PCOMPBIOL-D-26-00652

Dynamic vibration-driven feedback shapes predator–prey interactions in orb-weaving spiders

PLOS Computational Biology

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PLOS Computational Biology

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At this stage, the following Authors/Authors require contributions: Hsin-Yi Hung, Abel Corver, and Andrew G Gordus. Please ensure that the full contributions of each author are acknowledged in the "Add/Edit/Remove Authors" section of our submission form.

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Reviewers' comments:

Reviewer's Responses to Questions

Reviewer #1: Dynamic vibration-driven feedback shapes predator-prey interactions in orb-weaving spiders

General Comments:

This is a very sophisticated and thorough documentation, using a highly quantitative approach, of the details of the vibratory dialogue between a predator (an orb weaving spider) and a prey (fruit flies).

- I am not very familiar with this journal and thus cannot discuss its suitability, but this is a very solid study worthy of publication.

- Demonstrating that the spiders are using their web as a 2-way communication platform to manipulate prey behavior to their sensory advantage is not a trivial feat, yet these authors accomplish this with rigorous and convincing data.

- The methods used in this study – e.g., using pixel intensity changes to explore vibration transmission – are very novel and will be of interest to a broad range of scientists.

- The data collection and analyses are very sophisticated and likely to be copied by future researchers, ensuring high citations for this paper.

- Despite the somewhat non-traditional (at least in communication/animal behavior studies) methodological approach, the paper is written in a very understandable fashion, making it highly accessible.

- Overall, the idea that spiders can actively modulate their web to manipulate prey behavior and thus make prey more detectable is a very cool one!

Specific Comments

- I would not generalize the title to all orb-weaving spiders but instead say in “AN orb-weaving spider”. While it is likely that this is a general phenomenon of many web-building spiders, it has only been shown in your species so far.

- Abstract, page 2, line 31 – is there a word missing after “increased”?

- Page 15, line 17 – should it be “spiderS exhibit”?

- The sample size is not very large for a behavioral study and it might be good to ensure that readers can have confidence in your low sample size (e.g., page 18, line 81; 12 recordings).

- Page 32, line 89 – you should spell out the genus name if it starts a sentence or is a heading

Reviewer #2: Hung et al., investigate how U. diversus spiders use web-borne vibrations to guide prey capture behavior. The primary focus in on whether the spider actively modulates its own movements to enhance the detectability of prey-generated signals. The authors use high-speed video recordings to measure vibration, machine-learning-based pose estimation method for tracking the spider’s body posture, and unsupervised behavioral state modeling.

The results show that prey-generated signals from Drosophila are concentrated in the 2-50 Hz range and that species differences arise primarily from vibratory power rather than spectral composition. Moreover, the results discuss three discrete behavioral states and show that these states follow structured transition dynamics during prey capture. Additionally, the results reveal a reciprocal feedback loop between predator and prey. Spider crouching and shaking precede increases in fly-generated vibratory power. Lastly, the results show that spider orientation toward prey is predicted by the radial thread carrying the highest vibratory amplitude. The experiments are logical and the data presented in well-crafted visuals. As such, this work is appropriate for publication. I outline some concerns that are intended to improve the comprehension and follow-up on these impressive efforts.

Major Points

0. Are three Principal Components really justified based on the eigenvalues? Fig 2A6 and Fig 2D seem quite continuous.

1. The authors measure the “pure fly signal” at the fly's location, then use this as the sensory input to the spider GLM. However, the spider is moving (and transitioning between the three states), and its position on the web is not fixed. If the spider systematically moves closer to the fly during or after crouching, then the increased pure fly signal power observed in subsequent static states could reflect reduced propagation distance. Did the authors verify that fly-spider distance did not systematically vary across behavioral states? And if so, that this does not affect the results?

2. Similarly, does the fly location vary across recordings? Would the fly location have an effect on the results? The web is not a uniform transmission medium (as the paper's own AUC maps show). The fly's position on the web determines which thread segments it directly loads. The spectral content of the signal received at the spider depends not only on the fly's biology (melanogaster vs virilis), but on the mechanical properties of the local thread geometry at the catch site. The authors performed a whole-web FFT averaging, which is a partial mitigation, but the authors should report the catch location, and provide an analysis on whether location variations would affect the results.

3. Can the authors provide a hypothesis to why differences in web-borne signals between the two Drosophila species arise primarily from vibratory intensity rather than frequency composition?

4. The authors normalize the pixel intensity to get “pure” fly (line 323), however, it is unclear how these normalizations were performed. The authors should provide an explicit formulation in the Methods section.

5. The paper specifies a window of 400 samples for the STFT. Why 400 samples was chosen for the window?

Minor Points

Line 184: The equation is redundant here as it is a repeat of equation 7 in the Methods section. Suggestion: refer on page 9 to equation 7 in the Methods.

Line 187: Remove: “it is worth noting that”

Line 207-208: It is unclear how Fig 1F shows the statement in this line. Did the authors intend to refer to a different figure.

Line 213: The sentence starting with “To confirm that the …” can be a new paragraph.

Line 226: The concluding findings stated in this paragraph heavily relies on results presented in Fig S2, particularly H-J. For clarity, it might be worth considering moving these figures into the main manuscript as panels for Fig 1.

Line 238: Use “Three” instead of “3”

Line 268: The acronyms throughout the manuscript are not consistent. Multiple acronyms are being defined more than once. Sometimes a term is written as its acronym and others it is fully spelled out. In this line, HMM (268 and 274) is just an example, but this is also present with ROI, FFT, and BTA.

Line 430: Presenting equations 2, 3, 4, and 5 in the main text rather than in the Methods does not add to clarity. Instead, the text feels fragmented. I suggest that the authors move these equations to the Methods section.

Line 447: Moreover, equations embedded in text should be treated as text. As such, punctuations should be included. This also applies to the equations in the Methods section.

Line 627: Authors use i and j interchangeably to denote sqrt(-1).

Line 632: Use FFT instead of y. Add information from page 9.

Line 632: The SNR definition presented in equations 1 and 7 is not traditional and differs from the common definition. The authors should provide a citation for this definition or use an alternative name.

Fig 3D: Authors should change the color of one of the green graphs as it is hard to distinguish between the two visually.

Fig 3E: This figure belongs to supplementary more than the main manuscript. Additionally, the authors should include a legend for the three behavioral states

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Have the authors made all data and (if applicable) computational code underlying the findings in their manuscript fully available?

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Reviewer #1: Yes

Reviewer #2: None

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Reviewer #1: No

Reviewer #2: No

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Figure resubmission:

Reproducibility:

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Dear Dr. Gordus,

We are pleased to inform you that your manuscript 'Dynamic vibration-driven feedback shapes predator–prey interactions in an orb-weaving spider.' has been provisionally accepted for publication in PLOS Computational Biology.

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Thank you again for supporting Open Access publishing; we are looking forward to publishing your work in PLOS Computational Biology.

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Matthieu Louis

Academic Editor

PLOS Computational Biology

Marieke van Vugt

Section Editor

PLOS Computational Biology

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Reviewer's Responses to Questions

Comments to the Authors:

Please note here if the review is uploaded as an attachment.

Reviewer #1: The authors did an excellent job addressing all of the reviewer's concerns.

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Have the authors made all data and (if applicable) computational code underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data and code underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data and code should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data or code —e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

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Reviewer #1: No