Increase in metazoan ecosystem engineering prior to the Ediacaran–Cambrian boundary in the Nama Group, Namibia

The disappearance of the soft-bodied Ediacara biota at the Ediacaran–Cambrian boundary potentially represents the earliest mass extinction of complex life, although the precise driver(s) of this extinction remain unresolved. The ‘biotic replacement’ model proposes that an evolutionary radiation of metazoan ecosystem engineers in the latest Ediacaran profoundly altered marine palaeoenvironments, resulting in the extinction of Ediacara biota and setting the stage for the subsequent Cambrian Explosion. However, metazoan ecosystem engineering across the Ediacaran–Cambrian transition has yet to be quantified. Here, we test this key tenet of the biotic replacement model by characterizing the intensity of metazoan bioturbation and ecosystem engineering in trace fossil assemblages throughout the latest Ediacaran Nama Group in southern Namibia. The results illustrate a dramatic increase in both bioturbation and ecosystem engineering intensity in the latest Ediacaran, prior to the Cambrian boundary. Moreover, our analyses demonstrate that the highest-impact ecosystem engineering behaviours were present well before the onset of the Cambrian. These data provide the first support for a fundamental prediction of the biotic replacement model, and evidence for a direct link between the early evolution of ecosystem engineering and the extinction of the Ediacara biota.

Have you any concerns about statistical analyses in this paper? I do not feel qualified to assess the statistics

Recommendation?
Major revision is needed (please make suggestions in comments)

Comments to the Author(s)
Review of RSOS-190548: Increase in metazoan ecosystem engineering prior to the Ediacaran-Cambrian boundary in the Nama Group, Namibia by A. Cribb et al.
The manuscript by Alison T. Cribb and his colleagues discuss a many-sided problem of the Ediacaran-Cambrian transition heated by current achievements in geochemistry and palaeontology of this important interval in the Earth history. At the same time, new data show a mosaic pattern of environmental and biotic processes during this transition in different regions. Although the authors' data and interpretation are reliable in the limits of the Namibian basins, the thoughts that their model is applicable to global events can be disputed (see below). A clear timescale has to be adjusted by the authors to their study including each plot to make the discussion understandable.
GENERAL COMMENTS: Lines 48 and below: The terminal Neoproterozoic Ediacaran Period is dated by 635according to the International Chronostratigraphic Chart issued by International Commission on Stratigraphy in 2018 (www.stratigraphy.org). Thus, the authors' data frame of 635-538.5 Ma contradicts this figure and turns the entire problem under discussion to the shady zone of the age misinterpretations which, unfortunately, is among the key points of the reliability of the entire study: What events we actually discuss if these events occur 541-538.5 Ma--the late Ediacaran or the early Cambrian? Lines 107-112: Moreover, if the Ediacaran-Cambrian boundary is 'placed at the erosive unconformity' between strata dated at 541.61 Ma and 538.5 Ma, how can the authors prove that nothing has happened during 3 my gap embracing the very time of events under discussion? If the biotic replacement model discussed by the authors is verifiable at the Ediacaran-Cambrian successions of Namibia due to the presence of a serious time gap? Lines 299-302: For instance, if 'the trace fossil record of the Nama Group… illustrates Cambrianequivalent levels of metazoan ecosystem engineering in specific horizons and palaeoenvironments in the Ediacaran', the authors' model is 'consistent with the first prediction of the biotic replacement model'. However, if these horizons are already Cambrian the model is inconsistent. Fig. 3. This key figure is absolutely unclear: Here the Nomtsas Member has to be shown as a chronological subdivision above the Spitzkop Member ( Fig. 1 provides

Are the interpretations and conclusions justified by the results? Yes
Is the language acceptable? Yes

Do you have any ethical concerns with this paper? No
Have you any concerns about statistical analyses in this paper? I do not feel qualified to assess the statistics

Recommendation?
Accept with minor revision (please list in comments)

Comments to the Author(s)
The role of bioturbation during the Ediacaran-Cambrian transition, including its significance in ecosystem engineering, is a central issue for our understanding of the history of life. In addition, the thick and continuous terminal Ediacaran deposits of Namibia are instrumental to address this topic. The vast majority of studies dealing with the impact of bioturbation during the Ediacaran-Cambrian transition are simply based on measuring density of trace fossils in both cross-section and bedding-plane views. The authors should be commended for not falling in this trap and approaching this topic employing more sophisticated tools. With a little bit of additional work, this study will be a valuable addition to the literature on the topic.
My only criticism in this regard is the use of the Ecosystem Engineering Impact index of Herringshaw et al. (2017). This index encompasses several metrics, but without actually articulating the different elements in a consistent fashion. For example, Herringshaw et al. (2017) adopted the functional groups of Solan and co-workers without any adjustments. This is problematic because adjustments are needed for applying this scheme to the fossil record when dealing with tiering structure to avoid conceptual overlap. This was discussed by Minter et al. (2016, p. 22), who stated "We omit the categories of epifaunal bioturbators and surficial modifiers (Solan and Wigham 2005) because of their spatial constraints, being covered potentially by any of the other four means of sediment reworking in the epifaunal and semi-infaunal tier". This overlap compromises the evaluation of the intensity of ecosystem engineering represented by each ichnotaxon in the Ecosystem Engineering Impact approach and as a result the values obtained in this way may be rather arbitrary. My suggestion here is that the authors may well dispense of the Ecosystem Engineering Impact approach and just use the scheme put forward by Minter and co-workers, which covers the same ground on a more consistent fashion.
Also, it may be advisable not to include in the analysis those forms which have not been assigned to an ichnotaxon because the behavioural significance of these may be unclear. In any case, looking at the photographs, I would tend to think that those trace fossils illustrated in Fig Fig. 2F may be plug-shaped burrows as indicated by the authors, but also a preservational variant of a treptichnid (cutting the sample may resolve this issue). The one in Fig. 2G is really unconvincing and I am not even sure if it is a trace fossil. The one assigned to Planolites in Fig. 2I is unconvincing, I would place it in Helminthoidichnites. The one assigned to Streptichnus in Fig.  2K (note that the label is gone) is not convincing either, and it is too partially preserved to suggest an alternative name. In short, some adjustments are needed on this front and some of these will translate into changes in the evaluation of ecosystem engineering.
Finally, the author may wish to cite a recent paper that uses a similar approach to assess ecospace utilization in the interval of the Chapel Island Formation attributed to the Treptichnus pedum zone, comparing with the underlying strata in the same area. The reference is:  Figure 1) Line 124: "trace fossils" x "traces" Line 158: Using Carbone and Narbonne (2014) here may be complicated because trace fossils in that study are mostly classified in open nomenclature rather than simply assigned to specific ichnotaxa. Line 177: "Trace fossil assemblages present in slabs (n=16) from the Zaris Subbasin were of comparatively low diversity…." x "Trace fossil slabs (n=16) from the Zaris Subbasin were comparatively low diversity….". Lines 179-180: "In contrast, trace fossil assemblages present in slabs (n=61) from the Witputs Subbasin were of relatively high diversity…." x "In contrast, trace fossil slabs (n=61) from the Witputs Subbasin were relatively high diversity…." Line 276: "cf." x "c.f." Lines 291-293: It would be useful to back up this statement with some references or more precise facies information. The editors assigned to your paper ("Increase in metazoan ecosystem engineering prior to the Ediacaran-Cambrian boundary in the Nama Group, Namibia") have now received comments from reviewers. We would like you to revise your paper in accordance with the referee and Associate Editor suggestions which can be found below (not including confidential reports to the Editor). Please note this decision does not guarantee eventual acceptance.
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Once again, thank you for submitting your manuscript to Royal Society Open Science and I look forward to receiving your revision. If you have any questions at all, please do not hesitate to get in touch. The manuscript by Alison T. Cribb and his colleagues discuss a many-sided problem of the Ediacaran-Cambrian transition heated by current achievements in geochemistry and palaeontology of this important interval in the Earth history. At the same time, new data show a mosaic pattern of environmental and biotic processes during this transition in different regions. Although the authors' data and interpretation are reliable in the limits of the Namibian basins, the thoughts that their model is applicable to global events can be disputed (see below). A clear timescale has to be adjusted by the authors to their study including each plot to make the discussion understandable. My suggestion here is that the authors may well dispense of the Ecosystem Engineering Impact approach and just use the scheme put forward by Minter and co-workers, which covers the same ground on a more consistent fashion.
Also, it may be advisable not to include in the analysis those forms which have not been assigned to an ichnotaxon because the behavioural significance of these may be unclear. In any case, looking at the photographs, I would tend to think that those trace fossils illustrated in Fig. 2A may belong in Helminthoidichnites, the one in Fig. 2B may be referred to as a treptichnid (as the one in Fig. 2E, as indicated by the authors), and the one in Fig. D may be tentatively called Helminthopsis. The one in Fig. 2C is simply too fragmentary to say. The ones in Fig. 2F may be plug-shaped burrows as indicated by the authors, but also a preservational variant of a treptichnid (cutting the sample may resolve this issue). The one in Fig. 2G is really unconvincing and I am not even sure if it is a trace fossil. The one assigned to Planolites in Fig. 2I is unconvincing, I would place it in Helminthoidichnites. The one assigned to Streptichnus in Fig.  2K (note that the label is gone) is not convincing either, and it is too partially preserved to suggest an alternative name. In short, some adjustments are needed on this front and some of these will translate into changes in the evaluation of ecosystem engineering.
Finally, the author may wish to cite a recent paper that uses a similar approach to assess ecospace utilization in the interval of the Chapel Island Formation attributed to the Treptichnus pedum zone, comparing with the underlying strata in the same area. The reference is:  Figure 1) Line 124: "trace fossils" x "traces" Line 158: Using Carbone and Narbonne (2014) here may be complicated because trace fossils in that study are mostly classified in open nomenclature rather than simply assigned to specific ichnotaxa. Line 177: "Trace fossil assemblages present in slabs (n=16) from the Zaris Subbasin were of comparatively low diversity…." x "Trace fossil slabs (n=16) from the Zaris Subbasin were comparatively low diversity….". Lines 179-180: "In contrast, trace fossil assemblages present in slabs (n=61) from the Witputs Subbasin were of relatively high diversity…." x "In contrast, trace fossil slabs (n=61) from the Witputs Subbasin were relatively high diversity…." Line 276: "cf." x "c.f." Lines 291-293: It would be useful to back up this statement with some references or more precise facies information. Dear Ms Cribb, I am pleased to inform you that your manuscript entitled "Increase in metazoan ecosystem engineering prior to the Ediacaran-Cambrian boundary in the Nama Group, Namibia" is now accepted for publication in Royal Society Open Science.
You can expect to receive a proof of your article in the near future. Please contact the editorial office (openscience_proofs@royalsociety.org and openscience@royalsociety.org) to let us know if you are likely to be away from e-mail contact --if you are going to be away, please nominate a coauthor (if available) to manage the proofing process, and ensure they are copied into your email to the journal. Due to rapid publication and an extremely tight schedule, if comments are not received, your paper may experience a delay in publication.
Royal Society Open Science operates under a continuous publication model (http://bit.ly/cpFAQ). Your article will be published straight into the next open issue and this will be the final version of the paper. As such, it can be cited immediately by other researchers. As the issue version of your paper will be the only version to be published I would advise you to check your proofs thoroughly as changes cannot be made once the paper is published. However, we agree that this is a key point that may be lost on some readers, and so we have made a number of adjustments to the text and figures that makes these points clear.
We detail these in our responses to points 2, 5 and 6 below.  There is thus no reason at all to believe that our fossils are Cambrian, and a new date for the Ediacaran-Cambrian boundary will slowly filter its way into the ICS chart once it has been re-established in other key sections worldwide.
We do, however, agree with the reviewer that this point needs to be clear in the manuscript, and thus we have added the following text to the Geological Setting and Methods sections which should make these points clear. 3) "Moreover, if the Ediacaran-Cambrian boundary is 'placed at the erosive unconformity' between strata dated at 541.61 Ma and 538.5 Ma, how can the authors prove that nothing has happened during 3 my gap embracing the very time of events under discussion?"

CHANGES NOT MADE:
We suspect that there may be a fundamental misunderstanding on the part of the reviewer here -the point of our study was to quantify the ecosystem engineering impacts (EEIs) of trace fossils throughout the Ediacaran and Cambrian portions of the Nama Group and to test a key tenet of the 'biotic replacement' hypothesis. Our data illustrate that the EEIs of trace fossils increase prior to the Ediacaran-Cambrian boundary (specifically, in both the Nasep and basal Spitzkop Members), and thus that the environment was being modified prior to the appearance of a Cambrian-type biota. To be clear…we draw no conclusions on the nature of Ediacaran-Cambrian boundary itself, and do not in any way dismiss the 'catastrophe' model (and, in fact, we dedicate an entire paragraph beginning line 387 explaining how our data do, and do not, fit into the 'biotic replacement' vs. 'catastrophe' debate). Something catastrophic may well occur at the Ediacaran-Cambrian boundary in Namibia during the depositionary hiatus, but this does not in any way impact our data that show an increase in metazoan ecosystem engineering millions of years beforehand.

4) "
If the biotic replacement model discussed by the authors is verifiable at the Ediacaran-Cambrian successions of Namibia due to the presence of a serious time gap?" CHANGES NOT MADE: As above, this comment seems to stem from a misunderstanding of the text -our study clearly articulates that our results support a key prediction of the 'biotic replacement' hypothesis, but also that, "the trace fossil data presented here are not mutually exclusive of a 'catastrophe'-type scenario involving abiotically-induced environmental changes" (lines 399-401). Thus, our study is not designed to provide a concrete test between the two models, but rather to test a key tenet of one model and does not in any way dismiss the other. We therefore see no need to amend this identification here, especially without a more detailed and focused re-analysis of the material.
Moreover, we note that, as another terminal Ediacaran index fossil (as per the Reviewer), it hardly matters whether the fossils are interpreted as Shaanxilithes or Paleopascichnusboth would identify this part of the Schwarzrand Subgroup as Ediacaran in age.

CHANGES MADE:
The text has been fixed as suggested -thank you. because of their spatial constraints, being covered potentially by any of the other four means of sediment reworking in the epifaunal and semi-infaunal tier". This overlap compromises the evaluation of the intensity of ecosystem engineering represented by each ichnotaxon in the Ecosystem Engineering Impact approach and as a result the values obtained in this way may be rather arbitrary. My suggestion here is that the authors may well dispense of the Ecosystem Engineering Impact approach and just use the scheme put forward by Minter and co-workers, which covers the same ground on a more consistent fashion."

CHANGES MADE:
We agree that this is a limitation to Herringshaw et al.'s (2017) EEI method. However, we find that the EEI scheme is useful in addressing the fluid dynamic properties of why some bioturbation behaviours are more 'impactful' than others notably from the perspective of bioirrigation potential, particularly as shown by theoretical work by van de Velde and Meysman, (2016). Additionally, we find that it is a useful visual aid for stratigraphically displaying these behaviours, and that it is important to employ a range of methods used by the paleontology, ichnology, and geobiology methods.
We do find it is important to address these caveats and also clarify that the Minter et al.
(2017) scheme addresses these issues as well as provides a different framework for analysing ecosystem engineering behaviours. We make this clear with the addition of the following statement to the methods section: "We note that a limitation to the EEI method is a spatial overlap (e.g., the surficial tier and surficial modifiers) and impossible combinations (e.g., the deep tier and epifaunal locomotion) between tiering and functional group ( 2) "Also, it may be advisable not to include in the analysis those forms which have not been assigned to an ichnotaxon because the behavioural significance of these may be unclear.
In any case, looking at the photographs, I would tend to think that those trace fossils illustrated in Fig Fig. 2F may be plug-shaped burrows as indicated by the authors, but also a preservational variant of a treptichnid (cutting the sample may resolve this issue). The one in Fig. 2G is really unconvincing and I am not even sure if it is a trace fossil. The one assigned to Planolites in Fig. 2I is unconvincing, I would place it in Helminthoidichnites. The one assigned to Streptichnus in Fig. 2K (note that the label is gone) is not convincing either, and it is too partially preserved to suggest an alternative name. In short, some adjustments are needed on this front and some of these will translate into changes in the evaluation of ecosystem engineering."

CHANGES MADE:
We agree with these suggestions. 'Form A' and the Planolites in Figure 2 have been updated as Helminthoidichnites. 'Form D' has been updated as Helminthopsis. 'Form B' and 'Form E' have been updated as Treptichnus. We have removed 'Form C' due to our inability to confidently consistently distinguish it from body fossils. For the plug-shaped burrows which may be in fact be poorly preserved Treptichnus, we maintain our initial descriptions on the basis that many plug-shaped burrow slabs cannot be cut as they remain in Namibia (either in outcrop if in situ or at the Ministry of Mines and Energy), and this gives us the most conservative estimate of their ecosystem engineering impact. We have noted this in the following addition: "Trace fossils broadly interpreted as plug-shaped burrows can be classified as either Conichnus or Bergaueria when cut open. However, due to the inability to distinguish the two ichnogenera (and, although we did not observe this in samples which were cut and polished, some plug-shaped burrows may be poorly preserved Treptichnus; see Jensen et al., 2000) on the bedding plane alone when slabs were not able to be cut open." (lines 195-199) We have also removed the few Streptichnus due to the lack of convincing samples, although added the following addition to the discussion noting that Streptichnus is found in the Spitzkop even if not noted in this dataset: "Furthermore, the occurrence of other trace fossils which represent similar complex engineering behaviours which have been reported from the Nama Group but are not included here, such as Streptichnus narbonnei in the Spitzkop Member (Jensen and Runnegar, 2005), add to the robustness of these data." (lines 309-312).
These updated ichnotaxa assignments have been reflected in a rewriting of the trace fossil descriptions in the Electronic Supplemental Material, S1. For these new assignments, we have referenced the Minter et al. (2017) supplemental dataset and Herringshaw et al.
(2017) to reassign previously indeterminate forms to their new ichnotaxa assignments and updated the EEI scores and cube occupation spaces accordingly. We also removed the point-counted bioturbation data for 'Form C' and Streptichnus. This data has been updated in the supplemental material, S5 and S6, and throughout the results, discussion, and results figures. However, because we had largely based our initial EEI and cube assignments for the indeterminate trace fossils on these assignments anyways, the data has not significantly changed enough to change our initial interpretations and conclusions.
3) "Finally, the author may wish to cite a recent paper that uses a similar approach to assess ecospace utilization in the interval of the Chapel Island Formation attributed to the Treptichnus pedum zone, comparing with the underlying strata in the same area. The CHANGES MADE: Thank you for this reference. We have cited this paper and its results as a comparison made to the observed trends we see in increased ecosystem engineering impact and behaviors: "This trend in increasing ecosystem engineering prior to the Cambrian is comparable to other Ediacaran-Cambrian sections worldwide, notably in the Ediacaran-aged Blueflower Formation of northwestern Canada where complex burrowing behaviours associated with