replicates…
L101: “The mixture was left to mature for two weeks”. Any refs? Why 2 weeks?
119: “Winkler Chl-a” , I think this is a typo error.

L121: You said that you left at least during 6 h the DO bottle of fixation. This is quite a lot. Normally, we should leave the DO bottles, once fixed with R1 and R2, to settle the precipitate until reaching 1/3 of the bottle volume. If, for any logistical reason, we have to analyze latter the fixed DO bottles, It is advised to be kept in the dark and under water. Was that the case here?
L135: Nutrient samples were stored at -20°C until analyses. However it is not recommended to keep samples for silicate analyses at -20°C but rather at 4°C. Indeed, freezing can cause polymerization that can biased the analyses and specifically for samples from coastal, estuarine waters and with lower salinity (cf. Aminot and Kerouel). Considering that, I think the silicate data has to be analyzed with great precaution.

How do you think, by the end of the experiment, the diminution of mesocosms volume can affect planktonic communities and thus your analyses?

L175-185: What is the % of error of this method? Its reproducibility and inter-repeatability?

Results
Figure 1: How do you explain the great drop of DLI at day 12 and 13?

Figure 2: BA had opposite trends between control and treatment. How do you explain it? Why did you not analyze the phytoplanktonic abundance?

Figure4: Did you check CR/Chl or CR/BA?

Discussion
L382-387: Considering the mixing of the mesocosms waters (turn-over of 3.5 days), do you think that sedimentation is important?
L390: There is no relationship between CR and BA, so we cannot think that planktonic bacterial respiration represent a major part of community respiration here.
L407: Do you think that Mediterranean coastal lagoons are really net O2 producers today? Any refs?

Supplement information
Rnight = (mean of NCP during night period)*duration of night period*60 (Soulié et al. 2021.
Citation: https://doi.org/10.5194/egusphere-2023-2782-RC1
- AC1: 'Reply on RC1', Tanguy Soulié, 14 Dec 2023
  
  Response to Referee Comment 1
  Dear Dr. Regaudie-de-Gioux,
  We deeply thank you for your helpful comments, improving the quality and accuracy of the manuscript. Please find in the attached document detailed explanations about how we have considered and answered each comment.
  Concerning the modifications made on the revised version of the manuscript explained in the present document, please note that:
  - additional sentences or words were highlighted in yellow
  - deleted sentences or words were written in red and crossed out
  
  Citation: https://doi.org/10.5194/egusphere-2023-2782-AC1
RC2:
'Comment on egusphere-2023-2782', Tamara Cibic, 04 Jan 2024

The work by Soulié et al. “Simulated terrestrial runoff shifts the metabolic balance of a coastal Mediterranean plankton community toward heterotrophy” investigated the consequences of terrestrial runoff on plankton communities and some biological processes in the Thau lagoon on the Mediterranean coast. The results come from an in situ mesocosm experiment in which terrestrial runoff was simulated by adding soil and various chemical and biological variables were analyzed for 18 days.
The paper is well written, focused and interesting and should be published in Biogeosciences after revision.
A major criticism of this work is the fact that no real phytoplankton data are presented. All results were derived from Chl-a sensor data, including phytoplankton growth and loss rates. I know this is becoming more common and accepted lately, but similarly to Chl-a fluorescence and oxygen sensors data, for which some calibrations were done, actual phytoplankton counts and identifications should have been done on at least some samples to check if there is a match between Chl-a and microphytoplankton. Since flow cytometry was used in the paper to estimate heterotrophic bacterial abundance, the same method could have been used to assess the smaller phototrophic picoplankton. It is a pity that there is no information on the actual composition of the phytoplankton, as this is the topic of the article. If the authors have these (already published or unpublished) results, I think it would be a great addition to this publication to at least mention them in the discussion.
Introduction
I think it would be easier for the reader if some scientific questions or hypotheses were added at the end of the introduction section to structure the discussion.
M&Ms
Experimental design
It is not stated what the final volume in each mesocosm is. It is also not clear if the mesocosms are sealed at the top and what the bottom is like. Are the mesocosms open or sealed at the bottom? Are they floating? Please add this information.
L76: The experiments were conducted for 18 days. In my opinion, this is a very long time to test the effects of a flash flood on the coastal area. There is a strong mixing effect by the seawater, and even in a confined area like a lagoon, the terrestrial runoff will eventually be diluted in a few days. The choice of the duration of the experiment should be discussed.
L104: Why was the sampled soil left to mature for two weeks? Why was this step necessary? In a flash flood there is no such step, the soil is washed away directly by the heavy rain and transported into a river and eventually into an estuary. Flash floods do not last 14 days, this is unclear and should be better explained.
Discussion
What I miss here is a discussion of the ecological implications of these results at the lagoon mesoscale. In particular, a detailed discussion of the trophic state of the lagoon and a comparison with other Mediterranean lagoons.

Citation: https://doi.org/10.5194/egusphere-2023-2782-RC2
- AC2:
  'Reply on RC2', Tanguy Soulié, 17 Jan 2024
  
  Dear Dr. Cibic,
  We deeply thank you for your helpful comments, improving the quality and accuracy of the manuscript. Please find in the attached document detailed explanations about how we have considered and answered each comment.
  Concerning the modifications made on the revised version of the manuscript explained in the present document, please note that:
  - additional sentences or words were highlighted in light blue
  - deleted sentences or words were written in purple and crossed out
  
  Citation: https://doi.org/10.5194/egusphere-2023-2782-AC2
  - AC3: 'Reply on AC2', Tanguy Soulié, 17 Jan 2024
    
    The comment was uploaded in the form of a supplement: https://egusphere.copernicus.org/preprints/2023/egusphere-2023-2782/egusphere-2023-2782-AC3-supplement.pdf
    
    Citation: https://doi.org/10.5194/egusphere-2023-2782-AC3

Peer review completion

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

ED: Publish subject to minor revisions (review by editor) (24 Jan 2024) by Frédéric Gazeau

AR by Tanguy Soulié on behalf of the Authors (24 Jan 2024) Author's response Author's tracked changes Manuscript

ED: Publish subject to minor revisions (review by editor) (18 Feb 2024) by Frédéric Gazeau

AR by Tanguy Soulié on behalf of the Authors (21 Feb 2024) Author's tracked changes Manuscript

EF by Polina Shvedko (22 Feb 2024) Author's response Supplement

ED: Publish as is (23 Feb 2024) by Frédéric Gazeau

AR by Tanguy Soulié on behalf of the Authors (26 Feb 2024) Manuscript

Journal article(s) based on this preprint

17 Apr 2024

Simulated terrestrial runoff shifts the metabolic balance of a coastal Mediterranean plankton community towards heterotrophy

Tanguy Soulié, Francesca Vidussi, Justine Courboulès, Marie Heydon, Sébastien Mas, Florian Voron, Carolina Cantoni, Fabien Joux, and Behzad Mostajir

Biogeosciences, 21, 1887–1902, https://doi.org/10.5194/bg-21-1887-2024,https://doi.org/10.5194/bg-21-1887-2024, 2024

Short summary

Tanguy Soulié, Francesca Vidussi, Justine Courboulès, Marie Heydon, Sébastien Mas, Florian Voron, Carolina Cantoni, Fabien Joux, and Behzad Mostajir

Supplement

https://doi.org/10.5194/egusphere-2023-2782-supplement

Data sets

Dataset from a mesocosm experiment testing the effects of a terrestrial runoff on a Mediterranean plankton community Soulié Tanguy, Vidussi Francesca, Courboulès Justine, Heydon Marie, Mas Sébastien, Voron Florian, Cantoni Carolina, Joux Fabien, Mostajir Behzad https://www.seanoe.org/data/00861/97260/

Tanguy Soulié, Francesca Vidussi, Justine Courboulès, Marie Heydon, Sébastien Mas, Florian Voron, Carolina Cantoni, Fabien Joux, and Behzad Mostajir

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Due to climate change, it is projected that extreme rainfall events, bringing terrestrial matter into coastal seas, will occur more frequently in the Mediterranean region. To test the effects of runoffs of terrestrial matter on plankton communities from Mediterranean coastal waters, an in situ mesocosm experiment was conducted. The simulated runoff affected key processes mediated by plankton, such as primary production and respiration, suggesting major consequences of such events.


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