Complexity and diversity of motion amplification and control strategies in motile carnivorous plant traps

Similar to animals, plants have evolved mechanisms for elastic energy storage and release to power and control rapid motion, yet both groups have been largely studied in isolation. This is exacerbated by the lack of consistent terminology and conceptual frameworks describing elastically powered motion in both groups. Iconic examples of fast movements can be found in carnivorous plants, which have become important models to study biomechanics, developmental processes, evolution and ecology. Trapping structures and processes vary considerably between different carnivorous plant groups. Using snap traps, suction traps and springboard-pitfall traps as examples, we illustrate how traps mix and match various mechanisms to power, trigger and actuate motions that contribute to prey capture, retention and digestion. We highlight a fundamental trade-off between energetic investment and movement control and discuss it in a functional-ecological context.


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It is a condition of publication that authors make their supporting data, code and materials available -either as supplementary material or hosted in an external repository. Please rate, if applicable, the supporting data on the following criteria.

Do you have any ethical concerns with this paper? No
Comments to the Author Carnivorous plants have been associated inherently with rapid movements of their traps for long time. Besides this, there are also commonly slow movements of traps of carnivorous plants. The literature has usually termed the traps "active" and "passive" as based on the expenditure of metabolic energy to substantiate/drive the (rapid) movements, although all traps do function with the expenditure of metabolic energy (and also organic and mineral nutrients) not only for casual movement, but also for the trap construction, maintenance, enzyme secretion and nutrient absorption. As a result of this, the terms "active" and "passive" lose their sense both generally and also in the context of trap movements. The team of experienced authors, working significantly and successfully in the field of mobile traps, has tried to critically review and discuss the topics of activity and mobility of traps and has suggested to abandon the previously accepted subdivision of carnivorous plant traps into active and passive. I want to add that all primary literature data concerning CP traps have been published (at least a few years ago) and are not quite novel. Yet I consider the present paper as original as it thoroughly explains the interrelationships between trap motility and activity. In this respect, this well-arranged review is very useful and beneficial for the readers not only dealt with carnivorous plants or rapid plant movements. The three typical examples of rapid trap movements selected document the dominant majority of rapid movements in CPs. I have found only a few minor mistakes or typos to be corrected. They are listed below (page/line): p.5, l.95: one prey animal?: maybe better: one animal prey; p.5, l.117: "The traps of both species can snap repeatedly and re-open actively by growth" . Is this really so for Aldrovanda, too? I have thought that the re-opening in this species is a turgor-based process. See also p.27, l. 588. p.10, l.231-232: Carnivorous plants exclusively colonize sun-exposed, permanently wet habitats…. : I suppose that the word "exclusively" is not true as there are several dozens of CP species growing typically in shade. I suggest to write instead: mainly or usually or dominantly or prevailingly. Within this paragraph, the authors could also mention that terrestrial CPs grow relatively slowly, which reduces their needs for energy [17].

Comments to the Author
This is a generally well-written, interesting, and informative manuscript concerning the diversity of motile carnivorous plant traps. The authors use three diverse but well-studied examples to argue that the energetic cost of movement and resetting of traps varies dramatically, and therefore that use of the terms "motile" and "nonmotile" would be more accurate than "active" and "passive." Although the major thesis of the manuscript is clear, the argument is sometimes confusing. This is because the authors themselves employ the terms "active" and "passive" repeatedly in describing the movement in the three examples that they use (see, for example, lines78-80). It seems that they use these terms in reference to energy expenditure (lines 63-66). However, it would be helpful if they explicitly defined their use of the terms "active" and "passive" as "energy-requiring" or "energetically cost free." Even better, in my opinion, would be to avoid use of the terms "active" and "passive" completely while making the argument that these terms are misleading. They could instead use "energy-consuming" or "non-energy-consuming." Because of these issues, it seems that the authors aren't really arguing against the use of the terms "active" and "passive," but instead the recognition of the distinction between "active" and "motile".
There are a few minor typographical and/or editorial errors that need attention: Line 30: I assume that "divers" should be "diverse." Lines 73-74: The clause at the end of this sentence ("yet vary considerably in their investment in active processes proceeding such motion") doesn't make sense. Should "proceeding" be changed to "preceding"?

04-Jun-2020
Dear Mr Poppinga: I am writing to inform you that your manuscript RSPB-2020-0515 entitled "Functional and mechanical diversity of motile carnivorous plants, or why we should stop talking of 'active' versus 'passive' traps" has, in its current form, been rejected for publication in Proceedings B.
This action has been taken on the advice of referees, who have recommended that substantial revisions are necessary. With this in mind we would be happy to consider a resubmission, provided the comments of the referees are fully addressed. However please note that this is not a provisional acceptance.
The resubmission will be treated as a new manuscript. However, we will approach the same reviewers if they are available and it is deemed appropriate to do so by the Editor. Please note that resubmissions must be submitted within six months of the date of this email. In exceptional circumstances, extensions may be possible if agreed with the Editorial Office. Manuscripts submitted after this date will be automatically rejected.
Please find below the comments made by the referees, not including confidential reports to the Editor, which I hope you will find useful. If you do choose to resubmit your manuscript, please upload the following: 1) A 'response to referees' document including details of how you have responded to the comments, and the adjustments you have made. 2) A clean copy of the manuscript and one with 'tracked changes' indicating your 'response to referees' comments document.
3) Line numbers in your main document.
To upload a resubmitted manuscript, log into http://mc.manuscriptcentral.com/prsb and enter your Author Centre, where you will find your manuscript title listed under "Manuscripts with Decisions." Under "Actions," click on "Create a Resubmission." Please be sure to indicate in your cover letter that it is a resubmission, and supply the previous reference number.
A concern is that the review does not have broad enough appeal for Proc B's general readership. Terminological changes can be truly helpful, especially to specialists, but the undertone of the reviews is that something more is needed for this review to excite a broad audience. It is important that one or more reviewers is won over if you choose to resubmit, or we may have to make the undesirable decision of rejection. Nonetheless this is an intriguing topic and we hope that it can fit Proc B.
Sincerely, John R Hutchinson, Editor mailto: proceedingsb@royalsociety.org Associate Editor Reviewer(s)' Comments to Author: Referee: 1 Comments to the Author(s) Carnivorous plants have been associated inherently with rapid movements of their traps for long time. Besides this, there are also commonly slow movements of traps of carnivorous plants. The literature has usually termed the traps "active" and "passive" as based on the expenditure of metabolic energy to substantiate/drive the (rapid) movements, although all traps do function with the expenditure of metabolic energy (and also organic and mineral nutrients) not only for casual movement, but also for the trap construction, maintenance, enzyme secretion and nutrient absorption. As a result of this, the terms "active" and "passive" lose their sense both generally and also in the context of trap movements. The team of experienced authors, working significantly and successfully in the field of mobile traps, has tried to critically review and discuss the topics of activity and mobility of traps and has suggested to abandon the previously accepted subdivision of carnivorous plant traps into active and passive. I want to add that all primary literature data concerning CP traps have been published (at least a few years ago) and are not quite novel. Yet I consider the present paper as original as it thoroughly explains the interrelationships between trap motility and activity. In this respect, this well-arranged review is very useful and beneficial for the readers not only dealt with carnivorous plants or rapid plant movements. The three typical examples of rapid trap movements selected document the dominant majority of rapid movements in CPs. I have found only a few minor mistakes or typos to be corrected. They are listed below (page/line): p.5, l.95: one prey animal?: maybe better: one animal prey; p.5, l.117: "The traps of both species can snap repeatedly and re-open actively by growth" . Is this really so for Aldrovanda, too? I have thought that the re-opening in this species is a turgor-based process. See also p.27, l. 588. p.10, l.231-232: Carnivorous plants exclusively colonize sun-exposed, permanently wet habitats…. : I suppose that the word "exclusively" is not true as there are several dozens of CP species growing typically in shade. I suggest to write instead: mainly or usually or dominantly or prevailingly. Within this paragraph, the authors could also mention that terrestrial CPs grow relatively slowly, which reduces their needs for energy [17]. References: some journal names are abbreviated, some are not. Is it OK? To be united?
The photos properly document the text of the paper. However, Table 1S has not been available to me.
In conclusion, the paper is an interesting contribution to the knowledge of carnivorous plant biophysics and physiology, but addresses a broader readership and should be published after a minor revision, mostly formal.

Referee: 2
Comments to the Author(s) This manuscript was enjoyable to read and presents some proposed terminological changes to how trapping types are defined in carnivorous plants. It is well-written and with few grammatical or other errors ('divers' on L30 was the only obvious error). The rationale for changing terminology is sound and sufficiently justified. However, I am not sure that the content, potential authorship, or novelty of the theory presented meet the journal's requirement for reviews to be of "outstanding scientific importance and broad general interest". Certainly plant physiologists study carnivorous plants will find the review of interest, and the proposed terminology will likely be adopted within the carnivorous plant literature, but I am not sure I can see a significantly broader potential readership (e.g., population ecology, evolutionary ecology, botany) than this. I note the author's comments in the introduction that consistent terminology is important, and I certainly see the value in what is being proposed, but I feel it may be more suited to a journal publishing shorter reviews of this nature such as Biology Letters.

Referee: 3
Comments to the Author(s) This is a generally well-written, interesting, and informative manuscript concerning the diversity of motile carnivorous plant traps. The authors use three diverse but well-studied examples to argue that the energetic cost of movement and resetting of traps varies dramatically, and therefore that use of the terms "motile" and "nonmotile" would be more accurate than "active" and "passive." Although the major thesis of the manuscript is clear, the argument is sometimes confusing. This is because the authors themselves employ the terms "active" and "passive" repeatedly in describing the movement in the three examples that they use (see, for example, lines78-80). It seems that they use these terms in reference to energy expenditure (lines 63-66). However, it would be helpful if they explicitly defined their use of the terms "active" and "passive" as "energy-requiring" or "energetically cost free." Even better, in my opinion, would be to avoid use of the terms "active" and "passive" completely while making the argument that these terms are misleading. They could instead use "energy-consuming" or "non-energy-consuming." Because of these issues, it seems that the authors aren't really arguing against the use of the terms "active" and "passive," but instead the recognition of the distinction between "active" and "motile".
There are a few minor typographical and/or editorial errors that need attention: Line 30: I assume that "divers" should be "diverse." Lines 73-74: The clause at the end of this sentence ("yet vary considerably in their investment in active processes proceeding such motion") doesn't make sense. Should "proceeding" be changed to "preceding"?

Scientific importance: Is the manuscript an original and important contribution to its field? Excellent
General interest: Is the paper of sufficient general interest? Acceptable Quality of the paper: Is the overall quality of the paper suitable? Excellent Is the length of the paper justified? Yes

Do you have any concerns about statistical analyses in this paper? If so, please specify them explicitly in your report. No
It is a condition of publication that authors make their supporting data, code and materials available -either as supplementary material or hosted in an external repository. Please rate, if applicable, the supporting data on the following criteria.

Do you have any ethical concerns with this paper? No
Comments to the Author In this review paper, experienced authors deal with rapid movements of traps of carnivorous plants from a biohysical and functional point of view. They are focused on snap traps, suction traps and springboard-pitfall traps all exhibiting remarkable rapid movements. They distinguish three aspects of what has previously been named in the terms 'active' and 'passive' movement: (1) motion, (2) the conversion of metabolic energy into movement, (3) and the relative timing of energy conversion and motion. Although much has been written on rapid movements of traps of carnivorous plants, such an approach seems to be novel and promising for future research in this field. I have found that this well-arranged paper is perfectly written and reads well, underlining substantial features and aspects and omitting details. Moreover, the English is perfect and well understandable. Thus, I have found only a few minor mistakes/typos to be corrected or commented (page/line): p.7., l.130: "by"? should be probably: "be"; p.11, l. 226-241: Here, the authors have forgotten to state one crucial trait of Utricularia traps: spontaneous firing without any extrinsic stimulus, only when the negative pressure inside the bladder reaches the "critical" pressure value and the trapdoor cannot resist this pressure anymore. It is evident that this spontaneous firing is i) universal in aquatic Utricularia species and ii) has some ecological importance to gain suspended particles (e.g., nanoplankton) from the ambient water instead of prey. However, it this case, the triggering is entirely intrinsically powered. Thus, the authors should include this aspect of these traps into the text here.
p.15, l.319: "physiology"? Sensu stricto, physiology is a scientific branch. The authors might want to say rather: "physiological processes". In conclusion, the paper needs only a very minor revision.

26-Apr-2021
Dear Mr Poppinga I am pleased to inform you that your manuscript RSPB-2021-0771 entitled "Complexity and diversity of motion amplification and control strategies in motile carnivorous plant traps" has been accepted for publication in Proceedings B. Congratulations!! The referee(s) have recommended publication, but also suggest some minor revisions to your manuscript. Therefore, I invite you to respond to the referee(s)' comments and revise your manuscript. Because the schedule for publication is very tight, it is a condition of publication that you submit the revised version of your manuscript within 7 days. If you do not think you will be able to meet this date please let us know.
The reviewer has made some helpful final suggestions regarding wording and other presentational issues that all seem easy to implement.
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Sincerely, Prof. John R. Hutchinson, Editor mailto: proceedingsb@royalsociety.org Reviewer(s)' Comments to Author: Comments to the Author(s) In this review paper, experienced authors deal with rapid movements of traps of carnivorous plants from a biohysical and functional point of view. They are focused on snap traps, suction traps and springboard-pitfall traps all exhibiting remarkable rapid movements. They distinguish three aspects of what has previously been named in the terms 'active' and 'passive' movement: (1) motion, (2) the conversion of metabolic energy into movement, (3) and the relative timing of energy conversion and motion. Although much has been written on rapid movements of traps of carnivorous plants, such an approach seems to be novel and promising for future research in this field. I have found that this well-arranged paper is perfectly written and reads well, underlining substantial features and aspects and omitting details. Moreover, the English is perfect and well understandable. Thus, I have found only a few minor mistakes/typos to be corrected or commented (page/line): p.7., l.130: "by"? should be probably: "be"; p.11, l. 226-241: Here, the authors have forgotten to state one crucial trait of Utricularia traps: spontaneous firing without any extrinsic stimulus, only when the negative pressure inside the bladder reaches the "critical" pressure value and the trapdoor cannot resist this pressure anymore. It is evident that this spontaneous firing is i) universal in aquatic Utricularia species and ii) has some ecological importance to gain suspended particles (e.g., nanoplankton) from the ambient water instead of prey. However, it this case, the triggering is entirely intrinsically powered. Thus, the authors should include this aspect of these traps into the text here.

30-Apr-2021
Dear Mr Poppinga I am pleased to inform you that your manuscript entitled "Complexity and diversity of motion amplification and control strategies in motile carnivorous plant traps" has been accepted for publication in Proceedings B.
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Reply to editor and reviewers
Manuscript ID RSPB-2020-0515 Associate Editor: (1) A concern is that the review does not have broad enough appeal for Proc B's general readership. Terminological changes can be truly helpful, especially to specialists, but the undertone of the reviews is that something more is needed for this review to excite a broad audience. It is important that one or more reviewers is won over if you choose to resubmit, or we may have to make the undesirable decision of rejection. Nonetheless this is an intriguing topic and we hope that it can fit Proc B.
Reply: We agree with the editor's concern. To make the manuscript relevant to a broad readership, we expanded the scope of the manuscript substantially by changing the main narrative and conclusions of the manuscript. The manuscript places carnivorous plants into the framework of latch-mediated springs to explain the complexities and wide range of designs of their traps. So the change in terminology is now a recommendation coming forth from this framework. In the process of implementing this new narrative, we rewrote substantial portions of the manuscript.

Referee: 1
Carnivorous plants have been associated inherently with rapid movements of their traps for long time. Besides this, there are also commonly slow movements of traps of carnivorous plants. The literature has usually termed the traps "active" and "passive" as based on the expenditure of metabolic energy to substantiate/drive the (rapid) movements, although all traps do function with the expenditure of metabolic energy (and also organic and mineral nutrients) not only for casual movement, but also for the trap construction, maintenance, enzyme secretion and nutrient absorption. As a result of this, the terms "active" and "passive" lose their sense both generally and also in the context of trap movements. The team of experienced authors, working significantly and successfully in the field of mobile traps, has tried to critically review and discuss the topics of activity and mobility of traps and has suggested to abandon the previously accepted subdivision of carnivorous plant traps into active and passive. I want to add that all primary literature data concerning CP traps have been published (at least a few years ago) and are not quite novel. Yet I consider the present paper as original as it thoroughly explains the interrelationships between trap motility and activity. In this respect, this well-arranged review is very useful and beneficial for the readers not only dealt with carnivorous plants or rapid plant movements. The three typical examples of rapid trap movements selected document the dominant majority of rapid movements in CPs. I have found only a few minor mistakes or typos to be corrected. They are listed below (page/line): p.5, l.95: one prey animal?: maybe better: one animal prey.

Reply:
The relevant sentence and section have been rewritten entirely during the revision. p.5, l.117: "The traps of both species can snap repeatedly and re-open actively by growth" . Is this really so for Aldrovanda, too? I have thought that the re-opening in this species is a turgor-based process. See also p.27, l. 588.

Reply:
The revised manuscript states "The traps of both species can snap repeatedly, and re-open by means of energy-requiring growth processes [57, 63]", which is in fact the same statement. It is true that Aldrovanda also re-open by growth (reference 57: Ashida et al., 1934).