Darwin’s Digestion Myth: Historical and Modern Perspectives on Our Understanding of Seed Dispersal by Waterbirds

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

The paper addresses a fascinating and underexplored topic, providing a paper presents a comprehensive historical analysis of the concepts of endozoochory and epizoochory in the context of seed dispersal by waterbirds, focusing on the misconceptions propagated by Darwin’s initial assertions. The paper is well-researched and provides valuable insights into the evolution of scientific thought regarding seed dispersal mechanisms. The authors successfully argue the need for reassessment of current understanding, emphasizing the overlooked importance of endozoochory. The manuscript is well-structured and well-written, offering significant contributions to the fields of ecology and biogeography. However, there are several areas where the paper could be strengthened to enhance its clarity, impact, and scholarly rigor. Please see the appendix.

Comments for author File: Comments.pdf

Comments on the Quality of English Language

The English language quality of the manuscript is generally good, with a clear and coherent structure that effectively communicates complex historical and scientific concepts. The academic tone is appropriate, and the use of scientific terminology is accurate. However, there are areas for improvement, such as simplifying complex sentences for better readability, organizing paragraphs for improved coherence, and reducing the overuse of passive voice to make sentences more direct. Additionally, consolidating repetitive information, enhancing precision and conciseness, and correcting minor typographical and grammatical errors through thorough proofreading will significantly improve the manuscript's overall quality and readability.

Author Response

“The paper addresses a fascinating and underexplored topic, providing a paper presents a comprehensive historical analysis of the concepts of endozoochory and epizoochory in the context of seed dispersal by waterbirds, focusing on the misconceptions propagated by Darwin’s initial assertions. The paper is well-researched and provides valuable insights into the evolution of scientific thought regarding seed dispersal mechanisms. The authors successfully argue the need for reassessment of current understanding, emphasizing the overlooked importance of endozoochory. The manuscript is well-structured and well-written, offering significant contributions to the fields of ecology and biogeography.”

Thank you.

 

“However, there are several areas where the paper could be strengthened to enhance its clarity, impact, and scholarly rigor. Please see the appendix.”

A key, and very useful, suggestion in their appendix was to add summary table or bullet points. See the new Table 1 that aims to help the reader keep track of the chronology. We think the new Graphical Abstract will aso help to convey key points.

This reviewer also made similar suggestions to reviewer 2 about making several definitions more obvious. We have done this (see comments below under reviewer 2). We have also clarified that we did not carry out an electronic literature review.

Our further responses to details that were provided within the reviewer’s appendix are as follows:

We are limited in the abstract by the instructions to keep to “a total of about 200 words maximum”, but have made several changes in response to the review.

We have made a modification to the title, similar to that suggested.

We have changed the order of text, to deal with many of the comments. We have included some of the sentences proposed for the Introduction.

We have created a clear methods section and added clarifications.

We have added many new subheadings and reorganized the text, in the light of the referees’ suggestions.

 

 

 

Comments on the Quality of English Language

 

“The English language quality of the manuscript is generally good, with a clear and coherent structure that effectively communicates complex historical and scientific concepts. The academic tone is appropriate, and the use of scientific terminology is accurate. However, there are areas for improvement, such as simplifying complex sentences for better readability, organizing paragraphs for improved coherence, and reducing the overuse of passive voice to make sentences more direct. Additionally, consolidating repetitive information, enhancing precision and conciseness, and correcting minor typographical and grammatical errors through thorough proofreading will significantly improve the manuscript's overall quality and readability.“

We have now made many editorial changes thoughout the paper, but note that the other two reviewers seemed happy with the prose style.  

Reviewer 2 Report

Comments and Suggestions for Authors

 This review sought to examine the history of research into plant species dispersal by waterbirds. In particular, how and why our understanding of this process has gone around in circles over time. The history of the subject is important due to polarized debate around the relative importance of epizoochory vs endozoochorey. Authors have made considerable effort to include historical publications not written in English and are concerned with the dispersal of both terrestrial and aquatic plants (regardless of whether or not they produce fleshy fruits).

In my opinion, authors do a good job of being historians writing about science (although you’d have to ask a historian in the field of science writing to be sure).  The review is well written and interesting. It is divided into centuries, acknowledging the pre- and post-first world war break point. The toing and froing of opinion over time, between the relative importance of epizoochory vs endozoochorey (both evidence-based and not), becomes very clear in the review

 A critical question emerges  – do seeds survive gut passage? Given the importance of this question, it struck me that simulated gut passage treatments (i.e. seed scarification, acidification, or both) are not mentioned in the paper. I would assume, in relation to contemporary studies, it might be relevant, although I understand that experimental methods are not a focus of this paper.

In addition, authors discuss multiple studies in which seeds recovered from bird faeces germinated better than control seeds. Authors might consider exploring the opinions of co-evolution of bird and plant species, and gut passage as a germination requirement/an important part of the seed germination strategy. I would assume this idea would support endozoochorey?

May I also suggest that ‘waterbirds’ be defined early on (for us plant people), and that the ‘digestion myth’ (integral to the title, abstract and paper) be introduced earlier than line 230.

Congrats to authors on a great paper.

Author Response

“This review sought to examine the history of research into plant species dispersal by waterbirds. In particular, how and why our understanding of this process has gone around in circles over time. The history of the subject is important due to polarized debate around the relative importance of epizoochory vs endozoochorey. Authors have made considerable effort to include historical publications not written in English and are concerned with the dispersal of both terrestrial and aquatic plants (regardless of whether or not they produce fleshy fruits). In my opinion, authors do a good job of being historians writing about science (although you’d have to ask a historian in the field of science writing to be sure).”

Thank you. We are not aware of any science historian who has made more than passing reference to this topic. However, one of us (DMW), has a track record of writing history of science papers.

 

“The review is well written and interesting. It is divided into centuries, acknowledging the pre- and post-first world war break point. The toing and froing of opinion over time, between the relative importance of epizoochory vs endozoochorey (both evidence-based and not), becomes very clear in the review”

Thank you, we are pleased you found this key point clear.

 

“A critical question emerges  – do seeds survive gut passage? Given the importance of this question, it struck me that simulated gut passage treatments (i.e. seed scarification, acidification, or both) are not mentioned in the paper. I would assume, in relation to contemporary studies, it might be relevant, although I understand that experimental methods are not a focus of this paper.”

We have now mentioned studies using such treatments in our new section entitled “State of the Art: modern understanding of epizoochory and endozoochory”.

 

“In addition, authors discuss multiple studies in which seeds recovered from bird faeces germinated better than control seeds. Authors might consider exploring the opinions of co-evolution of bird and plant species, and gut passage as a germination requirement/an important part of the seed germination strategy. I would assume this idea would support endozoochorey?”

We have now briefly discussed germination strategies and possible coevolution in our new section entitled “State of the Art: modern understanding of epizoochory and endozoochory”.

 

“May I also suggest that ‘waterbirds’ be defined early on (for us plant people), and that the ‘digestion myth’ (integral to the title, abstract and paper) be introduced earlier than line 230”.

Thank you – a good suggestion (reviewer 1 suggested something similar too). We have now done this.

 

“Congrats to authors on a great paper.”

Thank you very much.

Reviewer 3 Report

Comments and Suggestions for Authors

The findings have significant implications for understanding plant biogeography and ecosystem dynamics. Recognizing waterbirds as vectors for a wider range of plants, including those without fleshy fruits, expands our understanding of how plants colonize new areas and maintain genetic diversity. This perspective is particularly relevant in the context of climate change, where shifting migratory patterns could alter dispersal routes and impact plant distribution.

Future research should focus on quantifying the relative contributions of endozoochory and epizoochory in different ecosystems and among various bird species. It would also be beneficial to explore the physiological traits of seeds that enable them to survive gut passage, as this could inform conservation strategies and the management of invasive specie

Line 252 Figure 1 and ordinary conditions. Please explain it better or delete it.

Lines 311-313: what type of dormancy do these species have? (in general). Perhaps dispersal, endozoochory and epizoochory may just be casual, not the main dispersal syndrome - the type of dormancy should also be included to better understand coevolution processes.

Line 339: Please delete “(as we have above)”.

 

Line 352: “(the smallest of all angiosperms)”, please indicate dimension or references.

References included in the paper should be amended according with the journal rules. Please check here: https://mdpi-res.com/data/mdpi_references_guide_v9.pdf

 

Author Response

“The findings have significant implications for understanding plant biogeography and ecosystem dynamics. Recognizing waterbirds as vectors for a wider range of plants, including those without fleshy fruits, expands our understanding of how plants colonize new areas and maintain genetic diversity. This perspective is particularly relevant in the context of climate change, where shifting migratory patterns could alter dispersal routes and impact plant distribution.”

Thank you, we agree (especially on the climate change point).

 

“Future research should focus on quantifying the relative contributions of endozoochory and epizoochory in different ecosystems and among various bird species. It would also be beneficial to explore the physiological traits of seeds that enable them to survive gut passage, as this could inform conservation strategies and the management of invasive specie.”

These topics are now addressed in our modified final section “Conclusions and recommendations”.

 

“Line 252 Figure 1 and ordinary conditions. Please explain it better or delete it.”

This is a quotation from 19^th C. publication (see earlier in paragraph). As described a few lines above they appear to imply relatively few seeds by this. However as we make clear in our text ‘ordinary conditions’ were not specifically defined in the original publication. In other words, we cannot explain it in any more detail (but consider that this is too important to delete). However, we have reorganized the sentence to improve clarity.

 

“Lines 311-313: what type of dormancy do these species have? (in general). Perhaps dispersal, endozoochory and epizoochory may just be casual, not the main dispersal syndrome - the type of dormancy should also be included to better understand coevolution processes.”

Seed dormancy has only recently started to be discussed in these contexts (especially by van Leeuwen et al. 2023). It was not discussed in these very early 20^th C. papers which are describing at this point in the manuscript, so its not historically relevant at this point in the discussion. We have discussed seed dormancy in this context recently in Green et al (2023). We believe there is a limited amount to what we can say, because Darwin’s digestion myth and the related flawed dispersal syndrome paradigm have themselves discouraged research into the relationship between endozoochory and dormancy strategies in dry-fruited plants.

We are concerned that there may be a degree of circularity behind this suggestion. As far as we can see from the literature, dormancy strategies have been assigned without adequate consideration for the evidence of endozoochory for dry-fruited plants. To be clear, plants that are not assigned a “physical dormancy strategy” are assumed not to have coevolved with endozoochory, without considering any evidence to the contrary. Most plants dispersed by waterbirds are assigned a “physiological dormancy strategy”, yet there is plenty of evidence that they have adaptive responses to gut passage (see van Leeuwen et al. 2023).

 

“Line 339: Please delete “(as we have above)”.”

Deleted                                                                                     

 

 

“Line 352: “(the smallest of all angiosperms)”, please indicate dimension or references.”

Size added.

 

“References included in the paper should be amended according with the journal rules. Please check here: https://mdpi-res.com/data/mdpi_references_guide_v9.pdf”

We will amend references once the paper is provisionally accepted. Each time the references are changed within the text, renumbering creates a lot of work for us. For that reason we do not wish to do it now, and then have to change everything again later.

Round 2

Reviewer 2 Report

Comments and Suggestions for Authors

Thanks for addressing my comments. A great paper, congrats to authors. 

Reviewer 3 Report

Comments and Suggestions for Authors

Authors have adequately addressed the comments made by the reviewers in the revised version of the manuscript. Therefore, I have no further comments.