the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Intra-skeletal variability in phosphate oxygen isotope composition reveals regional heterothermies in marine vertebrates
Romain Amiot
Guillaume Suan
Christophe Lécuyer
François Fourel
Fabien Demaret
Arnauld Vinçon-Laugier
Sylvain Charbonnier
Peggy Vincent
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- Final revised paper (published on 30 May 2022)
- Supplement to the final revised paper
- Preprint (discussion started on 19 Jan 2022)
- Supplement to the preprint
Interactive discussion
Status: closed
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RC1: 'Comment on bg-2022-10', Anonymous Referee #1, 10 Feb 2022
General Comments
This paper is welcome because it addresses a technique that has been used to estimate body temperatures of extinct animals from measurements of oxygen isotope in fossil bone and teeth. It recognises that temperature is not uniform throughout the body of aquatic vertebrates (and also terrestrial ones) and shows that isotope analysis of regional bones result in temperatures that are reasonably expected to occur in them. Two groups of extant aquatic species are chosen to represent marine mammals that show regional hypothermy in the limbs and endothermic fish that show regional endothermy by adaptively warming the red muscle, eyes and visceral organs. The results support the use of the method and are strikingly illustrated. The isotope analysis is done according to methods established in the authors’ world-class laboratory. The sample sizes are adequate, carefully analysed statistically and interpreted thoughtfully. The writing is generally clear, well organised and extremely well referenced with relevant citations. There are only a few unusual expressions and typographical mistakes that may be rectified by proofreading by a native English writer.
The major problems of the paper involve (1) terminology and (2) use of references. There are suggestions below about terms that may better describe regional patterns of temperature throughout the body. Unfortunately, there appear to be several references that are not used appropriately. Classical references are fine for original ground-breaking research, but more recent papers are best for citing, because presumably they contain the foundational papers as well as recent developments. Some examples are given below.
Specific comments (referenced to line numbers)
30-37 Some of the citations here and in the rest of the introduction are not very useful or even appropriate. For example, in referencing ectotherms, Rodbard (1953) is a short popular article on ‘warm-bloodedness’, nearly 70 years old and poorly referenced. The Hight and Lowe (2007) one is more recent, but as it apparently speculates on whether elevated Tb in leopard sharks aggregating in shallow embayments is behavioural thermoregulation. Crawshaw and Hammel (1971) is about Antarctic fish. Norbert Smith’s (1979) review of Tb in crocodilians has been long ago superseded (by, for example, G. Grigg and D. Kirshner 2015: Biology and Evolution of Crocodylians). Sherwin (2010) is a manual for animal husbandry and Allali et al. (2013) apparently concerns circadian clocks in camels, both not the best references for thermal physiology. The introduction would be better if no references were given for generally accepted facts than old specific references that provide little support for the points that the authors are making. Alternatively, more recent reviews on ectothermy and endothermy could be used, for example the Oxford Scholarship ‘Ecological and Environmental Physiology Series’. The authors should carefully review the appropriateness and utility of all references in the paper, not only those in the introduction.
60-63 (also lines 234-235) Here it is essential to provide a citation or two for actual data for regional heterothermy in extant animals.
71-74 The groups of animals in the study are classified as either ‘homeothermic endotherms’ or ‘poikilothermic endotherms’. Many would consider the first case misleading, because marine mammals are not wholly homeothermic, but regionally hypothermic, as the authors demonstrate. Also the second case of warm organs in fish seems like a contradiction in terms. ‘Poikilotherm’ meaning variable temperature is rarely used lately, and for good reason. For example, normal ectothermic fish living in the deep sea cannot be called poikilotherms because their body temperatures are constant. What is important here is that the mammals studied here have cool limbs and the fish have some warm organs. Therefore I would recommend redefining the groups in your study as two types of ‘regional heterotherms‘. ‘Regional’ is important to distinguish it from ‘temporal heterotherms’ which are endotherms that enter hibernation or torpor. In this study, the mammals allow the appendages to cool and the fish warm certain organs. This is simply defined and does not need special titles. You might label sections 4.2.1 ‘Marine mammals’ and 4.2.2 ‘Endothermic fish’. In any case, avoid the term ‘poikilotherm’ and its variants.
144-9 Please explain in greater detail the possible reasons for the differences in predicted temperatures in teeth of fishes and mammals. One would expect that tuna teeth would form under cold conditions, because tuna respire by ram-ventilation in which the seawater constantly flows in and around their teeth. In contrast, marine mammals have closed mouths. Yet the temperatures derived from isotopes are the opposite to expectations. Also, please give a little more detail about remodelling of fish bone. I was not aware that this occurs (=do not know the citations), so please point out how it differs from the amniote paradigm involving secondary osteons.
225-231 This final section seems to undermine the whole approach by suggesting the basis for the technique is not up to date. Please clarify this section by evaluating how much the equations differ and what is the magnitude of the difference. Would the study be compromised in its conclusion?
Technical corrections
35 Delete ‘and thermolysis’. This word means breaking down tissue or cells with heat. It is not appropriate.
38 Instead of ‘non-normothermic conditions is extremely…’, I suggest ‘at ambient temperatures below the thermal-neutral zone can be…’.
44 Instead of ‘thermometer reading’ use ‘thermometry’.
52 I think that both food and water would be taken in by both groups.
74 See notes above about the use of ‘poikilothermic’.
141 Instead of ‘results’ use ‘result’.
154 Use ‘prey’, which is the pleural.
156 Can you provide some numbers for the bone variability to compare with 0.4 for water?
155 Use ‘appendicular skeleton’, not ‘these skeletal regions’.
171 Use ‘little’, not ‘few’.
177 This equation refers to temperature, but the preceding sentence refers to temperature differences. It is confusing.
188 Carey et al. (1984) indicate that heat in tunas is also produced in the viscera.
201 Use ‘have’ not ‘has’.
210 and 215 Here and earlier reference is made to thermal imaging. I would remove this, because it is irrelevant in these cases.
449 Note subscript and superscript errors.
453 It is hard to see the stars. The red around the eyes is misleading, especially since the eye is warm, but apparently not measured in this study. If the ring could be white, it would not be confused with the red on the temperature scale.
461 Use ‘equal’, not ‘equals’.
465 In the footnote to the table, use ‘taken’ not ‘taking’.
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AC1: 'Reply on RC1', Nicolas Séon, 30 Apr 2022
The comment was uploaded in the form of a supplement: https://bg.copernicus.org/preprints/bg-2022-10/bg-2022-10-AC1-supplement.pdf
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AC1: 'Reply on RC1', Nicolas Séon, 30 Apr 2022
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RC2: 'Comment on bg-2022-10', Anonymous Referee #2, 05 Apr 2022
The manuscript „Intra-skeletal variability in phosphate oxygen isotope composition reveals regional heterothermies in marine vertebrates“ by Séon et al. is an interesting new contribution demonstrating that substantial differences in d18Op values of different skeletal parts exist whithin ectotherm and endotherm marine vertebrates, which has implications both for temperature and/or salinity reconstructions based on bioapatite phosphate oxygen isotope analysis.
The manuscript thus provides notes of caution for such palaeoceanographic seawater temperature and salinity reconstructions which may have a larger error range than previously thought. To support this claim the manuscript presents a convincing and substantial d18Op dataset on modern cetaceans and osteichthyians, it is concise and well written therefore I have only several minor suggestions/corrections to propose.
I miss some information on the salinity and water temperature differences in the method section for the regions from which the marine vertebrates where captured.
In the results section you must provide ranges for d18Op values for intra- and inter-bone variability and state that the variability is higher for poikilothermic versus homeothermic endotherms.
I think it could be useful to provide a graph and/or text to quantify the influence (error range) of intra-skeletal d18Op variability on water temperature and d18Owater reconstructions. A comparison of measured body temperature differences versus calculated body temperature differences from d18Op values and estimated versus measured d18Osw (when available) might be instructive.
Minor comments
Line 21, 238, 459: hydroxylapatite is the correct terminology according to the IMA (International Mineralogical Association)
Line 31: I assume there is also more recent pertinent literature to cite here than only Rodbard 1955. Same for line 35 Scholander 1955
Line 36: do you mean core body temperature (instead of deep) here?
Line 52: inhaled air oxygen also contributes to the body water pool of lung breathing marine mammals
Line 56: may be add at the end: in isotope equilibrium
Line 58: organisms is to unspecific. Use vertebrates
Line 60: paleontological (as you use American English)
Line 60: in Vennemann et al. 2001 also intra jaw tooth enameloid d18Op variability of modern sharks is presented
Line 66-68: Would it not be informative to provide a plot at least in the supplements to compare measured and calculated body temperatures (based on d18Op)?
Line 71: four extant fully marine species
Line 73: not four authors but Robineau et al. Furthermore, this reference is missing in the reference list
Line 76: All three dolphin specimens
Line 79: some more provenance information should be provided. Are those specimens form the fish shop from the Mediterranean Sea? Which area?
Line 80: may be you could refer here to one of the figures demonstrating which skeletal parts were sampled
Line 94, 95, 97: the current terminology for these international standard reference materials is NIST SRM plus the according number
Line 97: why did you choose a non-matrix matched reference material (BaSO4) and not another isotopically distinct silverphosphate? This is not ideal because of different cumbustion properties of different mineral phases.
Line 100: you should state the analytical error of d18Op analysis for samples too or at least mention that it is the same as for NIST SRM 120c.
Line 104: intra-skeletal
Line 117, 118: Fig. 1A; Fig. 2A (space missing before nr.)
Line 119: you mean variability instead of homogeneity here?
Line 119: why not providing the Fig. S1 in the main text?
Line 120: please provide values for d18Op ranges here
Line 123: any ideas why the teeth have higher d18Op values? Are the snout regions where they mineralize cooler? The 1.5 permil difference seem to suggest a 6 °C body temperature difference in dolphins. Is this to be expected and in line with instrumental body temperature measurements?
Line 141: result (singular not plural)
Lines 141-142: what do you mean with oxygen sources of the body: body water, inhaled oxygen? Can migration to different seawater masses with different d18Osw values play a role here too? What about any mother milk consumption effects? For early ontogenetically forming teeth this could play also a role. Furthermore, could also tissue specific differences in oxygen isotope fractionation (i.e. between dentin and enamel) play any role? Enamel of dolphin teeth is very thin. Thus may be you sampled a mixture between some dentin and enamel.
Line 144, 145, 151, 164: space after Fig. missing
Line 149: are not also the teeth of other osteichthyans (not only the tuna) replaced continously? Can you add a reference for this?
Line 151: Besides, all studied vertebrates…
Line 151: are different rates of air oxygen inhalation (marine mammals versus fish) not a significant factor for different d18Op values?
Line 154: you must quote a reference for the statement that food is the main water source for dolphins.
Line 155: marine vertebrates (instead of organisms)
Line 159: is there an estimate possible of how much of the inter-bone variance in d18Op is possible to attribute to temperature differences (based on modelled d18Op from measured temperatures versus measured d18Op)?
Line 164: Intra-skeletal
Line 167 and elsewhere in the text: should there not be a space between value and °C ? According to SI unit use guidelines.
Line 167: Is the +/- 2 °C for cetaceans (i.e. dolphins) in line with a +/- 0.5 permil 1 SD variance in measured d18Op? Then worth mentioning this here?
Line 173-174: no additional, newer references for dolphin body temperature available? What is the constant trunc body temperature, can you provide a value and 1 SD?
Line 174: Assuming only slight changes…
Line 180-181: could you back this statement up with values how large the differences between reconstructed and measured temperatures are?
Line 183: … represent a long-term average value…
Line 197-200: Is it not possible to compare the temperature variance of measured and calculated temperatures (from d18Op)? Why is the range of core body temperature and ambient water so large (4 to 20 °C)? Because some tuna were caught in cold water settings? I think it would be useful to point this here out as the differnces given here based on measured d18Op values are at the lower end of the huge range up to 20 °C quoted.
Line 205: Eq. (1), you can refer to Fig. 3A here for the body temperatures.
Line 206: what do you mean with global trend? Reword for clarification?
Line 212: …loggers are difficult…
Line 217: Well, you need to kill the animal to get bones or teeth for analysis, hence the method is leathal or at least invasive (except for collection of shed teeth or museum specimens). This should be acknowledged. You can add may be… that are difficult to monitor otherwise. Again replace the too unspecific organisms by marine vertebrates for which only skeletal remains are available…
Line 218: … and marine reptiles such as.. you may additionally mention megatooth sharks.
Line 225: Similarly or Along the same lines, seem more appropriat than the phrasing in the same idea.
Line 227: can you please provide the equation you quote here so that the reader is not forced to access the Ciner et al. (2016) reference.
Line 231: would it not be helpful to use the current published equations and illustrate the effects of intra-body d18Op variability on differences in reconstructed d18Osw and body temperature, in supplemenatary figure(s) for instance?
Line 239: … chemical alteration processes that take place during postmortem taphonomy and fossilization.
Note that this especially applies for enamel, less so for dentin and bone, which are more liable for alteration (e.g., Ayliffe et al., 1994). Furthermore, it is typically not common practice to quote studies in the conclusion section. I do not know how the Biogeosciences policy is concerning this. If considered ok you can leave as is.
Line 241, 441, 449: correct formatting of d18Op (super-, respectively, subscript)
Figures
Fig. 1B: may be you can provide a typical analytical error bar here?
Fig. 2 may be use same font size as in Fig. 1. May be use same scale for delta d18Op in A and B? The star symbols in B are rather small and difficult to see may be enlarge and fill the stars white to enhance visibility? May be add a note that absolute d18Op differences between the two fish is due to capture in different seawater bodies and mention those.
Fig. 3: use same symbol size in A and B. Are mean values and 1SD potted in the figures? Please specify.
Line 461: equal (without s)
Fig. 3B: may be plot real d18Osw ranges as shaded bars for comparison if there are such values available from the literature or NOA or other seawater d18O database for the regions of vertebrate capture?
Is there any reference to support the assumption that osteichthyians have d18Obw = d18Osw that could be cited here?
Are tooth values dentin and enamel mixtures or pur enamel? Not clear. As dolphin enamel is very thing may be the former?
Line 463: fractiontion equation for cetaceans by Ciner et al…. Mediterranean Sea
Table 1
Replace global by all skeletal remains
References
There are still several formatting errors in the reference list that you need to correct.
For instance, comma missing in author, and autor references
Line 284: O´Neil
Line 295: I-Fan; is this correct?
Line 318: Antarctic (capital A)
Line 336: subscript 2 in SO2
Line 351: journal, volume page number missing
Line 353: journal name not abbreviated
Line 356: Arctic (capital A)
Line 361, 362: words in article title not with capital letters
Line 367: degree sign for temperature missing
Line 381: incomplete reference: missing journal, volume, page numbers
Line 397: page numbers missing
Line 426: Science (capital S)
Line 429: book title words longer than three letters starting with capital letters
You did not cite the Barrick et al. 1992 whale d18Op paper that also contains cetacean d18Op data of modern whales, why not?
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AC2: 'Reply on RC2', Nicolas Séon, 30 Apr 2022
The comment was uploaded in the form of a supplement: https://bg.copernicus.org/preprints/bg-2022-10/bg-2022-10-AC2-supplement.pdf
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AC2: 'Reply on RC2', Nicolas Séon, 30 Apr 2022
Peer review completion



