New Geometric Morphometric Insights in Digital Taphonomy: Analyses into the Sexual Dimorphism of Felids through Their Tooth Pits
, Juan-José RodrÃguez-Alba 1, Antonio Garrucho 4, Jesús Recuero 4 and José Yravedra 1,2,5,*Round 1
Reviewer 1 Report
The study analyzes tooth pits on bones left by two closely related felid species for a purpose to ascertain whether there are sexual differences in the tooth pits' shape and size, i.e., whether sexual dimorphism in skull size and morphology contributes to intraspecific variability in tooth marks. The authors conclude that sexual dimorphism of the two species is not reflected in tooth pits, and sexual dimorphism is thus not a confusing factor in the species identification.
The tooth pits were analysed using by geometric morphology of 3D surface scanning model, and the methodological aspect of the study is really nice and impressive. Unfortunately, the datasets of tooth marks come only from one male and one female, and it is my major concern with the study. Although there were roughly 50 tooth pits per sex/species analysed, they are not independent – they come only from one individual and may thus not cover the intrasexual variability. For this reason, I am very sorry, but I do not fully agree with the authors' conclusion that “the present results reveal the sexual dimorphism present in these felid species to not be a conditioning factor of tooth pit morphology”. There are undoubtedly no differences between the particular male and female, but I am afraid that this conclusion cannot be extrapolate to the whole population. The obtained results may be false negative, considering small dataset (and also fact that in wolves there are detectable sexual differences (as stated by authors in Line 76)).
The solution may lie either in analysing of tooth pits on additional individuals (although I understand that it is undoubtedly problematic to obtain enough individuals of such species), or in rewriting the manuscript – in my opinion, the sexual dimorphism aspect should not be the main goal of the study (even though it is an interesting and important issue). The study should aim on the differences between the two closely related species, and sexual differences should be secondary outcome, with emphasizing that generalization may be problematic.
Specific comments and changes:
Line 47: citations 11 and 1 should be in brackets.
Line 48: “In this same study” – which study is meant?
Line 50: Citation 2 should be in bracket.
Line 70: replace “effecting” by “affecting”.
Line 76: Citation 10 should be in bracket, and I suggest to provide it as Toledo et al. [10]. Besides, I did not find the information in the referenced study (but maybe I did not find thoroughly).
Line 83: I did not expect that I ever use this phrase in science, but “to be or not to be”?
Line 86: As scientific names firstly appeared in the text, provide please authors of descriptions.
Line 103: Author and date of description should not be in brackets (the subspecies was describe in the current genus), but see previous comment.
Line 113: I suppose that the bovine ribs were provided with tissue, so afterwards they were probably cleaned. If so, please provide information.
Line 128: Citation 13 should be in bracket.
Line 174: Table 1.
Line 221: “has be” probably should be “has been”.
Lines 225 and 228: citations should be in brackets.
There are many errors in References and should follow format required by the journal:
Volume should be in italics.
Some Journal names are not abbreviated, e.g. Lines 298, 311, 353, 363, 366.
In some cases there is Year both after authors as well as after Journal name, e.g. Lines 284, 295, 324, 374.
In some cases scientific names are not in Italics, e.g.: Lines 335, 339, 341.
There are typos: e.g. “Scientific Repotrs”.
Line 320: Delete “a “after “J.M.”.
In some cases the Title of article is written with all first letters capital, e.g. reference n. 16
In some cases there issues after journal volume, e.g. Lines 280, 282, 293, 315, 336, 354, 356, 361, 363, 367.
Author Response
Comments to reviewer 1.
Rev 1.The study analyzes tooth pits on bones left by two closely related felid species for a purpose to ascertain whether there are sexual differences in the tooth pits' shape and size, i.e., whether sexual dimorphism in skull size and morphology contributes to intraspecific variability in tooth marks. The authors conclude that sexual dimorphism of the two species is not reflected in tooth pits, and sexual dimorphism is thus not a confusing factor in the species identification.
The tooth pits were analysed using by geometric morphology of 3D surface scanning model, and the methodological aspect of the study is really nice and impressive. Unfortunately, the datasets of tooth marks come only from one male and one female, and it is my major concern with the study. Although there were roughly 50 tooth pits per sex/species analysed, they are not independent – they come only from one individual and may thus not cover the intrasexual variability.
For this reason, I am very sorry, but I do not fully agree with the authors' conclusion that “the present results reveal the sexual dimorphism present in these felid species to not be a conditioning factor of tooth pit morphology”. There are undoubtedly no differences between the particular male and female, but I am afraid that this conclusion cannot be extrapolate to the whole population. The obtained results may be false negative, considering small dataset (and also fact that in wolves there are detectable sexual differences (as stated by authors in Line 76)).
Reply: We have lightened both the conclusion and the abstract according to the reviewer’s suggestion
According to the reviewer we state that sexual differences are present in wolves. We can see where the confusion has arisen, however did not mean this. The particular sentence the reviewer is referring to cites the work of Toledo et al. 2021 who found sexual differences in bite marks on dental wax (proposed as an analogy with flesh), as opposed to differences in the actual tooth marks. This is due to the distribution and actual size of female and male wolf teeth, but is not a factor in tooth mark morphology. We have thus tried to rectify and clarify this sentence.
From a different perspective, the review also mentions the possibility of these observations being a False Negative, which is a calculation we have indeed performed, and when concluding about the possibility of differences or similarity between sexes, our conclusions are still fairly strong.
Nevertheless, in light of the reviewers concerns, in future we will pay particular attention to obtaining a sample with more individuals of the same species.
The solution may lie either in analysing of tooth pits on additional individuals (although I understand that it is undoubtedly problematic to obtain enough individuals of such species), or in rewriting the manuscript – in my opinion, the sexual dimorphism aspect should not be the main goal of the study (even though it is an interesting and important issue). The study should aim on the differences between the two closely related species, and sexual differences should be secondary outcome, with emphasizing that generalization may be problematic.
Reply: The precise objectives of the present study were to detect whether sexual dimorphism is a conditioning factor in tooth mark morphologies, considering how differentiating between different carnivore species is already possible and not as innovative.. In a series of prior studies, we have already shown how our methodological approach is able to differentiate between different species of felids and canids (see references 1, 2, 3, 11, 18, 20, 21), while citation number 21 specifically mentions differentiation between 3 types of felids, including leopards, jaguars and lions.
The novel elements of the present study therefore are the intra-species analyses performed. The present study has been able to conclude that our samples show notable similarities between the two marks produced by different individuals of different sexes in the same species, presenting a 4 to 10% chance of these observations being a false positive. If the results were to be different, this would imply the need to produce much larger experimental samples with the need for separation between sexes in comparative studies with the fossil register
Specific comments and changes:
Line 47: citations 11 and 1 should be in brackets.
Reply: We have corrected this
Line 48: “In this same study” – which study is meant?
Reply: we have added the reference
Line 50: Citation 2 should be in bracket.
Reply: We have corrected this
Line 70: replace “effecting” by “affecting”.
Reply: We have corrected this
Line 76: Citation 10 should be in bracket, and I suggest to provide it as Toledo et al. [10]. Besides, I did not find the information in the referenced study (but maybe I did not find thoroughly).
Reply: We have added brackets around citation number 10 and included the term “Toledo et al.”. We apologize that in the original version of the manuscript we were incorrectly citing Toledo ety al. 2021 and should have been citing Toledo et al. 2020, which would explain why the reviewer could not find the information they were looking for.
Line 83: I did not expect that I ever use this phrase in science, but “to be or not to be”?
Reply: There was a typo here which we have corrected
Line 86: As scientific names firstly appeared in the text, provide please authors of descriptions.
Reply: We have corrected this
Line 103: Author and date of description should not be in brackets (the subspecies was describe in the current genus), but see previous comment.
Reply: We have corrected this
Line 113: I suppose that the bovine ribs were provided with tissue, so afterwards they were probably cleaned. If so, please provide information.
Reply: We have completed the corresponding sentence, however should already be implied by the term “weekly feeding”
Line 128: Citation 13 should be in bracket.
Reply: We have corrected this
Line 174: Table 1.
Reply: We have corrected this
Line 221: “has be” probably should be “has been”.
Reply: We have corrected this
Lines 225 and 228: citations should be in brackets.
Reply: this has been changed
There are many errors in References and should follow format required by the journal:
Reply: We have corrected this
Volume should be in italics.
Reply: We have corrected this
Some Journal names are not abbreviated, e.g. Lines 298, 311, 353, 363, 366.
Reply: it is made, these have been corrected
In some cases there is Year both after authors as well as after Journal name, e.g. Lines 284, 295, 324, 374.
Reply: it is made, these have been corrected
In some cases scientific names are not in Italics, e.g.: Lines 335, 339, 341.
Reply: it is made, these have been corrected
There are typos: e.g. “Scientific Repotrs”.
Reply: it is made, these have been corrected
Line 320: Delete “a “after “J.M.”.
Reply: it is made,
In some cases the Title of article is written with all first letters capital, e.g. reference n. 16
Reply: it is corrected,
In some cases there issues after journal volume, e.g. Lines 280, 282, 293, 315, 336, 354, 356, 361, 363, 367.
Reply: it is corrected,
Reply: We apologies for these careless mistakes and have made all the corresponding corrections.
Author Response File: 
Author Response.docx
Reviewer 2 Report
APPLSCI-1339148
New Geometric Morphometric Insights in Digital Taphonomy; analyses into the sexual dimorphism of felids through their tooth pits.
The authors have attempted to study the relationship between tooth pits between 2 species of felids, the raised question is interesting and is relatively an innovative tool for taphonomy. Nevertheless, I have some observation through the article that must be fixed before to be considered for a publication, a principal one should be revised carefully by a native speaker, and particularly I have some doubts related to the way of the authors decide to perform the analyses. I recommend include a test of measurement error (repeated measurement)
The use of geometric morphometrics methods nowadays has been applied in multiple areas of science in some can be applied in other is difficult to extrapolate the results for an easy interpretation, due to is applied science the journal where is being revised this article I not sure how other authors will validate this results in other studies, more advice about the use of this technique is missing here as an application.
Specific comments
The main of the specific comments are regarding grammar mistakes please its important to the authors send this article for a native speaker deep revision.
Line 35: Delete Great
41-45 Rephrase the sentence was hard to read I not sure what the authors mean with modern day ecological context
46-51: Also need rephrase I think maybe need 2 different paragraphs one that talk about 3D technology in taphonomy and other different about GMM.
74-48: Need Grammar check.
76: delete for example
79: delete nor confirmed.
Material and Methods
2.1 Sample
94: First the author mention the species Panthera tigris sandaica, then in line 96 Panthera tigris sandaica /sumatrae: this is not clear delete sumatrae or explain why are different
Line 96-100: This paragraph belong to Introduction, should be removed from methods
Line 103-108: This paragraph belong to Introduction, should be removed from methods
Line 128: proposed by Authors et al [13]. If not is not clear what you mean.
Line 133: The version of R seems to be wrong. Also there are no packages mentioned at all for any mehod
Line 146: I suggest before any further analyses test for measurement error, the location of landmarks seems to be hard to replicate and a measurement error indicating no problem with digitalization will solve this problem.
149-150: Not clear why authors decide go on use form. Allometry could be part and work with shape anyway by extracting the allometry of the analysis.
Line 152: Please fix redundancy
Line 157: What analyses were performed with the scores, why they were extracted.
Line 161: When you needed to use non-parametric in this study, normally GMM analyses are always parametric, develop such idea to the readers be clear with your analysis.
Line 170: Which packages were used? Again R version is wrong.
Line 175: grammar check.
Line 206-211: This sentence is not clear to me, please develop better the idea.
Line 215: Be careful with this, size is always a part of shape analyses are you mixing to spaces? Please take a look the following article for a deep understanding of the topic. Klingenberg 2016. Size, shape, and form: concepts of allometry in geometric morphometrics Development Genes and Evolution 226, 113-137.
Author Response
New Geometric Morphometric Insights in Digital Taphonomy; analyses into the sexual dimorphism of felids through their tooth pits.
The authors have attempted to study the relationship between tooth pits between 2 species of felids, the raised question is interesting and is relatively an innovative tool for taphonomy. Nevertheless, I have some observation through the article that must be fixed before to be considered for a publication, a principal one should be revised carefully by a native speaker, and particularly I have some doubts related to the way of the authors decide to perform the analyses. I recommend include a test of measurement error (repeated measurement)
Reply: One of the authors of this paper is a native speaker (Lloyd Austin Courtenay), and he has now re-read the text to ensure correct use of English. But we have a new revision of the edition of text.
With regards to the need for measurement error calculations, we have now included this information.
The use of geometric morphometrics methods nowadays has been applied in multiple areas of science in some can be applied in other is difficult to extrapolate the results for an easy interpretation, due to is applied science the journal where is being revised this article I not sure how other authors will validate this results in other studies, more advice about the use of this technique is missing here as an application.
Reply: Our methods have been published in great detail and can be consulted in all the referenced papers included within our manuscript. For the positioning of landmarks, the study by Courtenay et al. 2020 in PLoS ONE includes a manual for the positioning of landmarks on tooth pits as well as a detailed description for greater replicability. Similarly, all code and algorithms have been included in multiple studies.. Please consult:
Courtenay, L. A.; Yravedra, J.; Maté-González, M. A.; Vázquez-Rodríguez, J. M.; Fernández-Fernández, M.; González-Aguilera, D. The effects of prey size on carnivore tooth mark morphologies on bone; the case study of Canis lupus signatus. Hist. Biol. 2020a. https://doi.org/10.1080/08912963.2020.1827239
Courtenay, L. A.; Herranz-Rodrigo, D.; Huguet, R.; Maté-Gonzalez, M. A.; Gonzalez-Aguilera, D.; Yravedra, J. Obtaining new resolutions in carnivore tooth pit morphological analyses: A methodological update for digital taphonomy. PLoS ONE 2020b, 15(10), e0240328. https://doi.org/10.1371/journal.pone.0240328
Courtenay, L. A.; Herranz-Rodrigo, D, González-Aguilera, D.; Yravedra, J. Developments in data science solutions for carnivore tooth pit classification. Sci. Rep. 2021a, 11,10209 https://doi.org/10.1038/s41598-021-89518-4
Specific comments
The main of the specific comments are regarding grammar mistakes please its important to the authors send this article for a native speaker deep revision.
Reply: We have since revised the text
Line 35: Delete Great
Reply: We have corrected this
41-45 Rephrase the sentence was hard to read I not sure what the authors mean with modern day ecological context
Reply: As we have already stated, modern day ecological contexts refers to “livestock predation”.
46-51: Also need rephrase I think maybe need 2 different paragraphs one that talk about 3D technology in taphonomy and other different about GMM.
Reply: We have revised the paragraph and included more details about 3D technologies in taphonomy
74-48: Need Grammar check.
Reply: We have corrected this
76: delete for example
Reply: We have corrected this
79: delete nor confirmed.
Reply: We have corrected this
Material and Methods
2.1 Sample
94: First the author mention the species Panthera tigris sandaica, then in line 96 Panthera tigris sandaica /sumatrae: this is not clear delete sumatrae or explain why are different
Reply: really Panthera tigris sandaica /sumatrae: is the actual new nomenclature, but how there are authors that they do not use this term, we have unified the term to Panthera tigris sandaica,
Line 96-100: This paragraph belong to Introduction, should be removed from methods
Reply: We have corrected this
Line 103-108: This paragraph belong to Introduction, should be removed from methods
Reply: We have corrected this
Line 128: proposed by Authors et al [13]. If not is not clear what you mean.
Reply: This reference explain a detailed methodology used in the 3D reconstruction of tooth marks and the use of land marks. See supplementary material of this reference of reference 19 and 20. We have added the reference 20.
The references 19 and 20 were the previous 13 and 14
Line 133: The version of R seems to be wrong. Also there are no packages mentioned at all for any mehod
Reply: Reply: We are not sure as to what the reviewer is referring to, as the version of R we have stated is perfectly correct – Version 4.0. The reason we have not included the packages is that the list is very long. There is no single package that can perform the analyses we have carried out and we would undoubtedly saturate the text. From another perspective, many of the functions and algorithms we use are programmed and written directly by one of the authors (L.A.C.), therefore are not yet incorporated into an R library.
Line 146: I suggest before any further analyses test for measurement error, the location of landmarks seems to be hard to replicate and a measurement error indicating no problem with digitalization will solve this problem.
Reply: Reference 20 (previous 14) provides a very detailed description on how to replicate our methods, including instructional videos and a manual for replicability. We have, however, followed the reviewer’s recommendation of including a measurement error for landmark placement.
. 149-150: Not clear why authors decide go on use form. Allometry could be part and work with shape anyway by extracting the allometry of the analysis.
Reply: We do not go on to use form, we are just explaining what we would do if allometry were found to be significant, as indicated by the term
Line 152: Please fix redundancy
Reply: We have corrected this
Line 157: What analyses were performed with the scores, why they were extracted.
Reply: The scores were not analyzed because according to reference 22 (previous ref 16), the scores present intraspecific differences between populations. This study show how the tooth pits of 4 different populations of wolves (2 captivity and 2 wild wolves’ populations) do not have differences in the tooth pits. On contrary the scores are similar in wild wolves, but these scores are different in the two captivity wolves. The captivity stage affect to the variability of score, and this is the cause because we do not use the scores in this study.
For the text we have add this sentence at end of methods section.
Line 161: When you needed to use non-parametric in this study, normally GMM analyses are always parametric, develop such idea to the readers be clear with your analysis.
Reply: we have added new explanation and we added new references as examples for the readers
Line 170: Which packages were used? Again R version is wrong.
Reply: As we have answered before, the version of R we have stated is perfectly correct - Version 4.0. and we consider it unnecessary to add all the R libraries as suggested by the reviewer. This exceeds the objective of the work, and also implies access to libraries that everyone can download freely.
Line 175: grammar check.
Reply: We have corrected this
Line 206-211: This sentence is not clear to me, please develop better the idea.
Reply: We have clarified and changed this paragraph
Line 215: Be careful with this, size is always a part of shape analyses are you mixing to spaces? Please take a look the following article for a deep understanding of the topic. Klingenberg 2016. Size, shape, and form: concepts of allometry in geometric morphometrics Development Genes and Evolution 226, 113-137.
Reply: We had already considered this, thank you very much for the reference.
Author Response File: Author Response.docx
Round 2
Reviewer 1 Report
I thank the authors for their answers and corrections. I have only few minor suggestions:
Line 91: Are you sure that the year of description is 1949 – should not it be 1956?
Line 100: Delete the author and year of description.
Lines 98-99: “In this case, the male individual studied weighed 120.0 kg and the 98 female 86.2 kg.” – This information should be in Materials and methods, not in Introduction.
Line 105: Ditto.
Lines 119-120: Can you please specify how were the ribs cleaned – or they did not?
Line 321: “inPhysical” – Add space.
Line 323: “inthe genus” – Add space.
Lines 325, 327 and 330: Replace commas between authors' names with semicolon.
Line 333: Delete “.” in front of “Courtenay, L. A.”
Line 381: Journal name should be abbreviated.
Line 390: Article name should not be in Italics.
Line 392: Delete “.” in front of “Cohen, J.”
Line 402: Delete “2” in front of “Colquhoun, D.”
Author Response
I thank all comments. We have following all sugestions
Line 91: Are you sure that the year of description is 1949 – should not it be 1956?
Reply: this is corrected
Line 100: Delete the author and year of description.
Reply: this is corrected
Lines 98-99: “In this case, the male individual studied weighed 120.0 kg and the 98 female 86.2 kg.” – This information should be in Materials and methods, not in Introduction.
Reply: this is corrected. Now this is in sample
Line 105: Ditto.
Reply: this is corrected. Now this is in sample
Lines 119-120: Can you please specify how were the ribs cleaned – or they did not?
Reply: this information have been added
Line 321: “inPhysical” – Add space.
Reply: this is corrected
Line 323: “inthe genus” – Add space.
Reply: this is corrected
Lines 325, 327 and 330: Replace commas between authors' names with semicolon.
Reply: this is corrected
Line 333: Delete “.” in front of “Courtenay, L. A.”
Reply: this is corrected
Line 381: Journal name should be abbreviated.
Reply: this is corrected
Line 390: Article name should not be in Italics.
Reply: this is corrected
Line 392: Delete “.” in front of “Cohen, J.”
Reply: this is corrected
Line 402: Delete “2” in front of “Colquhoun, D.”
Reply: this is corrected
Author Response File: Author Response.docx
Reviewer 2 Report
The following article after a revision meet the requirement of publication,
1- Nevertheless I could not find the measurement error there are not placed in the methodology and not find any results about it. Please add it to the results to be finally published.
Author Response
We thank the comments of reviewer. We are sorry do not put the measurement error in the methodology and results, however, we consider that this would be repetitive since the reproduction error is addressed in references 20 and 21. Reference 20 and 21 provides a very detailed description on how to replicate analyses test for measurement error. Ref 20 included a video of how Landmark collection was performed using the free Landmark Editor software (v.3.0.0.6.) Inter-analyst experiments prior to landmark collection revealed the landmark model to have a robustly defined human-induced margin of error of 0.14 ± 0.09 mm (Median ± Square Root of the Biweight Midvariance). Detailed explanations as well as an instructional video on how to place both landmarks and semilandmarks can be consulted in the Supplementary Appendix and main text of ref 20. Finally, ref 21 shows a practical application of the error calculation in a work with a methodology similar to that described in this work.
Author Response File: Author Response.docx
