Microzooplankton Communities in a Changing Ocean: A Risk Assessment
Round 1
Reviewer 1 Report
The manuscript "Microzooplankton communities in a changing climate: a risk assessment" reviews the existing literature to conduct a risk assessment of the impact of climate change factors (temperature, pH, oxygen) on microzooplankton. As such, this study is very timely and addresses an important gap in the literature. I believe that this manuscript would be of interest for a broad readership. While I generally support this manuscript, there are several structural aspects which need to be improved and changed.
Major comments:
Overall the introduction does not really reflect the current knowledge status on microzooplankton. While I support the current study, and I agree that an analysis of the effects of climate change on microzooplankton is needed, the introduction does not present a fair overview of the state of the art on microzooplankton climate change research. Several studies have pointed out that the microbial loop, and microzooplankton in particular should benefit from climate change. This must be acknowledged.
l.97-98 I am very surprised that the current study does not consider eutrophication. Quite a few papers have been published on the influence of eutrophication microzooplankton and it would be a very useful addition. I therefore think that these studies, and the effect of eutrophication on microzooplankton should be added to the current manuscript. This goes beyond the studies presented in the short paragraph on N:P ratios.
I think that the approach taken to evaluate the impact of climate change on microzooplankton should be more objective. By nature, the way the analysis is conducted highlight the “vulnerability” of organisms to stressors. I would refrain from emphasizing the negativity of the response, and instead highlight whether the effects are very negative (- -), negative (-), neutral (0), positive (+), or very positive (+ +). This is particularly important since the major outcome of the study is that microzooplankton may benefit from climate change. However, this message gets a bit lost since the emphasis is played on “vulnerability”.
Moreover, the manuscript would tremendously benefit from an outlook part on the implications of the results. Firstly, the author should take the effects of the 3 (4 with eutrophication and N:P ratios) stressors altogether and discuss how microzooplankton communities may change in the future as they will be subjected to the concurrent effects of these stressors. Secondly, the consequences for food web functioning, nutrient cycles etc. should be discussed. This is a major gap in the current manuscript.
Minor comments:
The manuscript is generally well written but there are a few minor issues, for example:
l.28 and 29 Microzooplankton is used as a plural noun (encompass, their) but later, for example on line 35, it is use in the singular. While I have no strong opinion on whether this word should be plural or singular, it needs to be consistent.
l.35 „significant“
l.37 the link to the carbon pump is unclear
l.42-43 “transfer environmental signals” is very vague
l.48 I disagree that the diversity of microzooplankton is the limiting factor. I rather think that we simply do not have enough information and that before the present study, no integration had been made. If diversity is the limiting element, then no integration at the “microzooplankton” level should be possible (which would kill the idea of the current study). Instead, each functional unit within microzooplankton should be studied independently.
I would suggest to the author to have the manuscript proof read.
Author Response
Reviewer 1
Comments and Suggestions for Authors
The manuscript "Microzooplankton communities in a changing climate: a risk assessment" reviews the existing literature to conduct a risk assessment of the impact of climate change factors (temperature, pH, oxygen) on microzooplankton. As such, this study is very timely and addresses an important gap in the literature. I believe that this manuscript would be of interest for a broad readership. While I generally support this manuscript, there are several structural aspects which need to be improved and changed.
Major comments:
Overall the introduction does not really reflect the current knowledge status on microzooplankton. While I support the current study, and I agree that an analysis of the effects of climate change on microzooplankton is needed, the introduction does not present a fair overview of the state of the art on microzooplankton climate change research. Several studies have pointed out that the microbial loop, and microzooplankton in particular should benefit from climate change. This must be acknowledged.
I agree with this remark and appreciate reviewer’s viewpoint. The introduction section was reworked according to this suggestion (P2, L33-63).
l.97-98 I am very surprised that the current study does not consider eutrophication. Quite a few papers have been published on the influence of eutrophication microzooplankton and it would be a very useful addition. I therefore think that these studies, and the effect of eutrophication on microzooplankton should be added to the current manuscript. This goes beyond the studies presented in the short paragraph on N:P ratios.
Eutrophication was not included in the original version of the manuscript because it is not a climate-related driver. However, I do agree that its incorporation would benefit the present assessment as it deals with human-driven environmental changes. I have therefore added a new section reviewing the effects of this driver (P20, L591-673). An overview of this hazards was also added in the section “Climate-related hazards to planktonic communities” (P6, L188-198).
I think that the approach taken to evaluate the impact of climate change on microzooplankton should be more objective. By nature, the way the analysis is conducted highlight the “vulnerability” of organisms to stressors. I would refrain from emphasizing the negativity of the response, and instead highlight whether the effects are very negative (- -), negative (-), neutral (0), positive (+), or very positive (+ +). This is particularly important since the major outcome of the study is that microzooplankton may benefit from climate change. However, this message gets a bit lost since the emphasis is played on “vulnerability”.
The analysis used here is based on the methodological ensemble proposed by the Working Group II of the Intergovernmental Panel on Climate Change (IPCC). In order to reproduce the methodological protocol, I consider that all parametric categories proposed within this procedure must be included. However, I understand reviewer’s viewpoint and agree that the overall effect (either positive, negative or neutral) should be emphasised. Accordingly, I added a new column in Table 2 and included a motivation statement in the Methods section (P5, L153-154).
Moreover, the manuscript would tremendously benefit from an outlook part on the implications of the results. Firstly, the author should take the effects of the 3 (4 with eutrophication and N:P ratios) stressors altogether and discuss how microzooplankton communities may change in the future as they will be subjected to the concurrent effects of these stressors. Secondly, the consequences for food web functioning, nutrient cycles etc. should be discussed. This is a major gap in the current manuscript.
The consequences of the future changes on environmental hazards are somehow discussed in the corresponding sections as they were used to review the overall impact on microzooplankton. The consequences for food web functioning, nutrient cycles etc. are indeed an issue that needs further attention and is actually a field that deserves future research efforts. I have added a new section trying to summarize the available information using a carbon-flux approach (P24-25, L726-764).
Minor comments:
The manuscript is generally well written but there are a few minor issues, for example:
l.28 and 29 Microzooplankton is used as a plural noun (encompass, their) but later, for example on line 35, it is use in the singular. While I have no strong opinion on whether this word should be plural or singular, it needs to be consistent.
I checked the manuscript and homogenised the plural use of the term “microzooplankton”.
l.35 „significant“
Done.
l.37 the link to the carbon pump is unclear
The sentence was rewritten as follows:
“Their critical role in the biological carbon pump resides on their ability to repackage phytoplankton biomass and either respire carbon back to the atmosphere or transfer it to fast sinking mesozooplankton (Polimene et al. 2016). They also interfere in the microbial carbon pump (Jiao et al. 2010) through the ability of efficiently recycle nutrients that in turn delays the growth limitation of prey and prolongs the flow of carbon within the microbial food web (Armengol et al. 2019).” (P3, L75-81).
l.42-43 “transfer environmental signals” is very vague
The sentence was rewritten as follows:
“Microzooplankton are sensitive to most climate-related factors, and their responses to climate can produce cascading effects in marine food webs (Caron and Hutchins 2013).” (P3, L84-85).
l.48 I disagree that the diversity of microzooplankton is the limiting factor. I rather think that we simply do not have enough information and that before the present study, no integration had been made. If diversity is the limiting element, then no integration at the “microzooplankton” level should be possible (which would kill the idea of the current study). Instead, each functional unit within microzooplankton should be studied independently.
I understand reviewer’s viewpoint. To avoid misinterpretations, I have removed this sentence from the new version of the manuscript.
I would suggest to the author to have the manuscript proof read.
The English language was revised.
Reviewer 2 Report
The manuscript "Microzooplankton communities in a changing climate: a risk assessment" is a welcomed review on planktonic phagotrophic protist conservation biology. Using a simple risk assessment methodology, it concludes that the risk level to those protists under current and future climate change is rather low. Overall the article is good, well written, fairly detailed and fair in its assessment. I do have a few issues/questions/comments though.
My main one is with the idea of protists migrating poleward as mitigation process under increasing global temperature. First, i have a conceptual issue with the word migration in this context, and the issue although it sounds purely semantic does have an important consequence I think. By definition plankton movement is mostly controlled by the movement of the water mass. I think what we refer to as migration here is in fact range shifting over generations of planktonic organisms (rather than actual individuals moving on long distance, i. e. migration proper). Meaning that the speed of those shifts is somewhat dependent on the generational length (and to some extent of the regional oceanography), i. e. it somewhat varies from one species to the other (and from one basin to the next). Consequently not all species will "migrate" at the same speed, and may lag in relation to other species (and thus increase local competition over resources, with species shifting ranges faster acting as invasive species [the author does allude to this issue somewhat though around l.303]) and in relation to the environmental gradient responsible for the shift (and thus the shifting population ends up with suboptimal fitness in relation with the environment they currently are in [as mentioned in Jonkers et al. (2019) for instance]). That point put aside, yes there are evidences indeed of species shifting their range poleward to mitigate raising temperature, though some populations (e. g. the polar ones) can not and thus are at higher risk and this should be discuss. Also, paleontological evidence (in particular in polycystine radiolarians, e. g. Trubovitz et al. 2020 recently) show that the proportion of species that do not shift their range to mitigate global temperature shifts is not negligeable.
My second issue is that I do not see in the paper a clear explanation/justification for the statement that the low risk level has a "medium confidence level". What is the methodology to assess the confidence of the assessment? I do not see that clearly in Bindoff et al. 2019 or in the paper. I am assuming it is based on the overall agreement of the references as shown in Table 1 but the way this is compiled into a single confidence level is not spelled out in the paper.
Follows additional minor notes (lines by lines):
Table 1: some of those references are missing in the reference list (e. g. Stock et al. 2009). Also "Orsi et al. 2012" is given in the list for divesity loss in case od deoxygenation: is it Orsi et al. 2012a, Orsi et al. 2012b or both?
l. 191-192 Also Kvale et al. 2015 Potential increasing dominance of heterotrophy in the global ocean. Environmental Research Letters
l. 261 "8.5% of ciliates' morphospecies exhibit [...] endemism (Agatha 2011)" contrast with the TARA oceans related paper by Gimmler et al. (2016). Generally speaking I m surprised that no TARA related paper made it into the review, given the wealth of data they generated.
Author Response
Reviewer 2
Comments and Suggestions for Authors
The manuscript "Microzooplankton communities in a changing climate: a risk assessment" is a welcomed review on planktonic phagotrophic protist conservation biology. Using a simple risk assessment methodology, it concludes that the risk level to those protists under current and future climate change is rather low. Overall the article is good, well written, fairly detailed and fair in its assessment. I do have a few issues/questions/comments though.
My main one is with the idea of protists migrating poleward as mitigation process under increasing global temperature. First, i have a conceptual issue with the word migration in this context, and the issue although it sounds purely semantic does have an important consequence I think. By definition plankton movement is mostly controlled by the movement of the water mass. I think what we refer to as migration here is in fact range shifting over generations of planktonic organisms (rather than actual individuals moving on long distance, i. e. migration proper). Meaning that the speed of those shifts is somewhat dependent on the generational length (and to some extent of the regional oceanography), i. e. it somewhat varies from one species to the other (and from one basin to the next). Consequently not all species will "migrate" at the same speed, and may lag in relation to other species (and thus increase local competition over resources, with species shifting ranges faster acting as invasive species [the author does allude to this issue somewhat though around l.303]) and in relation to the environmental gradient responsible for the shift (and thus the shifting population ends up with suboptimal fitness in relation with the environment they currently are in [as mentioned in Jonkers et al. (2019) for instance]). That point put aside, yes there are evidences indeed of species shifting their range poleward to mitigate raising temperature, though some populations (e. g. the polar ones) can not and thus are at higher risk and this should be discuss. Also, paleontological evidence (in particular in polycystine radiolarians, e. g. Trubovitz et al. 2020 recently) show that the proportion of species that do not shift their range to mitigate global temperature shifts is not negligeable.
I appreciate this remark. More adequate terms (i.e. poleward range shift) was used to replace the term “migration”. Also, I added some text to emphasise the fact that some protists may not be able to mitigate warming by species’ relocation (P15, L414-425). Suggested citations were added into the text (P14, L375-378 - P15, L411-414) and in Table 1.
My second issue is that I do not see in the paper a clear explanation/justification for the statement that the low risk level has a "medium confidence level". What is the methodology to assess the confidence of the assessment? I do not see that clearly in Bindoff et al. 2019 or in the paper. I am assuming it is based on the overall agreement of the references as shown in Table 1 but the way this is compiled into a single confidence level is not spelled out in the paper.
Indeed, the confidence level is based on both the amount and the overall agreement of existing evidence. Compared to phytoplankton and mesozooplankton, evidence on the effects of climate change on microzooplankton is still scarce. For instance, studies dealing with acidification effects on microzooplankton have revealed contradictory results as for its indirect (prey-mediated) impacts. It is still not clear whether this is the result of an overall weak effect on microbial plankton or if there is still insufficient data to extract regularities. I added some text to clarify this issue in the Conclusion section:
“Compared to phytoplankton and mesozooplankton, the amount of data regarding the effects of microzooplankton to climate change is still limited. The lack of sustained observations on the field and under controlled laboratory conditions, prevents the identification of consistent regularities on several aspects of species- and community-level responses. Hence, to allow the emergence of trends beyond short-term variability, further investigations will be required to increase the confidence of the present assessment. In spite of these limitations, existing data evidence a general consensus on the robustness of microzooplankton communities under present and future climate change.” (P25, L768-774).
This issue was also clarified in the Methods section:
“The vulnerability at present day and future scenarios is assigned a confidence level based on the reference amount and agreement (i.e. the amount of available observations reporting effects of similar size and sign). Confidence levels are low, medium, high and very high, according to IPCC calibrated language.” (P5, L149-153).
Follows additional minor notes (lines by lines):
Table 1: some of those references are missing in the reference list (e. g. Stock et al. 2009). Also "Orsi et al. 2012" is given in the list for diversity loss in case of deoxygenation: is it Orsi et al. 2012a, Orsi et al. 2012b or both?
I have added the correct citation of Stock et al. 2009 to the reference list and checked for other missing references. The referred citation in Table 1 is Orsi et al. 2012b, this was amended in the new version of the manuscript.
191-192 Also Kvale et al. 2015 Potential increasing dominance of heterotrophy in the global ocean. Environmental Research Letters
I have added this reference (P11, L275).
l. 261 "8.5% of ciliates' morphospecies exhibit [...] endemism (Agatha 2011)" contrast with the TARA oceans related paper by Gimmler et al. (2016). Generally speaking I m surprised that no TARA related paper made it into the review, given the wealth of data they generated.
I entirely agree with this remark. I have added the following sentences:
“The Tara Oceans expedition, which uncovered unprecedented taxonomic discrimination of the majority of ciliate’s clades reported that only 17% of taxa were distributed among all oceanic regions. The analysis of DNA sequences, showed a close correlation between ciliate’s diversity and environmental factors of local relevance (temperature, chlorophyll, salinity, and inorganic nutrients) but no clear large-scale latitudinal gradients (Gimmler et al. 2016).” (P13, L355-360).
“The Tara Ocean expedition revealed that cosmopolitan ciliates had higher local abundances than ciliates with a restricted distribution, although in general, open-water species showed low diversity. This highlights the vulnerability of species with restricted distribution and narrow niches (Gimmler et al. 2016).” (P16, L442-445).
Reviewer 3 Report
This review entitled “Microzooplankton communities in a changing climate: a risk assessment” analyses the consequences of the current and future changes of the oceanic environmental conditions (warming, increase of pH, de-oxygenation, etc.) on the populations of microzooplankton.
This is a strongly complex task and difficult to summarize in a text of 13 pages. Please remember that this is an electronic journal, and extension is less limited than in the printed journals. It is complex because the microzooplankton is a heterogeneous group, and microbes experience a high versatility in the trophic modes and lifestyles (phagotrophic, mixotrophic, parasitism, mutualistic symbioses) than makes difficult to predict their responses to changing environmental conditions. In addition,
when compared to groups such as microalgae (coccolithophorids) or metazoans, the data are more limited, both the laboratory experimental data and the field data from monitoring programs. This review does not summarize and analyze quantitative data from other
publications, showing new graphs from these published data. This review is a successive list of comments on the results of other papers. Finally, the conclusions are presented with a subjective terminology “low, medium, high”, and only the de-oxygenation is reported to have a high impact.
When a problem is complex, the strategy must be to define the problem, to split it in small parts attacking each part.
If your target is the microzooplankton as reported in the title, first please define it. In the introduction is only reported: “Microzooplankton
encompass a heterogeneous group of phagotrophic and mixotrophic protists”. The prefix micro- is used for the organisms between 20-200
microns. For example, the dinoflagellate Noctiluca reaches a size of 2000microns, and it does not fit in the definition of microzooplankton.
Karlodinium veneficum is cited in the text, but it does not reach 20microns.
Phagotrophic is used as distinct from mixotrophic, but the mixotrophic organisms are also phagotrophic. Do you consider the dinoflagellate Dinophysis as mixotrophic? Has it permanent chloroplasts? Please do not confuse heterotrophic with phagotrophic. The definition of phagotrophy is the process of ingesting relatively large particles of food that carries out via intracellular digestion. In the text is cited Protoperidinium spp., do you know that these species fed by extracellular digestion?
First of all, please define the terminology that you will use.
line 33: microzooplankton collectively consume most primary production in marine ecosystems.
line 39: In addition, microzooplankton is able to photosynthesize, graze on prokaryotes, parasite,
Please delimit if the microzooplankton consume the primary production or it is a primary producer. Please delimit if the microzooplankton graze on parasite, and it is a parasite.
When a problem is complex, please consider the split. There are several options. The most common solution is the split into phylogenetic groups. A phylogenetic group has similar ultrastructure that physiological adaptation to the environmental changes. For example, fishes and dolphins have similar habitats and appearances. Fishes may have problems with the deoxygenation, while dolphins are expected to be less affected as they respire atmospheric air. Then, the phylogeny of each group determinates its physiological response. It seems coherent to organize this review into the main phylogenetic groups of the microplankton (alveolates: ciliates and dinoflagellates; rhizaria, stramenopiles, etc.). The author avoids the problem since the second sentence of the introduction “Their wide genetic variability and diverse ancestral origin has led to the adoption of non-phylogenetic classification consisting on grouping organisms that respond similarly to environmental factors or “functional types”. In that case, please define “functional types”.
Abstract line 20: “The highest risk is associated with the sensitivity to deoxygenation since microzooplankton, especially ciliates, are known to reduce metabolic rates under hypoxic conditions”. Please do not confuse the response in experiments of hypoxia with low levels of oxygen.
When I observe the high diversity and abundance of ciliates is low-oxygen environments such as the sediments of the mangroves, I wonder if a small decrease of the oxygen level will have a significant effect on the ciliates.
Line 441: Moreover, the survival of some ciliates and dinoflagellates to low oxygen is facilitated by the association with particular endosymbiotic bacteria, the ability to develop parasitism or to form resting stages (Orsi etal. 2012a, More et al. 2018).
What dinoflagellate? Please cite the dinoflagellate species. None of these publications (Orsi et al. 2012a, More et al. 2018) report any extant dinoflagellate. Low oxygen is related to the ability to develop parasitism? Please report the page where these authors report that information. According to table 1, only 5 references deal on the effect of the deoxygenation in microzooplankton, and none publication in the last four years. If really this is important problem, why there are no studies in the last 4 years? In the abstract is reported "and their capacity to migrate are". Please be careful of the use of –migrations- in the terrestrial sense: seasonal migration of the wildebeest in the Serengeti-Mara ecosystem. That does not exist for microplankton.
line 259: Although truly cosmopolitan species are rare. Wrong, the correct sentence is “Although truly endemic species are rare”.
Line 281: The Continuous Plankton Recorder (CPR). This paragraph deals on the CPR as a tool to evaluate the changes of the
populations of microzooplankton.
What is the microplankton? You cite Karlodinium veneficum of less than 18microns size. The Continuous Plankton Recorder (CPR) is a net that filter water. If you want to study the microplankton, will you use the Continuous Plankton Recorder? The mesh size of the plankton is 280 μm. The sample are fixed in formalin that fully destroys important groups of microzooplankton such as the ciliates. A rational researcher will never use that tool to study the microzooplankton and will ignore any results based on that method. The author reports examples of the poleward expansion of thermophilic species based on the CPR. Please read: Johns et al. 2003. Increased blooms of a dinoflagellate in the NW Atlantic MEPS 265:283-287 doi:10.3354/meps265283. The arctic dinoflagellate Ceratium arcticum expands into the temperate Atlantic Ocean.
Line 274: Similarly, a rage expansion of Noctiluca scintillans since 1860 from Australian coasts toward the Southern Ocean
Please check the misspellings.
line 274 a rage expansion,
line 189: This authors.
Please report the name of the person than studied the dinoflagellates in Australia in 1860 or before. The first studies on dinoflagellates in Australia began in the 1960’s (Wood 1963). The dinoflagellate study in the Southern Ocean began in the 1900’s. You have no data on the expansion of the “rage” of Noctiluca.
Line 293: “warming and wind patterns become more favourable to the development of diatoms leading to a progressive exclusion of
Protoperidinium spp.” This is an unfortunate sentence. If you observe the classical Margalef’s Mandala, the diatoms are not favoured by the warming. For that reason, the blooms of diatoms occur in winter and spring. Dinoflagellates are favoured by warming, for that reason the red-tides of dinoflagellates occur preferentially in summer. Warming is not leading to a progressive exclusion of Protoperidinium.
Diatoms are main prey of Protoperidinium spp.
Author Response
Reviewer 3
Comments and Suggestions for Authors
This review entitled “Microzooplankton communities in a changing climate: a risk assessment” analyses the consequences of the current and future changes of the oceanic environmental conditions (warming, increase of pH, de-oxygenation, etc.) on the populations of microzooplankton.
This is a strongly complex task and difficult to summarize in a text of 13 pages. Please remember that this is an electronic journal, and extension is less limited than in the printed journals. It is complex because the microzooplankton is a heterogeneous group, and microbes experience a high versatility in the trophic modes and lifestyles (phagotrophic, mixotrophic, parasitism, mutualistic symbioses) than makes difficult to predict their responses to changing environmental conditions. In addition, when compared to groups such as microalgae (coccolithophorids) or metazoans, the data are more limited, both the laboratory experimental data and the field data from monitoring programs. This review does not summarize and analyze quantitative data from other publications, showing new graphs from these published data. This review is a successive list of comments on the results of other papers. Finally, the conclusions are presented with a subjective terminology “low, medium, high”, and only the de-oxygenation is reported to have a high impact.
Overall, I agree with reviewer’s comments. All aspect that may obscure a confident assessment of microzooplankton response to climate trends have been mentioned in the introduction section. The terminology used here follows that proposed by the Working Group II of the Intergovernmental Panel on Climate Change (IPCC). This methodology has recently gained acceptance given the urgent need to extract meaningful information to direct mitigation actions. The procedure is intended to rapidly visualize the impacts and risk of either ecosystems or biotic components, as a function of climate threats (reviewed in Zommers et al. 2020, Nature Reviews Earth & Environment, https://doi.org/10.1038/s43017-020-0088-0). Consequently, although the exact methodology was not reproduced in this manuscript, I consider that major attempts to reproduce consensual methodological procedures must be made in order to optimize communication.
When a problem is complex, the strategy must be to define the problem, to split it in small parts attacking each part.
If your target is the microzooplankton as reported in the title, first please define it. In the introduction is only reported: “Microzooplankton encompass a heterogeneous group of phagotrophic and mixotrophic protists”. The prefix micro- is used for the organisms between 20-200 microns. For example, the dinoflagellate Noctiluca reaches a size of 2000microns, and it does not fit in the definition of microzooplankton.
Karlodinium veneficum is cited in the text, but it does not reach 20microns.
I introduced the definition of microzooplankton as employed in this manuscript. The following was added in the Methods section:
“The term microzooplankton as used here, encompasses no predetermined size range as in Sieburth et al. (1978). Instead, the term encompasses protistan organisms with the ability to consume prey by different mechanisms, although this may not be the unique energy acquisition method. That is, many protists are able to combine phago-heterotrophy with a phototrophic mode of nutrition in variable degrees. Hence, the term microzooplankton used here includes several functional types as described in Mitra et al. (2016): phago-heterotrophs, constitutive mixotrophs, generalist non-constitutive mixotrophs, plastidic specialist-non-constitutive mixotrophs and endosymbiotic specialist-non-constitutive mixotrophs. Parasitic forms are not included in the present assessment.” (P5, L155-163).
Phagotrophic is used as distinct from mixotrophic, but the mixotrophic organisms are also phagotrophic. Do you consider the dinoflagellate Dinophysis as mixotrophic? Has it permanent chloroplasts?
The definition of mixotrophs was clarified in the introduction section (P2-3, L65-68).
Please do not confuse heterotrophic with phagotrophic. The definition of phagotrophy is the process of ingesting relatively large particles of food that carries out via intracellular digestion. In the text is cited Protoperidinium spp., do you know that these species fed by extracellular digestion?
First of all, please define the terminology that you will use.
The term “phagotrophic” was revised in the entire manuscript and replaced by “phago-heterotrophic” to refer to the general mechanism of energy acquisition by consumption of macromolecules. The term phagotrophy was only used in specific cases in which trophic modes were documented (e.g. Ochromonas sp., Karlodinium sp.).
line 33: microzooplankton collectively consume most primary production in marine ecosystems.
line 39: In addition, microzooplankton is able to photosynthesize, graze on prokaryotes, parasite,
Please delimit if the microzooplankton consume the primary production or it is a primary producer. Please delimit if the microzooplankton graze on parasite, and it is a parasite.
The term parasite was removed from the new version of the manuscript since although there are many parasitic protists, these are not included in the present assessment. Here, I consider protists with the ability to consume prey as (non-exclusive) energy acquisition mode.
When a problem is complex, please consider the split. There are several options. The most common solution is the split into phylogenetic groups. A phylogenetic group has similar ultrastructure that physiological adaptation to the environmental changes. For example, fishes and dolphins have similar habitats and appearances. Fishes may have problems with the deoxygenation, while dolphins are expected to be less affected as they respire atmospheric air. Then, the phylogeny of each group determinates its physiological response. It seems coherent to organize this review into the main phylogenetic groups of the microplankton (alveolates: ciliates and dinoflagellates; rhizaria, stramenopiles, etc.). The author avoids the problem since the second sentence of the introduction “Their wide genetic variability and diverse ancestral origin has led to the adoption of non-phylogenetic classification consisting on grouping organisms that respond similarly to environmental factors or “functional types”. In that case, please define “functional types”.
I agree with this remark. Unfortunately, not enough data is available to confidently individualize climate responses on phylogenetic groups. This approach, however, should certainly guide future research to better individualize and anticipate climate impacts.
Here I focus on a simplified model of the microbial food web in which phago-heterotrophic protists are categorized into functional groups in order to avoid the complex definition of species. Under this approach, microzooplankton is defined as potential grazers able to ingest carbon from prey and redirect it back to the atmosphere by respiration or toward higher trophic levels. This approach allows to reduce the complexity of the system in order to identify pattern and mechanisms. Within this definition, several functional types are recognized (Mitra et al. 2016, Protist, http://dx.doi.org/10.1016/j.protis.2016.01.003). This classification was added in the methods section. (P5, L155-163).
Abstract line 20: “The highest risk is associated with the sensitivity to deoxygenation since microzooplankton, especially ciliates, are known to reduce metabolic rates under hypoxic conditions”. Please do not confuse the response in experiments of hypoxia with low levels of oxygen.
When I observe the high diversity and abundance of ciliates is low-oxygen environments such as the sediments of the mangroves, I wonder if a small decrease of the oxygen level will have a significant effect on the ciliates.
I understand reviewer’s point. In this manuscript, the assessment of microzooplankton vulnerability to de-oxygenation (and all other hazard here considered), is not exclusively focused on the adaptive capacity of protistan communities as a whole. That is, while specialized protist are able to tolerate environmental conditions well outside the tolerance range of most protistan counterparts, I here also focus on the magnitude of environmental change a protistan species may experience along several generations as a consequence of climate change. From a species-level point of view, experimental data reveal essential information regarding the potential effects on organisms when exposed to either progressive trends or episodic events outside their optimal environmental conditions. The occurrence of sub-optimal or even lethal conditions is particularly relevant for certain hazards such as de-oxygenation, which may manifest as episodic events associated with coastal eutrophication.
At the community level, highly specialized species will certainly tolerate the future trend of ocean de-oxygenation, but the overall effect will be a replacement of local unspecialized species by tolerant ones. In order to clarify this issue, I rewrote the corresponding text in the Abstract (P1, L22-25) and in Section 3. De-oxygenation (P20, 583-586).
Line 441: Moreover, the survival of some ciliates and dinoflagellates to low oxygen is facilitated by the association with particular endosymbiotic bacteria, the ability to develop parasitism or to form resting stages (Orsi etal. 2012a, More et al. 2018).
What dinoflagellate? Please cite the dinoflagellate species. None of these publications (Orsi et al. 2012a, More et al. 2018) report any extant dinoflagellate. Low oxygen is related to the ability to develop parasitism? Please report the page where these authors report that information.
The sentences refers to the ability of dinoflagellates to form cysts (not to perform a parasitic mode of nutrition) as a potential strategy to survive under low ambient oxygen conditions (More et al. 2018, page 255). This sentence was rewritten as follows to clarify these concepts:
“Moreover, under low oxygen conditions, the survival of some ciliates is facilitated by the association with particular endosymbiotic bacteria, while dinoflagellates may form resting stages to overcome adverse conditions (Orsi et al. 2012a, More et al. 2018).” (P19, L559-562).
According to table 1, only 5 references deal on the effect of the deoxygenation in microzooplankton, and none publication in the last four years. If really this is important problem, why there are no studies in the last 4 years?
This is a fair point. However, evidence do exist on the vulnerability of some ciliates to hypoxia. I rewrote the sentence in the abstract section in order to reduce the relevance given to this hazard as a factor producing negative responses at the community level as follows:
At the individual level, the highest risk is associated with the sensitivity to de-oxygenation since microzooplankton, especially ciliates, are known to reduce metabolic rates under hypoxic conditions, however, vulnerable species can be readily replaced by specialized taxa from a similar functional type (P1, L22-25).
In the abstract is reported "and their capacity to migrate are". Please be careful of the use of –migrations- in the terrestrial sense: seasonal migration of the wildebeest in the Serengeti-Mara ecosystem. That does not exist for microplankton.
The term “migration” was removed and replaced by “range expansion” or similar.
line 259: Although truly cosmopolitan species are rare. Wrong, the correct sentence is “Although truly endemic species are rare”.
This text was removed from the new version of the manuscript. The new sentence reads as follows:
“The delimitation of microzooplankton species distribution is often challenging as significant dispersion limits do not exist in the ocean. A review analysis revealed that only 8.5% of ciliates’ morphospecies exhibit restricted distribution or endemism (Agatha 2011).” (P13, L353-355).
Line 281: The Continuous Plankton Recorder (CPR). This paragraph deals on the CPR as a tool to evaluate the changes of the populations of microzooplankton.
What is the microplankton? You cite Karlodinium veneficum of less than 18microns size. The Continuous Plankton Recorder (CPR) is a net that filter water. If you want to study the microplankton, will you use the Continuous Plankton Recorder? The mesh size of the plankton is 280 μm. The sample are fixed in formalin that fully destroys important groups of microzooplankton such as the ciliates. A rational researcher will never use that tool to study the microzooplankton and will ignore any results based on that method. The author reports examples of the poleward expansion of thermophilic species based on the CPR. Please read: Johns et al. 2003. Increased blooms of a dinoflagellate in the NW Atlantic MEPS 265:283-287 doi:10.3354/meps265283. The arctic dinoflagellate Ceratium arcticum expands into the temperate Atlantic Ocean.
I agree that the CPR has many constrains since net tows do not conservatively assess species relative abundance neither it preserves unarmoured cells’ integrity. These constrains were introduced in the new version of the manuscript as follows:
“The relatively large pore size of the plankton net contained in the CPR (270 µm), determines that phytoplankton and microzooplankton size classes are not conservatively sampled. Also, delicate, unarmoured organisms are frequently damaged by the sample filtration and retention mechanisms. Consequently, the information provided by this tool is limited and researches have relied only on group specific trends of large, armoured species such as dinoflagellates and diatoms (McQuatters-Gollop et al. 2015).” (P14, L389-395).
Taken cautiously, CPR data may provide helpful information. In particular, this tool does not provide reliable information of species composition, richness and short-term abundance patterns of unarmoured and small species, but the general, non-quantitative trend of abundance and distribution of species that are integrally retained in the silk mesh may by depicted over long periods of time. The two studies cited here (Hinder et al. 2012a,b), are based on armoured species (thecated dinoflagellates and tintinnids) that may resist cell damage during the sampling, however, cell size of targeted species are smaller than the silk mesh. Authors account for this sampling caveat and argue that their results are semi-quantitative. In addition, they emphasize the fact that the sampling of very small species (Dictyocysta spp.) remained consistent over time and even denoted a positive trend during the monitoring. This denotes that in spite of its large limitations, CPR is a useful tool to glance at the long-term trend of plankton in the open ocean.
This concerns are now explicitly mentioned in the manuscript.
Finally, I added some text discussing the results obtained by Johns et al. (2003) in order to highlight that the geographic range shifts of microzooplankton may not always respond to global/regional climate trends. (P15, L433-437).
Line 274: Similarly, a rage expansion of Noctiluca scintillans since 1860 from Australian coasts toward the Southern Ocean
Please check the misspellings.
line 274 a rage expansion,
Done.
line 189: This authors.
Done.
Please report the name of the person than studied the dinoflagellates in Australia in 1860 or before. The first studies on dinoflagellates in Australia began in the 1960’s (Wood 1963). The dinoflagellate study in the Southern Ocean began in the 1900’s. You have no data on the expansion of the “rage” of Noctiluca.
The correct year is 1960, this was amended in the new version of the manuscript.
Line 293: “warming and wind patterns become more favourable to the development of diatoms leading to a progressive exclusion of Protoperidinium spp.” This is an unfortunate sentence. If you observe the classical Margalef’s Mandala, the diatoms are not favoured by the warming. For that reason, the blooms of diatoms occur in winter and spring. Dinoflagellates are favoured by warming, for that reason the red-tides of dinoflagellates occur preferentially in summer. Warming is not leading to a progressive exclusion of Protoperidinium. Diatoms are main prey of Protoperidinium spp.
The sentence was rewritten as follows:
“During this period, a shift in local wind patterns promoted water mixing and turbulence. Authors suggested that increased turbulence may have promoted the retention of diatoms within illuminated layers and that under these conditions outcompeted dinoflagellates leading to their progressive exclusion (Hinder et al. 2012a).” (P15, L407-411).
Round 2
Reviewer 3 Report
It is difficult to evaluate this review because the topic is quite difficult due to the high versatility and diversity of ecological characteristics of the microzooplankton. Any section is susceptible to receive criticisms, and the review process can be eternal. Under these circumstances, this review manuscript must be regarded as a compilation of results, unable to provide quantitative conclusions. It is not easy to review the succession of ecological concepts and terminologies. I disagree in many aspects with the author and the conclusions are questionable. However, I consider that this manuscript is an opportunity to open discussions.
The title is "Microzooplankton communities in a changing climate". In this revised version, there is a new section about the coastal eutrophication. I assume that this is due to the comments of other reviewer. If you include the coastal eutrophication, you must modify the title because the coastal eutrophication is not fully derived from the climate changes. Coastal eutrophication existed in the Ancient Egypt before the industrial revolution and massive CO2 emissions. This manuscript is already very long, and to add a new section is unfortunate. I recommend removing the coastal eutrophication
This manuscript uses hundreds of concepts and terms on ecology. For example:
line 25: onferring stability to marine food webs
What is stability in marine food webs?
The term phago-heterotrophic does not exist. The author is confused due to the huge diversity of nutritional modes of the microzooplankton.
line 149: Parasitic forms are not included in the present assessment.
It is unfortunate to exclude the parasites, but certainly, this requires other review.
Please check for a few misspellings:
line 19: specie’s range
In conclusion, this reviewer and many of the readers will disagree with the conclusions of this review. However, the microzooplancton and climate have received less attention than other groups, and this compilation of information is useful. More than to recommend the publication of this manuscript, I will not oppose to the publication, as a way to open the discussion in this difficult topic. Please remove the section of coastal eutrophication because it is not directly linked to the climate, increasing excessively the extension of the manuscript.
Author Response
It is difficult to evaluate this review because the topic is quite difficult due to the high versatility and diversity of ecological characteristics of the microzooplankton. Any section is susceptible to receive criticisms, and the review process can be eternal. Under these circumstances, this review manuscript must be regarded as a compilation of results, unable to provide quantitative conclusions. It is not easy to review the succession of ecological concepts and terminologies. I disagree in many aspects with the author and the conclusions are questionable. However, I consider that this manuscript is an opportunity to open discussions.
The title is "Microzooplankton communities in a changing climate". In this revised version, there is a new section about the coastal eutrophication. I assume that this is due to the comments of other reviewer. If you include the coastal eutrophication, you must modify the title because the coastal eutrophication is not fully derived from the climate changes. Coastal eutrophication existed in the Ancient Egypt before the industrial revolution and massive CO2 emissions. This manuscript is already very long, and to add a new section is unfortunate. I recommend removing the coastal eutrophication.
I agree that eutrophication is not a climate-related driver and the title and the terminology used throughout the manuscript was modified accordingly.
Also, I agree that the length of the current version of the manuscript, with the inclusion of coastal eutrophication, may discourage wide readership. But the available literature regarding this issue is broad enough to warrant a confident assessment that may add some usefulness to the present manuscript.
I would be pleased that this manuscript opens the debate regarding the environmental feedbacks of microzooplankton in a future ocean, and that it encourages new hypothesis-based research. This is a surprisingly understudied topic and considering the critical role of microzooplankton within microbial food webs, it certainly needs further attention.
This manuscript uses hundreds of concepts and terms on ecology. For example:
line 25: onferring stability to marine food webs
What is stability in marine food webs?
I rephrased the sentence to clarify this concept:
“Microzooplankton seem to act as functional buffer of environmental threats, thus conferring stability, in terms of community connectedness, to marine food webs and ecosystems against external disturbances.” (P1, L26-28).
The term phago-heterotrophic does not exist. The author is confused due to the huge diversity of nutritional modes of the microzooplankton.
The term “phago-heterotrophic” was replaced by “heterotrophic”.
line 149: Parasitic forms are not included in the present assessment.
It is unfortunate to exclude the parasites, but certainly, this requires other review.
I agree, parasitic forms involves an enormous genetic and functional diversity and would require a separate assessment.
Please check for a few misspellings:
line 19: specie’s range
Done.
In conclusion, this reviewer and many of the readers will disagree with the conclusions of this review. However, the microzooplancton and climate have received less attention than other groups, and this compilation of information is useful. More than to recommend the publication of this manuscript, I will not oppose to the publication, as a way to open the discussion in this difficult topic. Please remove the section of coastal eutrophication because it is not directly linked to the climate, increasing excessively the extension of the manuscript.
I wish to acknowledge the comments made by the reviewer that helped me question and/or reconfirm some of my established concepts. The overall writing process of this manuscript was truly enriching.
