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Thanks for your attention to detail in response to the suggestions from the reviewers.
[# PeerJ Staff Note - this decision was reviewed and approved by Andrew Farke, a PeerJ Section Editor covering this Section #]
The reviewers did not identify major issues with your manuscript and I agree. They have some minor point that you should take care of, maybe most importantly being more explicit about the rationale for your research along the lines of the first reviewer's comment number 3.
Otherwise, I see no problems in publishing this manuscript.
The reporting is improved, a few issues with the citations that should be looked over. There are still some other issues.
1) The abstract still ends with an unclearly worded sentence.
2) Line 48, sentence starting with "The tympanic bulla's...": Technically the bony labyrinth is a space that contains soft tissue, not a bony element – consider rewording.
3) While the intro has more information about the bulla now, and I agree that not every paper "needs to be a magnum opus", it would still be nice to know what the questions of the study are and why the study was embarked upon. There should still be more specific information about the bulla, why it was chosen for the study, and how it helps to answer these questions. Was it simply a matter of, as I suggested before and the authors include in the methods, an easy thing to measure that maybe relates to hearing? If that is the case then maybe move that information to the introduction. Without this fundamental justification, the reader is not going be given much reason to carry on.
4) line 61, citations, see also Gearty et al. 2018 PNAS
Some improvement here, but as noted above the specific questions of the study are not outlined and it is not clear how the research fills an identified knowledge gap. There's perhaps some info in the discussion on this, so maybe some repetition from that area should be included in the introduction so readers know why the study was undertaken and how it can be useful.
It would be good to include in the methods information on whether the measurements were taken on physical specimens - it is unclearly worded currently, but perhaps implied. The methods figure provided may imply to readers that 3D surface models were used for measurements. If it was a combination of both, then this information should also be included somewhere.
I noticed that some of the measurements taken from the literature are from papers that were published before Tsai & Fordyce 2015 (the cited bulla measurement method). How are the authors sure that these earlier measurements were taken in the same way as their measurements? A sentence on justification would be good here.
The authors note in the methods why they elected to use the bulla. Some of this information would be better in the introduction (see above). There is also an implication that CT studies can't be replicated, which is incorrect. Again, if the reason for looking at the bulla is purely because it's easy to measure then include that info in the introduction.
Small note: Wording of first sentence of results needs adjustment.
Although the original research question(s) is still not clear, the discussion is still relatively informative and interesting. There are some citation errors, e.g., Galatius et al. 2019 is a paper that looks at the evolution of specialized hearing in whales, it does not talk about the paedomorphic cetacean ear. There are several papers that I suggested previously that do talk about how the organ of hearing in whales develops precocially, as with all mammals. It would be better to include those in this area, and perhaps the Galatius one in the part where other studies on hearing are discussed.
The authors have addressed my previous comments very well, and I have no further comments at this stage. It might be good to check through the references once more, e.g. in the Intro, line 6, you refer to Nummela et al. 2017; do you perhaps mean 2007 instead of 2017?
I trust this work will find its place in the future, perhaps together with some further studies, contributing to our understanding of scaling between ear structures and animal body size, and their constrains.
I agree with both reviewers that the references and citations need work. All citations need to be referenced, and no additional references should be provided. Your choice of papers to cite is unusual in a number of occasions, some papers that should be cited are not, some that are cited appear peripheral to your subject. Please be diligent about your choices, this alone is a major revision of your manuscript.
I also agree with the comment by the reviewers (although phrased somewhat differently by both) that the paper would benefit from some context. You mention the tension between phylogeny and functional aspects affecting the variables you study. Can you address more specifically, in introduction and discussion, how your results bear on that tension?
I feel less strongly about the request by reviewer 1 to include a discussion of ontogeny. I agree that ontogenetic scaling of the ear is very allometric, but do not believe that that needs to be addressed in depth in this paper.
The reviewers have many other significant comments on your paper that are less pervasive. Please address all of these, or let me know, explicitly, why you did not for each of them.
[# PeerJ Staff Note: Please ensure that all review comments are addressed in a rebuttal letter and any edits or clarifications mentioned in the letter are also inserted into the revised manuscript where appropriate. It is a common mistake to address reviewer questions in the rebuttal letter but not in the revised manuscript. If a reviewer raised a question then your readers will probably have the same question so you should ensure that the manuscript can stand alone without the rebuttal letter. Directions on how to prepare a rebuttal letter can be found at: https://peerj.com/benefits/academic-rebuttal-letters/ #]
[# PeerJ Staff Note: It is PeerJ policy that additional references suggested during the peer-review process should only be included if the authors are in agreement that they are relevant and useful #]
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This paper compares the relationship between tympanic bullae length and width measurements and bizygomatic width (a measure of skull size that correlates with body length in whales) across a large dataset of whales from “archaeocetes” to modern clades. The methodology seems sound, and the results are expected as per previous studies, but there are some issues with the paper discussed below that, if addressed, will make it acceptable for publication in PeerJ.
The three most important issues with the paper are: 1) the lack of contextualization of the paper (i.e., why was it done in the first place?), 2) lack of complete referencing; and, 3) lack of discussion of development as a possible constraint on bulla size in adulthood.
Expanding on the first point (lack of contextualization): It is never clearly stated in the introduction (nor circled back round to in the discussion) why the project was implemented, and what the implications of the results might be in the broader context of the widely and long-studied evolution of whale ears. A suggestion for improvement in this area might be to reframe the introduction. More clearly state that body size is probably the most important influence on the biology of animals, but almost nothing in organisms scales proportionally/isometrically. Given this, what sorts of results would you have expected to find? If the authors don’t expect body size to correlate with bulla size, why? What exactly is the role of the bulla, and what about whale bullae should be different or unusual compared with other parts of the skull? The size of the inner ear labyrinth (within the petrosal, not studied here) is strongly correlated with body mass (Ekdale 2015 J Anat, Racicot et al. 2016 BJLS), so why would one expect other parts of the ear not to be?
In terms of the second point (citations): The in-text citations are often irrelevant or likely incorrect – several, but not all, examples are listed below in the detailed line-by-line comments. Upon first read one gets the impression that the authors have not read any of the many papers on whale ear morphology that have been published over the years. When one reaches the bibliography, one finds that many of the important papers are listed, with quite a few unusual inclusions and omissions. For the omissions, a non-thorough list of alternative papers is included in the line-by-line comments. Given that I cannot thoroughly correct the paper for citation errors and exclusions, the authors should thoroughly review and correct citations in the paper.
Lastly, in terms of the third point (the lack of discussion surrounding development): The authors hint at the precocial nature of ear bone development in whales (actually this is true for all mammals) with one sentence in the introduction, but it is not discussed again. Based on the results of the paper, developmental constraints on ear bone size seem like a logical explanation for why the trend in baleen whales isn’t the same as the other groups. Similarly, precocial development and impacts of paedomorphism on the evolution of skulls may explain some of the trends seen in the groups of odontocetes that are known for possessing paedomorphic characteristics, e.g., see Galatius and Kinze 2003 Can J Zool, Galatius et al. 2006 Acta Zool, Galatius 2010 BJLS, Galatius et al. 2011 J Morph for discussions and quantitative analyses of phocoenids.
Below please find line-by-line suggestions and corrections:
The authors write “only about 70%” – 70% is a large proportion of the data that can be explained by the proxy for body size. Consider rephrasing.
The final sentence as written is a bit confusing. First, the results, rather than the dataset, would ‘suggest’ “that auditory functional capacity is dependent on congruent osteological morphology rather than allometric scaling”. Second, the quoted line is a bit confusing as worded. Please consider rewriting – I don’t have a suggestion, as I am not clear on what is meant.
It might be worth citing Ketten papers (most are in the bibliography) and Ekdale 2015 J Anat that include discussion of the correlation between ear size and body size.
Line 36: Citations listed here are not papers about hearing in whales.
Line 39: Several additional citations could be included here, but one of particular interest is: Lancaster et al. 2014. Mar Mam Sci
Paragraph starting with Line 43: Quite a few more citations on the evolution of whale hearing and anatomy are needed throughout this paragraph. Further, could it be explained somewhere how the tympanic bulla is specific to whales? It is homologous to the tympanic bulla in other mammals, so if there’s something the authors want to point out as special about it, it would be good to go into some specifics about how it functions compared to other mammals. It would also be interesting if the authors could explain why or how its size might affect auditory capacity.
Line 53: I am not sure if the Yamato & Pyenson paper discusses fossil-related markers of acoustic evolution, and the Geisler et al. 2014 paper does not discuss ear bones in the main text. It might be worth mentioning somewhere here that other researchers have been using the periotic/petrosal, which is a lot more robust than bullae and contains a great deal more anatomical information, including the internal anatomy, to understand the evolution of whale hearing (among other aspects of sensory evolution). A nonexhaustive list of additional papers that should be included here are: Ekdale & Racicot 2015 J Anat, Galatius et al. 2019 BJLS, Mourlam & Orliac 2017 Curr Biol, Park et al. 2016 Biol Lett, Park et al. 2017 Proc Roy Soc B, Park et al. 2019 BMC Evol Biol, Racicot et al. 2016 BJLS, Racicot et al. 2018 J Anat, Racicot et al. 2019 Biol Lett. Although the periotic may be more phylogenetically and anatomically informative regarding hearing, an advantage of the present paper is that the measurements used might be quick and easy to replicate, assuming you have complete skulls with completely preserved bullae.
Did the authors need to do any correction for damage to the bullae (bullae are a bit more fragile than petrosals) or skulls, particularly in fossils? Or were all specimens used in completely perfect condition? Is it possible to decide that a fossil is undamaged? Were none of the fossils used distorted during the fossilization process?
How was bulla length and width measured? Were specific anatomical landmarks used? If so, please include this information. Figure 1 is not particularly informative regarding these questions.
Starting from Line 148, sentence beginning “These non-“: This part of the paragraph should go into the discussion. Log transformation is standard for these types of analyses. The line “increases in magnitude” is unclear in meaning.
Line 154, sentence beginning “However, as body size increases”: This belongs in the discussion.
Line 156 sentence beginning “We conducted…”: Suggest reword to “Our PIC analysis yielded no genus-level...”
This section will need some restructuring to better explain and reframe the results as suggested regarding the introduction. Circle back to the main points of why the project was done, what the main findings were, what do they mean in the broader context of what we already know and what we can use them for moving forward.
Line 169: These citations should be modified. Perhaps the authors need only cite the Society for Marine Mammalogy Committee on Taxonomy list.
Line 170, sentence beginning with “Whale ear bones…”: The paper cited here (Slater et al. 2017) does not mention the words “ear bones” nor any related words, nor does it discuss or address ear or hearing evolution in whales. If the authors mean, “Whale body size”, then rephrase.
Line 175: This first sentence should actually be somewhere in the introduction. It can be restated in the discussion but there is no mention of function in the introduction where we really need an understanding of what the authors are investigating and why.
Line 175, whole paragraph: Here is where the authors should also mention developmental constraints. The three possible factors are all related.
The reference list is quite impressive, although many important papers are not cited in the main text. Also, many can likely be excluded from the list. For example, Racicot & Berta 2013 – while pterygoid sinuses are related to sound reception, I would suggest citing the papers listed above that directly investigate the inner ears of different cetacean groups.
Figure 1. The bulla measurements should be shown in the same way as the BZW measurements, i.e., with ticks at the ends of the lines rather than arrows. Otherwise, it is unclear where precisely the measurements were taken.
Figures 2–3. Both figures should include the r-squared and p-values for each regression line somewhere in the blank space of the plots.
What are the limits on whale ear bone size? Non-isometric scaling of the cetacean bulla, by Groves et al.
1. This ms studies the morphometrics of the cetacean tympanic bullae in a large set of different cetacean skulls, both extinct and extant. The tympanic bulla forms part of the cetacean peripheral hearing organ, and its size is of relevance for the auditory characteristics of an animal. This also seems to be the purpose of the authors, to provide data that would increase our understanding of the evolution of cetacean hearing better. The authors mention various issues that might lie behind the scaling results found for the tympanic bulla.
2. The cetacean tympanic bulla is found to be "non-isometric" when related to body size. I wonder why it was expected in the first place that the bulla would be isometric; many structures in different mammals have been found to be allometric, and positively allometric, like also in this ms, for example the middle ear structures that lie within the bulla, i.e., the middle ear ossicles and their parts (see e.g., Nummela et al. 1999, Scaling of the cetacean middle ear. Hear. Res. 133: 71-81)
3. Resolving the dilemma between phylogenetic vs. functional vs. ecological causes/constraints is not an easy task, and that was evidently not the task here either, however, the authors keep on talking about the different constraints without ever really taking the discussion any further.
4. Were you only concerned about the upper size limit for the cetacean bulla, or also about the lower size limit of the bulla? It might be fruitful to ask, how small a cetacean bulla can be, in order to still house the structures needed for its auditory task. In any case, I was expecting some more discussion on the functional aspects of size, at least in odontocetes.
5. Lines 164-165: "Our results demonstrate that all cetacean ear dimensions increase in a positively allometric pattern irrespective of taxonomic identity or phylogenetic history." Did you measure "all ear dimensions"? I think this statement is somewhat an exaggeration.
6. Lines 172-174: "Such departures from linearity suggest that functional auditory capacity is not based on proportional congruences, but may instead be constrained by functional or biological auditory limits." So, what you say here is that functional auditory capacity may be constrained by functional auditory limits. Could you rephrase the sentence so it would become more clear what you actually mean with this.
7. Additionally, related to this discussion when including mysticetes, it might be good to point out that the hearing mechanism of mysticetes has not yet been quite resolved, at least one can say that it is not the mechanism which odontocetes use, so drawing direct conclusions from the bulla size to its function is a bit uncautious.
8. Lines 178-180: "The pachyosteosclerotic bulla enhances the reception of sound underwater, and therefore may be bound within a functional size range." Could you explain what you mean with this?
You list about 130 references for the ms, of which I could find only 21 among the text. This is certainly unintentional. For the Supplemental references, I didn't start checking. Please check these through and make the corrections needed in both reference lists.
All the figures are clear and illustrative, they show well how the measurements were taken, and what the results are.
For each individual, did you use both bullae separately, or did you calculate the mean value for the left and right bulla? Aren't the left and right bulla size dependent on each other, as they are products of one and same individual?
This is an important work in that it adds to our knowledge on the morphometrics of the cetacean auditory structures, and given that cetaceans now after their evolution of over 50 million years probably have reached their maximun body size, it is fascinating to ask the question what constrains the size of their hearing organ, and of course their whole body size. The results of this ms are certainly useful for future pondering.
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