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Brief Report
Peer-Review Record

Estuary Stingray (Dasyatis fluviorum) Behaviour Does Not Change in Response to Drone Altitude

by Emily Bourke 1, Vincent Raoult 1,2,*, Jane E. Williamson 2 and Troy F. Gaston 1
Reviewer 1:
Reviewer 3: Anonymous
Submission received: 18 January 2023 / Revised: 9 February 2023 / Accepted: 20 February 2023 / Published: 27 February 2023
(This article belongs to the Topic Drones for Coastal and Coral Reef Environments)

Round 1

Reviewer 1 Report (Previous Reviewer 1)

I have re-read this paper and appreciate that the authors have considered my suggestions for revision. I think the quality is now adequate for publication

Author Response

We thank the reviewer for their response. No changes made.

Reviewer 2 Report (New Reviewer)

Review detail for authors

Abstract

Line 15: “While stingrays demonstrated a range of behaviours, these behaviours rarely changed during drone observations (n = 6 or 12% of flights)” It is not clear. Be more extended, can you clarify the results in the abstract?

Introduction

Line 25-26: You can add some studies in seabirds:

Rümmler, M.; Mustafa, O.; Maercker, J.; Peter, H.; Esefeld, J. Measuring the influence of unmanned aerial vehicles on Adélie penguins. Polar Biol. 2016, 39, 1329–1334.

Line 43-44: I recommend this paper to read and be cited. The information could be linked as well in lines 153-156, and 194-196 in the Discussion.

Frixione, M.G.; Salvadeo, C. Drones, Gulls and Urbanity: Interaction between New Technologies and Human Subsidized Species in Coastal Areas. Drones 20215(2), 30.

Line 56: I think the aim of the study is well presented and all the description about the importance of the study is precise, however before you present the goal of the study, the introduction should bring some information about the species in 3-4 lines. Distribution, reproduction, conservation status, they move in groups or lonely?, etc. This information help the lector to be in context, otherwise the lector get lost.

Methods

Study area: How about the water?, is marine water or it has some freshwater source?. Is this a large city or a small town (population?)? How about recreation activities? Boats, kayaks?

Line 97: Authors should describe briefly the Fettermann de Oliveira approach, the paper is quite short, the lector need more information about the methods.

Line 93: What speed did you fly the drone in descendant flight?

Figure 1: I consider the brownish color is not the best option. I cannot appreciate the sampling area in the picture. I would try to change this color or increase transparency or only mark borders with lines, because the picture has interesting information. Also, the figure of New South Wales in the corner should be improved. I would add the position in the Australia map instead NSW map or consider a map with Australia and colored the NSW state with a point in the study area, the journal is read around the world and not many people knows where is NSW.

Line 79: Add the weight (g) and the sound (dB)

Results

Results are very clear, try to be clear also in the abstract. However, when the authors say they still swimming…they could swim faster. If they do not detect any change on the speed they should say it. Also I think it should be included in Methods as part of the observed behaviors considered. I would change Figure 3, occurrence is detailed in Table 2, may be is better if you consider to change the Y axis by % of individuals evidencing behavior change.   

Discussion

Line 200: How about the noise and the acoustic sensory receptors of elasmobranchs? There is any difference with marine mammals? You can give some reflection on this subject

Line 203-204: Here is where I get lost…there is no information about ecology and breeding performance of the species. Was the sampling conducted during the breeding season? Can you recognize juveniles, how are them? How about the size of individuals?

Author Response

We thank the reviewer for their helpful feedback. We have made all the suggested changes, please see our detailed responses to comments highlighted in red below.

 

Abstract

Line 15: “While stingrays demonstrated a range of behaviours, these behaviours rarely changed during drone observations (n = 6 or 12% of flights)” It is not clear. Be more extended, can you clarify the results in the abstract?

 

Introduction

Line 25-26: You can add some studies in seabirds:

Rümmler, M.; Mustafa, O.; Maercker, J.; Peter, H.; Esefeld, J. Measuring the influence of unmanned aerial vehicles on Adélie penguins. Polar Biol. 2016, 39, 1329–1334.

We have added the recommended citation.

Line 43-44: I recommend this paper to read and be cited. The information could be linked as well in lines 153-156, and 194-196 in the Discussion.

Frixione, M.G.; Salvadeo, C. Drones, Gulls and Urbanity: Interaction between New Technologies and Human Subsidized Species in Coastal Areas. Drones 2021, 5(2), 30.

We have added the recommended citation.

Line 56: I think the aim of the study is well presented and all the description about the importance of the study is precise, however before you present the goal of the study, the introduction should bring some information about the species in 3-4 lines. Distribution, reproduction, conservation status, they move in groups or lonely?, etc. This information help the lector to be in context, otherwise the lector get lost.

We have added some information on the species lines 58 - 59 for context.

Methods

Study area: How about the water?, is marine water or it has some freshwater source?. Is this a large city or a small town (population?)? How about recreation activities? Boats, kayaks?

We have added details lines 72 - 78.

Line 97: Authors should describe briefly the Fettermann de Oliveira approach, the paper is quite short, the lector need more information about the methods.

We feel that the subsequent section provides sufficient detail (it would be very repetitive to highlight the Fettermann approach further). This statement was added to justify the approach we chose. No changes made.

Line 93: What speed did you fly the drone in descendant flight?

Typically 1m/s, comment added. See line 105.

Figure 1: I consider the brownish color is not the best option. I cannot appreciate the sampling area in the picture. I would try to change this color or increase transparency or only mark borders with lines, because the picture has interesting information. Also, the figure of New South Wales in the corner should be improved. I would add the position in the Australia map instead NSW map or consider a map with Australia and colored the NSW state with a point in the study area, the journal is read around the world and not many people knows where is NSW.

We have increased the transparency and increased the highlighting of the outline of the flight area. We have refrained from making other changes on the map, however, as Sydney is clearly indicated and most people would know its location.

Line 79: Add the weight (g) and the sound (dB)

We have added details about this drone model. See line 84.

Results

Results are very clear, try to be clear also in the abstract. However, when the authors say they still swimming…they could swim faster. If they do not detect any change on the speed they should say it. Also I think it should be included in Methods as part of the observed behaviors considered. I would change Figure 3, occurrence is detailed in Table 2, may be is better if you consider to change the Y axis by % of individuals evidencing behavior change.   

While we agree that including movement speed would be useful, it would be extremely complex to link video observation to behavioural variation as measured from the drone. Regarding the second point, it wouldn't change the figure significantly since 50 individuals were tracked (it would only change Y axis values). No change made.

Discussion

Line 200: How about the noise and the acoustic sensory receptors of elasmobranchs? There is any difference with marine mammals? You can give some reflection on this subject

This is a good point, very little is known about sight and hearing of elasmobranchs. We have added a section on this lines 206 - 212.

Line 203-204: Here is where I get lost…there is no information about ecology and breeding performance of the species. Was the sampling conducted during the breeding season? Can you recognize juveniles, how are them? How about the size of individuals?

Gravid females can be identified visually by the large 'humps' on their back, however these are difficult to identify from the drone NADIR video. Breeding doesn't really happen in a seasonal sense, but the females may be gravid for months before birth. There is very little information on the breeding parameters of this species, we have added some information on this lines 218 - 219.

Reviewer 3 Report (New Reviewer)

The presented study is not a complete study, is just the first step in the methodology to do a study on the abundance, distribution or behavior of fauna using drones as a work tool: to see that the device does not affect the behavior of the target species (eg. https://www.mdpi.com/2504-446X/4/4/64). In the following work (eg: https://www.mdpi.com/2072-4292/13/1/40), the same authors had already observed that drone flight height did not affect the behavior of stingrays; according to their methodology they descend to 5–25 m to track fine-scale movements of stingrays. In the present “study” the same authors say: "the data were used to identify the appropriate altitude that should be used for the remainder of the study"; so they should publish the complete work and not in stages. Besides, the target specie hardly reacts to the activity of these vehicles since: 1) it is benthic specie (it has no activity on the surface water), 2) it does not have aerial predators, and 3) it is not commercially fished. Therefore, the information generated would not be useful to evaluate the potential interaction of this species due to the increase in civil and commercial use of drones (eg. https://www.mdpi.com/2504-446X/5/2/30). And finally, the approximation is very simple, and does not consider other variables that could influence whether or not the stingray perceives the drone overhead: 1) time of day and the generation of shadows; and 2) the height of the tide (0.5m deep is not the same as 1.5m above stingray´s head, the tidal heights were obtained from the following page: https://tides.willyweather.com.au/nsw/central-coast/brisbane-waters--woy-woy-bridge.html)

Author Response

We thank the reviewer for their feedback. Please see our responses to their comments in red below.

"The presented study is not a complete study, is just the first step in the methodology to do a study on the abundance, distribution or behavior of fauna using drones as a work tool: to see that the device does not affect the behavior of the target species (eg. https://www.mdpi.com/2504-446X/4/4/64). In the following work (eg: https://www.mdpi.com/2072-4292/13/1/40), the same authors had already observed that drone flight height did not affect the behavior of stingrays; according to their methodology they descend to 5–25 m to track fine-scale movements of stingrays. In the present “study” the same authors say: "the data were used to identify the appropriate altitude that should be used for the remainder of the study"; so they should publish the complete work and not in stages. "

This study was conducted on its own, and is not part of a larger study. The work part of this team was involved in highlighted by the reviewer (https://www.mdpi.com/2072-4292/13/1/40) was conducted on a different and much larger species in a completely different estuary. What's more, the study in question didn't formally assess reactions to drones, rather the comment that the rays did not seem to react was purely subjective (which was a critique we received when publishing that paper, and largely led to this study). We have removed the typo referring to "the remainder of the study".

"Besides, the target specie hardly reacts to the activity of these vehicles since: 1) it is benthic specie (it has no activity on the surface water), 2) it does not have aerial predators, and 3) it is not commercially fished. Therefore, the information generated would not be useful to evaluate the potential interaction of this species due to the increase in civil and commercial use of drones (eg. https://www.mdpi.com/2504-446X/5/2/30). "

Respectfully, we disagree that knowing the animals' life history is sufficient to determine whether they are likely to react to drones. The best example of this is the research demonstrating that bears or kangaroos, who have absolutely no reason to be threatened by drones, show adverse reactions to their presence (https://www.mdpi.com/2504-446X/3/2/41; Ditmer M.A., Vincent J.B., Werden L.K., Tanner J.C., Laske T.G., et al. 2015. Bears show a physiological but limited behavioral response to unmanned aerial vehicles. Curr. Biol. 25(17): 2278–2283.; Jagielski, P.M., Barnas, A.F., Grant Gilchrist, H., Richardson, E.S., Love, O.P. and Semeniuk, C.A., 2022. The utility of drones for studying polar bear behaviour in the Canadian Arctic: opportunities and recommendations. Drone Systems and Applications10(1), pp.97-110.). In addition, there have been no studies trying to assess reaction of elasmobranchs to drones in a formal setting.

"The approximation is very simple, and does not consider other variables that could influence whether or not the stingray perceives the drone overhead: 1) time of day and the generation of shadows; and 2) the height of the tide (0.5m deep is not the same as 1.5m above stingray´s head, the tidal heights were obtained from the following page: https://tides.willyweather.com.au/nsw/central-coast/brisbane-waters--woy-woy-bridge.html)"

We specifically underline that those factors could affect results and should be examined, see lines 185 - 188. 

Round 2

Reviewer 3 Report (New Reviewer)

I saw the comments of the authors and I am really not convinced by their answers. It is an incomplete work since it does not consider the time of day or the height of the tide. In addition to the fact that it is a benthic species without behavior on the surface; and a bear and a kangaroo are not underwater and have more evolutionarily developed sensory systems to hear or see the device in the air.

This manuscript is a resubmission of an earlier submission. The following is a list of the peer review reports and author responses from that submission.


Round 1

Reviewer 1 Report

I read the paper with interest and I believe that your topic is useful to all researchers who are approaching the study of the behavior of elasmobranchs through the use of drones. However, I believe some integration is needed before it can be published.

Introduction and methodology are clear and exhaustive.

The results are a bit sparse. I would suggest to the authors to provide some more details, rather than figure 3 which alone is not very interesting. For example, show the differences observed between the various types of behavior: who was more or less influenced by the presence of the drone among the three behaviors investigated?

Also, a summary table of the data might be helpful, rather than listing all the observations reported in the supplementary materials.

In the rare episodes in which the drone caused behavior changes, what environmental conditions were there? The tide? The wind? the time of day? Providing this information may be helpful to the reader.

The discussion is well organised

 

Small changes following:

 

line 25: “Despite” instead of “Sespite”

 

line 60: “All flights were conducted in the waters to the east of Woy Woy”: I do not think that a drone can fly in water, so please rephrase that.

Author Response

Dear reviewer, thank you for your productive and positive comments that have significantly improved our manuscript. We have compiled your comments and our responses below. Our responses have been highlighted in red to make them easier to follow. To make the changes easier to see on the manuscript, we have also included a version of the manuscript with track changes:

I read the paper with interest and I believe that your topic is useful to all researchers who are approaching the study of the behavior of elasmobranchs through the use of drones. However, I believe some integration is needed before it can be published.

Introduction and methodology are clear and exhaustive.

We thank the reviewer for their positive feedback.

The results are a bit sparse. I would suggest to the authors to provide some more details, rather than figure 3 which alone is not very interesting. For example, show the differences observed between the various types of behavior: who was more or less influenced by the presence of the drone among the three behaviors investigated?

We agree with the reviewer that more detail could be included. As a result, we have added a summary table of results as suggested, and added detail on the patterns of response (there were only two rays whos behaviours changed during flights). Please see changes lines 130 - 138.

Also, a summary table of the data might be helpful, rather than listing all the observations reported in the supplementary materials.

Please refer to the above comment.

In the rare episodes in which the drone caused behavior changes, what environmental conditions were there? The tide? The wind? the time of day? Providing this information may be helpful to the reader.

We have provided this information in the discussion lines 185 - 189. Because all flights were in similar conditions, we don't think that they would be the cause of the observed changes.

The discussion is well organised

We thank the reviewer for their positive feedback.

Small changes following:

 

line 25: “Despite” instead of “Sespite”

Correction made.

line 60: “All flights were conducted in the waters to the east of Woy Woy”: I do not think that a drone can fly in water, so please rephrase that.

We have changed this to 'to the east of Woy Woy'

Reviewer 2 Report

The paper offers a method to study the behavior of marine animals using drones. The work is not well laid out based on a systematic protocol that develops a methodology. They do not have a clear methodology and only perform actions such as taking several videos at different scales or flight level. The methods of analysis are simple, and the problem statement is basic, they do not have a broad bibliographic support. The document revolves around a discussion of other experiences.

Advantages:

The paper could be interesting and relevant to the scope of the journal. But The researchers do not clearly express their rationale and do not clearly show methods and results.

 Disadvantages.

1. The paper has few bibliographic references which indicates that they did not investigate thoroughly, there are multiple experiences around the world with drones and wildlife works.

2. The statement that drones have little visible impact on the behavior of rays is something that would be almost obvious, being the marine environment one of the ecosystems where observation with drones is the least invasive. The flight heights of 5 meters are limited by the physical approach of the drone by its optical capacity, if they used a higher resolution camera and better optics could fly even higher, obtaining the same or better spatial resolution with less or no impact.

3. The materials and methods are not clear; they only mention tools and some techniques used.

4. There is a problem with the maps and graphs, the way of presenting the results is confusing.

5. The discussion is based on other experiences and not in discussing and analyzing their own study.

 

Problems:

A plagiarism analysis was performed with the turniting tool and a result of 40% was obtained with a report presented at the University of Newcastle, many of the texts come from this report which is presumed to be a degree work or university report.

In conclusion, the authors do not present something understandable and adequate to be published.

Author Response

Dear reviewer, thank you for your comments. We have compiled your comments and our responses below. Our responses have been highlighted in red to make them easier to follow. To make the changes easier to see on the manuscript, we have also included a version of the manuscript with track changes:

The paper offers a method to study the behavior of marine animals using drones. The work is not well laid out based on a systematic protocol that develops a methodology. They do not have a clear methodology and only perform actions such as taking several videos at different scales or flight level. The methods of analysis are simple, and the problem statement is basic, they do not have a broad bibliographic support. The document revolves around a discussion of other experiences.

Respectfully, we believe these comments are inappropriate on a professional level as well as being unhelpful. The reviewer does not provide any suggestions on what could be improved.

Advantages:

The paper could be interesting and relevant to the scope of the journal. But The researchers do not clearly express their rationale and do not clearly show methods and results.

We are pleased the reviewer finds that the reason for the study is valid, and highlight that reviewer #1 was very pleased with our rationale for the study. We have expanded on the introduction further to try and address this. We have also added additional details in the results as per helpful feedback from reviewer #1, but given the vagueness of reviewer #2's comments, we cannot action any changes.

 Disadvantages.

  1. The paper has few bibliographic references which indicates that they did not investigate thoroughly, there are multiple experiences around the world with drones and wildlife works.

As highlighted at the top of the document, this study is a short communication and therefore should not have large numbers of references, however, we have still added over 10 references to address this concern. Respectfully, we disagree with the second point, as there are no studies on behavioural responses to drones of elasmobranchs, as we highlight in paragraph lines 42 - 56.

  1. The statement that drones have little visible impact on the behavior of rays is something that would be almost obvious, being the marine environment one of the ecosystems where observation with drones is the least invasive. The flight heights of 5 meters are limited by the physical approach of the drone by its optical capacity, if they used a higher resolution camera and better optics could fly even higher, obtaining the same or better spatial resolution with less or no impact.

Respectfully, we disagree. There are numerous studies including Raoult et al. 2020 and others that highlight that responses of marine animals to drones vary and are hard to predict. We expand on this point specifically in the paragraph lines 42 - 56 in the introduction. Regarding the second point, we agree, this is why we have explicitly suggested this to reduce impacts lines 226-241.

  1. The materials and methods are not clear; they only mention tools and some techniques used.

We invite the reviewer to provide more helpful comments that can be actioned. We have specified the drone model, including specifications, flight patterns, the location of the flights, the experimental design, the analysis of video, and the statistical analysis. Please outline what aspect of the methods was unclear.

  1. There is a problem with the maps and graphs, the way of presenting the results is confusing.

We invite the reviewer to outline what is wrong with the graphs and the way results are presented. As per reviewer #1, we have added a table and some detail in the results to further outline the observed patterns.

  1. The discussion is based on other experiences and not in discussing and analyzing their own study.

Respectfully, every paragraph of the discussion relates the results from our own study in the context of the broader literature, which is what discussion sections should be about. For example, the first paragraph lines 143 - 170 highlights the lack of predictability about which animals will respond to drones, and that there are species/taxa specific traits. The second paragraph lines 171 - 191 outlines how flight characteristics or airframes could be the cause, and how that relates specifically to our population of rays that are constantly exposed to pelicans. We have also added a section here as per reviewer #1 on flight environment conditions. The paragraph lines 192 - 208 outlines how biological factors of our population, like being gravid, could explain our patterns. Paragraph 209 - 225 highlights how our study is visual only, and the caveats (along with other studies) on what that could mean. Finally paragraph line 226 - 241 outlines recommendations on research on rays using drones given the results of our study.

Problems:

A plagiarism analysis was performed with the turniting tool and a result of 40% was obtained with a report presented at the University of Newcastle, many of the texts come from this report which is presumed to be a degree work or university report.

The University of Newcastle report in question is that of the first author of this study, Emily Bourke, and it therefore expected that there are some similarities given the source data are the same. It's commonplace to use theses (Honours, Masters or PhD) as a basis for publication in a peer-reviewed journal.

In conclusion, the authors do not present something understandable and adequate to be published.

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