This is an interesting paper that extends some of the results presented in Frederick et al. (2024) regarding adaption of the metabolic rate of copepods to low oxygen conditions in an eastern boundary upwelling system (EBUS).  While the title and abstract imply that this manuscript will be a general review of hypoxia stress on EBUS zooplankton, their focus is on modification of respiration (Pcrit) and reactive oxygen stress (ROS). There are other zooplankton individual, population and community responses such as reductions in fecundity, growth rate, species size, changes in the species composition, etc. which are not addressed in this Review and Synthesis. The authors might want to acknowledge this narrower focus (perhaps change the Title) and provide references to other reviews of hypoxia effects on zooplankton.

Line 84: The authors cite Chisholm and Rolf (1990) as the reference for oxygen-regulators/conformers as related to Pcrit. This citation was not in the references and I do not think it is the proper reference for this topic.

The focus of the paper is on zooplankton of the EBUS, most of which are copepods which do not have gills. Many of the references (lines 95-98) provided on oxygen regulation are for fish and invertebrates which have gills which may have different regulatory oxygen capacity than copepods which obtain oxygen by diffusion through their body surface.

The Legend for Figure 3 is not correct. The Y axis is Metabolic Rate (presumably oxygen consumption/zooplankton and the X axis is Oxygen Partial Pressure (presumably in kPA). Pcrit is the oxygen partial pressure at which the slope of the line changes.

Line 127-128. It should be noted that the study referenced for Acartia tonsa was conducted in Chesapeake Bay, a shallow estuary in the U.S. not an OMZ.

Line 145. Perhaps a reference should be listed to support this sentence.

Comments to the authors of ‘Reviews and synthesis: increasing hypoxia in eastern boundary upwelling systems: a major stressor for zooplankton’ (Frederick et al)

General comments

This project aims to provide a synthesis of zooplankton responses to changes in hypoxia in Eastern Boundary Upwelling Systems (EBUS). To this end, the authors motivate their review by discussing changes in the biogeochemistry of the EBUS due to climate change, with a particular focus on upwelling and the vertical expansion of hypoxic layers and the Oxygen Minimum Zone (OMZ). The authors then introduce two different adaptive modes by which organisms change their metabolic activity to decreasing oxygen concentration and show possible adaptive responses, as well as the non-adaptive response. This is then followed by an extended section on the oxidative stress in zooplankton, where the authors explore the consequences of hypoxia and the production of reactive oxygen species for both migratory and non-migratory zooplankton.

This review is very timely as ocean deoxygenation is increasing globally. However, in my opinion, the review could go more into detail with respect to the mechanisms presented, and provide more details on the individual- and population-level consequences of an increase in the exposure of zooplankton to low oxygen levels.

Furthermore, the link between the adaptive responses and the oxidative stress was for me not entirely clear. In other words, It was unclear to me if the responses to oxidative stress change depending on the adaptive responses shown in Figure 3, and whether one response would be favored over another under increasing deoxygenation.

Finally, I felt that some of the physical and behavioral processes presented in the review are oversimplified or do not match other findings/definitions. Here I am referring to the oversimplification of increased wind-driven upwelling across the EBUS and the depth of diel vertical migration (DVM). I think the authors oversimplify the processes by which upwelling has changed across the EBUS, where for instance the review by Bograd et al. (2023) does a great job at detailing the differences in upwelling intensity across different EBUS. With respect to the DVM, the authors use a euphotic zone of 50 m rather than the usual 200 m, and the vertical extent of DVM shown seems extremely shallow, which does not match the description in the text.

Specific comments

L.15: As mentioned above, I think the authors should address the uncertainty in upwelling trends depending on the data set, region, and proxy variable used, since this seems to be the one of the key process in the paper by which organisms can be exposed to low oxygen concentration. For instance, regional observations have shown a weakening or no significant trend in upwelling intensity for the Canary Upwelling System (Bode et al. 2019). Or Pardo et al. (2011) that found a small weakening trend in the Humboldt System and no trend in the California Current System using trends in sea surface temperature.

L.29-31: This sentence contains a strange redundancy stating that a warmer ocean drives increases in mean global sea surface temperature. In addition, I would argue that the warming drives the physico-chemical changes rather than just a warmer ocean. Please revise the sentence.

L.34: Here, I suggest the authors be more quantitative and say by how much the oxygen concentration has changed since the middle of the 20th century. With such a measure, the authors can compare the long-term changes with seasonal and spatial changes in oxygen concentration.

L.40-43: Given that short-term changes in oxygen are of interest for this review, I suggest to also include the role of extreme events, which can lead to transient habitat reductions of variable duration in EBUS such as the California Current System and the Humboldt System (Köhn et al., 2022).

L.47-48: As spatial heterogeneity in oxygen conditions is one of the key factors determining the exposure of zooplankton to low oxygen, I urge the authors to explore how the spatial changes in upwelling due to the poleward displacement of coastal upwelling winds (Rykaczewski et al. 2015) has or will likely change the overall oxygen conditions in the poleward vs the equatorward boundaries of EBUS. 

L.54-55: Here the authors should provide some examples of the various ecological and biogeochemical consequences, preferably with a quantitative metric, as this would add more meaning to their statement and improve their review for future readers.

L.56: The authors introduce the terms normoxia and mild or severe hypoxia. I understand that these levels are species-specific, however, it would help to  have a range or a mean of a selected number of species. I would also imagine that using the levels for copepods would suffice given their abundance and importance.

L.79-85: The authors explain very clearly two adaptive modes and illustrate the differences between them. To increase the impact of the review, they should also mention characteristic timescales at which such changes can occur in zooplankton and provide examples of possible organisms that follow each adaptive mode if possible.

Furthermore, given the evidence from Cobbs and Alexander (2018) on the existence of other response types to progressive hypoxia among marine animals; including zooplankton; the authors could expand their review to include more response types.

L.99-103: The authors explain very briefly how maternal effects can play a role in shaping the plasticity of stress responses in organisms, putting a focus on the effects of life-history on individual-level responses and possible consequences for the population. However, the authors then remain relatively vague in explaining how this mechanism works and do not explain possible feedbacks and consequences on the population.

L.125-129: The authors name some changes in behavior and distribution as a result of exposure to hypoxia. While I agree with the examples in the text, it would help to give other examples of strategies observed in the field (e.g. Hauss et al., 2016).

L.132-133: Here again, it would be important to have a sense of the spatio-temporal scales to fully grasp how the exposure to low oxygen conditions changes along the life-history of individual organisms.

L.143-145: Here, it would be important to get some comparison of the effect of oxidative stress on the different physiological costs, or rather how was the significance measured?

L.153-154: The authors explain how ROS production occurs both during hypoxic conditions and after re-oxygenation. Thus my question was what are the implications of this, or can you say something about the difference in ROS production under the different conditions and by how much it changes?

L.179: Can you say something about the consequences of a limited DVM and compare it to other strategies observed in the field (see Hauss et al., 2016)?

L.203-204: The authors explain how hypoxic conditions may reach the surface due to strong upwelling. Here, it would be important to compare the exposure of such surface conditions to what migratory zooplankton experience during DVM. Maybe you could provide some characteristic intensities or durations of exposure?

Technical corrections

L.37: What do you mean by “becomes even more critical”? Do you mean deoxygenation is enhanced or that it is more critical for marine life?

L.54: It should be become rather than becomes. In addition, what is meant by “plankton become more concentrated”? Do you mean they are more abundant? There is also a similar phrasing in the caption of Figure 1.

L.74: It should be “At the ecosystem level…”. This sentence is also rather convoluted. Can you rephrase it for clarity as it has many clauses.

L.84: The reference Chisholm and Roff, 1990 is not in the bibliography.

L.85: Please introduce the abbreviations used on the first mention. Here you can introduce the abbreviation for metabolic rate (MR).

L.89-91: Please split up this sentence to increase readability.

Figure 2: The term routine metabolism was not introduced in the main text. In addition, the axis descriptors do not match the text descriptors, making the interpretation of the figure more difficult. The caption should include more information of what is shown in the figure. Finally, unless I missed something, I was not able to find a similar figure in Rogers et al., 2016 from which figure 2 was adapted.

L.97: The authors introduce the term “maximum oxygen supply capacity” without definition. As this is a review, I feel that important terms like this should be defined.

L.137: Here, a lot of abbreviations are used without introducing them first.

Table 1: Some abbreviations are not introduced (e.g., GR in Pteropoda). Also, what is the difference between having different biomarkers linked by a slash and a dash? In the caption, to the best of my knowledge it should be “Lactato deshidrogenase” and “Peroxidase”.

L.173-174: Can you say  in which organisms POS has been proposed as a mechanism to strengthen antioxidant defences?

L.175: To the best of my knowledge, it should be migratory and non-migratory.

L.185: The abbreviation POS seems strange because “doing POS” would mean “doing preparation for oxidative stress” rather than preparing for oxidative stress.

L.186: Should read “The interplay between ROS production and POS…”. Please revise throughout the manuscript when using abbreviations (e.g. L 190).

L.189: Should read “reduction/increase”

Figure 4: The depth axis does not match the reference “Riquelme-Bugueño et al. (2020)” or the main text. The abbreviations used in the figure are not explained. It might be better to show the direction of change with arrows rather than with multiple “+” signs, as this would resemble the symbols used in Table 1. Also, what is the meaning of the dotted line.

L.209: What is meant by “during high frequency change”?

Figure 5: As the main text refers to seasonal changes, I was expecting to see a timeseries (resembling Figure 4). Also, the abbreviations are not properly explained in the caption.

L.227: Rather than saying it seems more difficult, you can simply say that it is more difficult.

L.232: DO has not been introduced.

L.232: Remove “front”.

L.234: Rephrase to “experiments carried out at temperatures ranging between 9°C and 16°C.” 

Section 3.1: I was initially confused as this section begins with explaining the high antioxidant potential of diatoms in a zooplankton paper. It wasn’t until the last paragraph in this section that I realized how this fits in the story line. Thus I would suggest changing the sequence in which the information is presented to increase readability.

Bibliography

Bode A, Álvarez M, Ruíz-Villarreal M, Varela MM. 2019. Changes in phytoplankton  production and upwelling intensity off A Coruña (NW Spain) for the last 28 years. Ocean Dyn. 69:861–73

Bograd SJ, Jacox MG, Hazen EL, Lovecchio E, Montes I, Pozo Buil M, Shannon LJ, Sydeman WJ, Rykaczewski RR. Climate Change Impacts on Eastern Boundary Upwelling Systems. Ann Rev Mar Sci. 2023 Jan 16;15:303-328. doi: 10.1146/annurev-marine-032122-021945. Epub 2022 Jul 18. PMID: 35850490.

Cobbs GA, Alexander JE Jr (2018) Assessment of oxygen consumption in response to progressive hypoxia. PLoS ONE 13(12): e0208836. https://doi.org/10.1371/journal.pone.0208836

Hauss, H., Christiansen, S., Schütte, F., Kiko, R., Edvam Lima, M., Rodrigues, E., Karstensen, J., Löscher, C. R., Körtzinger, A., and Fiedler, B.: Dead zone or oasis in the open ocean? Zooplankton distribution and migration in low-oxygen modewater eddies, Biogeosciences, 13, 1977–1989, https://doi.org/10.5194/bg-13-1977-2016, 2016.

Köhn, E. E., Münnich, M., Vogt, M., Desmet, F., & Gruber, N. (2022). Strong habitat compression by extreme shoaling events of hypoxic waters in the Eastern Pacific. Journal of Geophysical Research: Oceans, 127, e2022JC018429. https://doi.org/10.1029/2022JC018429

Pardo P, Padín X, Gilcoto M, Farina-Busto L, Pérez F. 2011. Evolution of upwelling systems coupled to the long term variability in sea surface temperature and Ekman transport. Clim. Res. 48:231–46

Rykaczewski, R. R., J. P. Dunne, W. J. Sydeman, M. García-Reyes, B. A. Black, and S. J. Bograd (2015), Poleward displacement of coastal upwelling-favorable winds in the ocean's eastern boundary currents through the 21st century, Geophys. Res. Lett., 42, 6424–6431, doi:10.1002/2015GL064694.