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Article
Peer-Review Record

Phytoplankton Diversity Relates Negatively with Productivity in Tropical High-Altitude Lakes from Southern Ecuador

Sustainability 2019, 11(19), 5235; https://doi.org/10.3390/su11195235
by Alonso Cartuche, Ziyu Guan, Bastiaan W. Ibelings and Patrick Venail *
Reviewer 1: Anonymous
Reviewer 2: Anonymous
Sustainability 2019, 11(19), 5235; https://doi.org/10.3390/su11195235
Submission received: 10 September 2019 / Revised: 18 September 2019 / Accepted: 19 September 2019 / Published: 24 September 2019

Round 1

Reviewer 1 Report

Sustainability review

Overall, this is an interesting contribution, and the information is a useful addition to understanding the ecology of Tropical High-Altitude Lakes, particularly within the scope of the Ecuadorian freshwater systems examined.

I have some minor suggestions for the authors to consider in revising their text.

It may be helpful if the authors provide a brief explanation of the rationale for choosing the particular 24 lakes (Line 83) from the 75 available. It is clear that approximately half (11) are from the Amazon (eastern) mountain range and approximately half (13) from the Andes (western) range, but overall if there was some rationale for the sampling design, it would be of interest to some readers. That is, were the 24 approximately a random choice with half from the east and half from the west range, or basically what was done. The authors provide boundary information on the areas max. depths, and ranges for the altitudes which are helpful. Was the glutaraldehyde buffered and what concentration of glutaraldehyde was used (Line 96). Line 109, it would be helpful to be more detailed about how biovolume was determined, that is what metrics or algorithms (etc.) were used to convert microscopic measurements to volumes (µm3). Given the large variations in solid geometric shapes of some phytoplankton, it is difficult to fully interpret what the procedures were – if the authors used previously published protocols, it would be sufficient to cite the published sources. This is all the more important, among other aspects, because the authors report in the Discussion some interesting contrasting sources of results as follows: “Despite the positive correlation of chlorophyll-a with total phytoplankton biovolume observed in our dataset, the links between the different abiotic variables and total biovolume were weak. Among all the abiotic variables included in this study, only total phosphate concentration related to total phytoplankton  biovolume, explaining just 18% of its variation (versus 52% for chlorophyll-a).”

Clarifying how the biovolume was calculated, can help the reader better interpret such findings if the methodology is better explained. This is not a criticism of the report, or discussion of the findings, only a request to more clearly define how biovolumes were obtained across such as wide variety of phytoplankton morphologies.

Line 117, pi should be pi, that is a subscript I is needed (small typographical issue). Line 146, it would help to clarify the sentence to state “These two measures of phytoplankton diversity (genera richness and Shannon’s diversity index) were positively related ……etc. I presume these are the two measures of diversity referred to. Line 148, It might be interesting to mention either in the Results or in the Discussion, that although four of the variables are clearly statistically significant as cited, the altitude relationship with Chlorophyll-a is not the strongest accounting for approximately 19% of the variance (r2 of 0,428 = 0,19). Also, I note a small contradiction in values in Table 2 compared to Figure 2 for correlation of Total phosphates and Log biovolume (Table 2 value is 0,428 and Figure 2 value is 0,429). Lines 163-165. The observation that the phytoplankton production in the lakes might be phosphorus limited is worthy of note, but phosphate is also a common limiting nutrient in freshwater systems compared to marine systems, for example, where nitrate is more commonly a limiting nutrient. Line 168, to direct the reader to the exact source of the information it would be helpful to repeat that this is found in Figure 3 “Taxa richness was not related to either chlorophyll-a 168 concentrations or total phytoplankton biovolumes. On the contrary, diversity was negatively correlated to 169 both chlorophyll-a concentrations and total phytoplankton biovolumes (Figure 3).” Lines 172-173, recommend additional clarity in wording by including biovloume diversity rather than just phytoplankton diversity and also the other underlined wording, to depict, (the authors apparently did not determine diversity of genera, per se): “Regarding the negative relationship between  phytoplankton biovolume diversity and total biovolume (Figure 3, low right hand panel), a closer look at data allowed  us to depict some interesting trends. “

Subsequently, throughout the manuscript, please use the exact wording ‘ phytoplankton biovolume diversity ’ merely to make the reading more clear and interpretable.

Line 186, to be taxonomically more precise, please consider clarifying that these taxa are colonial diatoms (Synedra, Fragilaria, and Asterionella). It is morphologically accurate to categorize Mougeotia as a filamentous algae (family: Zygnemataceae). I am fairly confident that the authors recognize this finer detail, but it only is intended to make the text more precise for some readers. Lines 254-257. This observation is of interest, but is it not likely to be the case, given that the diversity is a measure of Shannon biovolume diversity across genera, so one would expect some covariation between total biovolume and Shannon biovolume diversity, simply due to the same data being used in the two quantitative estimates. If this involves my misinterpretation, perhaps the authors may want to make a clarifying statement somewhere in the text to help readers avoid such misinterpretations.

 

 

Author Response

Reviewer 1:

Overall, this is an interesting contribution, and the information is a useful addition to understanding the ecology of Tropical High-Altitude Lakes, particularly within the scope of the Ecuadorian freshwater systems examined.

R/ Thank you for the compliments.

I have some minor suggestions for the authors to consider in revising their text.

It may be helpful if the authors provide a brief explanation of the rationale for choosing the particular 24 lakes (Line 83) from the 75 available. It is clear that approximately half (11) are from the Amazon (eastern) mountain range and approximately half (13) from the Andes (western) range, but overall if there was some rationale for the sampling design, it would be of interest to some readers. That is, were the 24 approximately a random choice with half from the east and half from the west range, or basically what was done.

R/ We valuate the suggestion. The three largest lakes were intentionally included given their relative importance as the largest water reservoirs in the system. Those three lakes are in the western mountain range. The other 21 lakes were chosen randomly using a map. We added this information in the text (lines 86-88).

Was the glutaraldehyde buffered and what concentration of glutaraldehyde was used.

R/ We purchased 70% glutaraldehyde that we diluted to 1% and neutralized to pH 7 with NaOH. We added this information in the text (lines 101-102).

Line 109, it would be helpful to be more detailed about how biovolume was determined, that is what metrics or algorithms (etc.) were used to convert microscopic measurements to volumes (µm3). Given the large variations in solid geometric shapes of some phytoplankton, it is difficult to fully interpret what the procedures were – if the authors used previously published protocols, it would be sufficient to cite the published sources. This is all the more important, among other aspects, because the authors report in the Discussion some interesting contrasting sources of results as follows: “Despite the positive correlation of chlorophyll-a with total phytoplankton biovolume observed in our dataset, the links between the different abiotic variables and total biovolume were weak. Among all the abiotic variables included in this study, only total phosphate concentration related to total phytoplankton biovolume, explaining just 18% of its variation (versus 52% for chlorophyll-a).” Clarifying how the biovolume was calculated, can help the reader better interpret such findings if the methodology is better explained. This is not a criticism of the report, or discussion of the findings, only a request to more clearly define how biovolumes were obtained across such as wide variety of phytoplankton morphologies.

R/ Thank you for this suggestion. Given the plethora of cellular forms that we observed, we used different formulae for the calculation of cell biovolumes. We decided to add five examples of the more representative forms as supplementary material.

Line 117, pi should be pi, that is a subscript I is needed (small typographical issue).

R/ Corrected.

Line 146, it would help to clarify the sentence to state “These two measures of phytoplankton diversity (genera richness and Shannon’s diversity index) were positively related ……etc. I presume these are the two measures of diversity referred to.

R/ Than you, we corrected it.

Line 148, It might be interesting to mention either in the Results or in the Discussion, that although four of the variables are clearly statistically significant as cited, the altitude relationship with Chlorophyll-a is not the strongest accounting for approximately 19% of the variance.

R/ We appreciate this comment. Indeed, the coefficient for the correlation between altitude and chlorophyll-a concentration was 0,436 (Table 2), meaning that the variance explained was 19%. We added this information in the document (lines 164-166).

Also, I note a small contradiction in values in Table 2 compared to Figure 2 for correlation of Total phosphates and Log biovolume (Table 2 value is 0,428 and Figure 2 value is 0,429).

R/ Thanks for noticing. We corrected Table 2.

Lines 163-165. The observation that the phytoplankton production in the lakes might be phosphorus limited is worthy of note, but phosphate is also a common limiting nutrient in freshwater systems compared to marine systems, for example, where nitrate is more commonly a limiting nutrient.

R/ We agree, thanks for the comment. Given the information that we have, we prefer avoiding much speculation about the limiting factors.

Line 168, to direct the reader to the exact source of the information it would be helpful to repeat that this is found in Figure 3 “Taxa richness was not related to either chlorophyll-a concentrations or total phytoplankton biovolumes. On the contrary, diversity was negatively correlated to both chlorophyll-a concentrations and total phytoplankton biovolumes (Figure 3).”

R/ Done.

Lines 172-173, recommend additional clarity in wording by including biovolume diversity rather than just phytoplankton diversity and also the other underlined wording, to depict, (the authors apparently did not determine diversity of genera, per se): “Regarding the negative relationship between  phytoplankton biovolume diversity and total biovolume (Figure 3, low right hand panel), a closer look at data allowed  us to depict some interesting trends.” Subsequently, throughout the manuscript, please use the exact wording ‘phytoplankton biovolume diversity’ merely to make the reading more clear and interpretable.

R/ Thanks for the suggestion. We have modified the document accordingly and improved the explanation of this variable in the methods section.

Line 186, to be taxonomically more precise, please consider clarifying that these taxa are colonial diatoms (Synedra, Fragilaria, and Asterionella). It is morphologically accurate to categorize Mougeotia as a filamentous algae (family: Zygnemataceae). I am fairly confident that the authors recognize this finer detail, but it only is intended to make the text more precise for some readers.

R/ We edited the document accordingly.

Lines 254-257. This observation is of interest, but is it not likely to be the case, given that the diversity is a measure of Shannon biovolume diversity across genera, so one would expect some covariation between total biovolume and Shannon biovolume diversity, simply due to the same data being used in the two quantitative estimates. If this involves my misinterpretation, perhaps the authors may want to make a clarifying statement somewhere in the text to help readers avoid such misinterpretations.

R/ We understand the confusion this may have generated. The Shannon’s diversity index used in this study is based on the contribution of each genera’s biovolume to total biovolume (not in abundances). Thus, it is a measure of the evenness in the distribution of total biovolume across the different genera in a sample/lake. Lakes can reach higher total biovolumes in two ways. First, by having a more even distribution of biovolumes across taxa (higher Shannon’s index). Second, by having a few taxa contributing more to total biovolume, which means having lower Shannon’s index values. The first option would result in a positive correlation between phytoplankton biovolume diversity and total biovolume. The second option would lead to a negative relationship. This is what we observed in our dataset. This means that the covariation between biovolume diversity and total biovolume is not really expected. We added some lines of explanation in the document (lines 125-131).

We would like to thank you for the constructive comments and suggestions.

Reviewer 2 Report

Phytoplankton Diversity Relates Negatively with Productivity due to Strong Compositional Effects in Tropical High-Altitude Lakes in Ecuador are assessed in the paper. In the paper the authors explored the links between several environmental variables and productivity, measured as chlorophyll-a concentration and total phytoplankton bio volume, across twenty-four tropical high-altitude lakes located over three-thousand meters above sea level. I believe that the paper will be published, but I would appreciate if the authors add some points to the manuscript after moderate revision.

 

General comments

The novelty of the study it is not clear and it should be mentioned at the end of “Introduction” The writing of the manuscript it’s not academic, it should be revised. Some sentences in the manuscript is too long and they should be rewrite and summarize.

 

Technical comments

The title of manuscript seems too long. It better to short it. The authors in the title of manuscript mentioned that “Phytoplankton Diversity Relates Negatively with Productivity due to Strong Compositional Effects in Tropical …” what do authors mean by “Strong Compositional Effects”? In the abstract the sentence in lines 12-15 is too long. Line 15-16 should be revised to better academic form. In the “Introduction”, some past related works recommended to be referred. A sensitivity analysis of Lake water level response to changes in climate and river regimes. Phytoplankton Composition and Water Quality of Kamil Abduş Lagoon (Tuzla Lake), Istanbul-Turkey Design of environmental flow regimes to maintain lakes and wetlands in regions with high seasonal irrigation demand. Determination of the distribution of phytoplankton related to water quality in sea bass (Dicentrarchus labrax) FARMING LAND PONDS (Muğla, Turkey) Can lake sensitivity to desiccation be predicted from lake geometry?

 

Line 20-22 should be revised to better academic form “We hope this study will…” The legend of the Figure 1 has low quality and some text that it’s not clear. It should be improve by quality. In the Fig 1. There is no any scale!!!!!!! As authors mentioned in the section of method: The field work was performed in November 2016. Following they mentioned “Water samples for nutrient analyses were collected in 10 ml plastic acid-washed…” are they in the same date or not? If they are not in the same. How authors justify this matter? The lines 29-32 “Like high altitude temperate lakes, tropical high-altitude lakes (hereafter TRHALs) have low average water temperatures that are negatively related to altitude and cloud cover as a determinant of solar incidence. TRHALs also can have extreme diel water temperature variations, are submitted to strong winds and receive intense solar UV radiations”. Should be address. In the Table 1. The authors mentioned the list of studies about the relationship between phytoplankton diversity and functioning around the world. What is the main differences between your study and other studies as you listed them. Line 66-68 should be revised to better understand for readers. In the manuscript the “Conclusions” didn’t consider by the authors. It is important to consider it. Check the references list and modify them based on journal style.

 

 

Author Response

Reviewer 2:

The novelty of the study it is not clear and it should be mentioned at the end of “Introduction”

R/ Thank you for the suggestion. Our introduction includes a new sentence that highlights the novelty of our study. 

The writing of the manuscript it’s not academic, it should be revised. Some sentences in the manuscript are too long and they should be rewrite and summarize.

R/ We went through the entire document and edited some sentences to improve their accessibility.

The title of manuscript seems too long. It better to short it. The authors in the title of manuscript mentioned that “Phytoplankton Diversity Relates Negatively with Productivity due to Strong Compositional Effects in Tropical …” what do authors mean by “Strong Compositional Effects”?

R/ Thanks for the suggestion. We shortened the title by removing the mention to “strong compositional effect”. We agree that the use of “compositional effect” was not very clear. We deleted this term form the entire document.

In the abstract the sentence in lines 12-15 is too long.

R/ We split the sentence in two shorter sentences.  

Line 15-16 should be revised to better academic form.

R/ We edited the sentence.

In the “Introduction”, some past related works recommended to be referred.

A sensitivity analysis of Lake water level response to changes in climate and river regimes. Phytoplankton Composition and Water Quality of Kamil Abduş Lagoon (Tuzla Lake), Istanbul-Turkey Design of environmental flow regimes to maintain lakes and wetlands in regions with high seasonal irrigation demand. Determination of the distribution of phytoplankton related to water quality in sea bass (Dicentrarchus labrax) FARMING LAND PONDS (Muğla, Turkey) Can lake sensitivity to desiccation be predicted from lake geometry?

R/ We appreciate this suggestion. We carefully read these five publications. We found that the studies entitled: Phytoplankton Composition and Water Quality of Kamil Abduş Lagoon (Tuzla Lake), Istanbul-Turkey and Determination of the distribution of phytoplankton related to water quality in sea bass (Dicentrarchus labrax) FARMING LAND PONDS (Muğla, Turkey) are very interesting. They both include detailed information on phytoplankton community composition but not in the context of biodiversity-ecosystem functioning. While interesting too, the other three publications are not much in the research area of our study. Thus, we decided not to include them as references in this study.

Line 20-22 should be revised to better academic form “We hope this study will…”

R/ We edited the sentence.

The legend of the Figure 1 has low quality and some text that it’s not clear. It should be improve by quality. In the Fig 1. There is no any scale!!!!!!!

R/ We edited the figure and improved its quality. We removed the legend and added a scale.

As authors mentioned in the section of method: The field work was performed in November 2016. Following they mentioned “Water samples for nutrient analyses were collected in 10 ml plastic acid-washed…” are they in the same date or not? If they are not in the same. How authors justify this matter?

R/ Yes, water samples were taken the same day as the in situ measurements. We added this into the text.

The lines 29-32 “Like high altitude temperate lakes, tropical high-altitude lakes (hereafter TRHALs) have low average water temperatures that are negatively related to altitude and cloud cover as a determinant of solar incidence. TRHALs also can have extreme diel water temperature variations, are submitted to strong winds and receive intense solar UV radiations”. Should be address.

R/ We edited this section to improve clarity.

In the Table 1. The authors mentioned the list of studies about the relationship between phytoplankton diversity and functioning around the world. What is the main differences between your study and other studies as you listed them.

R/ As we explained in the text (lines 60-62), to our knowledge, no study about the relationship between phytoplankton diversity and functioning has been performed in tropical high-altitude lakes before.

Line 66-68 should be revised to better understand for readers.

R/ We edited the sentence.

In the manuscript the “Conclusions” didn’t consider by the authors. It is important to consider it.

R/ Given the simple message of our paper we want to avoid being redundant by adding a conclusion section that would reiterate what the discussion says.

Check the references list and modify them based on journal style.

R/ We carefully revised the reference list according to the journal’s instructions.  

We much appreciate your comments and suggestions that definitively helped us improving the manuscript.

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