the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
| 20 Mar 2024
Reviews and syntheses: Biological Indicators of Oxygen Stress in Water Breathing Animals
Abstract. Anthropogenic warming and nutrient over-enrichment of our oceans have resulted in significant, and often catastrophic, reductions in dissolved oxygen (deoxygenation). Stress on water-breathing animals from this deoxygenation has been shown to occur at all levels of biological organization: cellular; organ; individual; species; population; community; and ecosystem. Most climate forecasts predict increases in ocean deoxygenation, thus it is essential to develop reliable biological indicators of oxygen stress that can be used by regional and global oxygen monitoring efforts to detect and assess the impacts of deoxygenation on ocean life. This review focuses on indicators of low-oxygen stress that are manifest at different levels of biological organization and at a variety of spatial and temporal scales. We compare particular attributes of these indicators to the dissolved oxygen threshold of response, time-scales of response, sensitive life stages and taxa, and the ability to scale the response to oxygen stress across levels of organization. Where there is available evidence, we discuss the interactions of other biological and abiotic stressors on the biological indicators of oxygen stress. We address the utility, confounding effects, and implementation of the biological indicators of oxygen stress for both research and societal applications. Our hope is that further refinement and dissemination of these oxygen stress indicators will provide more direct support for environmental managers, fisheries and mariculture scientists, conservation professionals, and policy makers to confront the challenges of ocean deoxygenation. An improved understanding of the sensitivity of different ocean species, communities and ecosystems to low oxygen stress will empower efforts to design monitoring programs, assess ecosystem health, develop management guidelines, track conditions, and detect low-oxygen events.
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RC1: 'Comment on egusphere-2024-616', Anonymous Referee #1, 09 May 2024
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Roman & Levin et al. provide a thorough and authoritative review of indicators of seawater deoxygenation, which I found very useful and interesting. I think it represents a great deal of work and knowledge that readers of many disciplines will be grateful for. All of my comments are minor but the authors may find them useful, especially to improve clarity in several places.
It depends on other nominations but this synthesis manuscript is certainly of wide appeal to the broad geoscience community and discusses how the importance of seawater deoxygenation remains underappreciated in the scientific, political, and management communities, and the general public.My comments are generally preceded by the line number in the original pdf.
67. Delete 'have'. sounds like the evolution was recent
70. comma after 'temperatures'
93. Maybe a note to caution here that, in general, all indicators can give the wrong impression if they are not thoroughly studied or poorly decided e.g. if the same behaviour may be correlated with other impacts
137-142. It may be best here to supplement this important section (especially "there were also clear interactions among stressors in their biotic effects") with a meta-analysis that considered interactions with deoxygenation e.g. Reddin et al. 2020, which is also not as restrictive in deoxygenation threshold i.e. 'hypoxic event' as in Sampaio et al. 2021; Vaquer-Sunyer & Duarte 2011 though note that this paper does not use a conventional meta-analysis approach, which limits the robustness of its conclusions
Reddin, C. J., Nätscher, P. S., Kocsis, Á. T., Pörtner, H. O., & Kiessling, W. (2020). Marine clade sensitivities to climate change conform across timescales. Nature Climate Change, 10(3), 249-253.
Vaquer-Sunyer, R. & Duarte, C. M. Temperature effects on oxygen thresholds for hypoxia in marine benthic organisms. Glob. Change Biol. 17, 1788–1797 (2011).
Figure1. The benthos seems a bit empty (perhaps it has already suffered from hypoxia) of indicators. e.g. as mentioned later the microbial mat, lack of bioturbation, benthic organisms ‘snorkelling’ the better oxygenated water column. Some of the higher up indicators could show their benthic component. Not clear what the different shades of blue are – simply depth? Purely artistic?
165. Can give a little more information on what constitutes a responsive and less responsive species? Not quite a definition perhaps, but more information would be nice.
Section ‘sensory systems’. The section lacks a summary that the previous section had. A general theme here seems to be that the use of sensory system changes as a deoxygenation indicator is promising but needs much further research before any general application is possible?
221. “levels of growth hormone-insulin-like growth factor”. I am not familiar with this topic but this description is particularly difficult to understand
223. Is this sentence needed? Seems obvious. “Cortisol levels increase when oxygen levels are low enough to cause a physiological stress response”
245. “understood,” rather than “understand”
In general, it would improve clarity to use more commas, where appropriate, to show the main sentence from the components that add information but are grammatically unnecessary e.g. the “where appropriate” above. Alternatively, long sentences could be broken into two or more smaller sentences. There are many instances early on in the MS (it seems not so bad later on) but here is one example (L271-4) of both the above points:
e.g. “The laboratory data were then used to develop a model of the endocrine functioning of vitellogenesis of individual fish (Murphy et al., 2009) to examine how the indicators measured as blood and organ concentrations would vary over time and under exposures not replicated in the laboratory.”
To
“The laboratory data were then used to develop a model of the endocrine functioning of vitellogenesis of individual fish (Murphy et al., 2009). This allowed examination of how the indicators, measured as blood and organ concentrations, would vary over time and under exposures not replicated in the laboratory.”
345. “estimate” rather than “ascertain”
388. Also consider that spawning adults may have greater sensitivities than other stages (though whether this results in mortality or lower ultimate fertility may determine which section this is more appropriate for)
413. Three as written form, rather than ‘3’
446-448. This sentence is unclear: “The resting metabolic oxygen demand of the 447 metabolic indices (Deutsch et al., 2020; Penn et al., 2018) occurs at the onset of mortality 448 or anaerobic metabolism (Deutsch et al., 2015).” The demand occurs at the onset of mortality? This doesn’t make sense to me.
466. DIC should be familiar but doesn’t harm to define.
483-5. Commas are a bit messed up in this sentence.
498. “types of soft-bodied fishes, cnidarians (jellies) and ctenophores”. Maybe give an example of these fishes. Also perhaps be more specific with ‘cnidarians’, since that includes corals, which I don’t think would be a good fit here. ‘Jellies’ is rather informal – can a better/more taxonomic term be found?
504-508. Maybe note that care need taking to account for changing sedimentation or even erosion rates.
536. It would be good to mention that the use of a single indicator taxon may incur error as species niches are not unidimensional, while the use of multiple indicators at once (and multiple threads of evidence in general) should be more robust.
562-7. Please split this long sentence.
718. Perhaps add Simpson’s 1-D. I am not familiar with the ‘ESx’ acronym the authors have here. In my mind, rarefaction is a sampling standardization approach, not a diversity metric in itself, but any of these listed metrics could be based on rarified data. E.g. rarefaction curves are usually of species richness values. Also, species dominance and evenness are two sides of the same coin, rather than separate (usually Simpson’s D or 1-D)
753. Perhaps change “shifts to a dominant that is a hypoxia-tolerant species” to “shifts to dominance by a hypoxia-tolerant species”
759. Salinity may be another important factor in coastal waters
765. These references for ‘fossil forming biota’ all seem to be about foraminifera. Would be nice to have some macrofauna references e.g. Aberhan, M., & Baumiller, T. K. (2003). Selective extinction among Early Jurassic bivalves: a consequence of anoxia. Geology, 31(12), 1077-1080.
766. I would not say alpha diversity is scaled up to beta diversity as one only needs two sites to obtain a beta diversity estimate (i.e. change between two sites). Correct that gamma diversity is the next scale up from alpha diversity.
839. Can be more specific? “than that required to see changes in diversity”. But several diversity metrics use abundance data, so these changes would be visible in those metrics, wouldn’t they? Depends how diversity is defined e.g. if it was species richness, I would agree with the authors.
959. There is a stray colon and then semi-colons later in the sentence in a way that looks intended but is not the usual way these are used. Please write as a normal sentenceDiscussion.
The different aspects of scale that the authors are delineating here are not completely clear to me. Please try to distill a clear summary of each aspect. The first aspect of scaling here appears to be sampling, i.e. relating the scale aspects of the sample to the wider population that the samples are attempting to capture. Second aspect seems to be level in the biological and ecological hierarchy, which are linked mechanistically and thus scales can be crossed not by statistics but via this mechanistic understanding. The third aspect I am unclear about how it differs. It seems an integration of statistical and mechanistic modelling (aspects 1 and 2)?
1071. Please break this sentence down e.g. split it. It is unclear. “Modeling involves significant effort beyond the conceptual modeling that is thus done in 1072 scaling of indicators when quantitative links from the indicator to the system state are 1073 needed.” Especially “that is thus done”
1081. “time and space scales”. Temporal and spatial scales
Table 1. This table did not display well on the pdf and I am not sure the displayed version is the complete version e.g the edges look like they were cut off. The text in many cells is cut off and the font is difficult to read. Better spread table over two pages than miss information. Acronyms and abbreviations need spelling out in a footnote or somewhere. Column ‘Useful/relevant settings’: aren’t all these indicators to be used in the field? Makes this column dubious in its use. ‘Expertise required’: why has ‘basic’ got a question mark? One cell in this column also has a red earmark.
1117. What does “non-sublethal” mean?Citation: https://doi.org/10.5194/egusphere-2024-616-RC1
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