Temporal and spatial dynamics in soil acoustics and their relation to soil animal diversity

Marcus Maeder; Xianda Guo; Felix Neff; Doris Schneider Mathis; Martin M. Gossner

doi:10.1371/journal.pone.0263618

Peer Review History

Original SubmissionOctober 6, 2021
1 Dec 2021 Decision Letter - Haru Matsumoto, Editor PONE-D-21-32125Temporal and spatial dynamics in soil acoustics and their relation to soil animal diversity.PLOS ONE Dear Dr. Maeder, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Jan 15 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. 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This paper could be a key paper that many future publications would refer to. Having said that I have the same concern with reviewer 2. It is a little stretch to claim that their research is the first one to relate the biodiversity of the soil to soundscape. Both reviewers did a good job suggesting critical references. Please consider including a faunal data set as reviewer 2 suggested which I believe improves the quality of the paper. Overall it is very good paper. Please resubmit with revisions. [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Yes Reviewer #2: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes ****** 3. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data 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 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—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes Reviewer #2: No ****** 4. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes ****** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: The authors conducted acoustic surveys over two years at a Swiss forest site used for irrigation experiments. Samplings of soil biodiversity and microclimatic conditions were performed alongside. The overall aim of the study was to test the hypothesis if soil meso- and macrofauna diversity and composition can be predicted by the complexity of soil soundscapes in both space and time. The study was part of the research project “Sounding soil” of which I have been keen to see scientific results published. Soil acoustic methods have the potential to be a very helpful tool in urgently needed soil biodiversity monitoring, but the available research is quite scarce so far and mainly focused on pest insects. Thus, this manuscript is very timely and it offers very interesting insights into several methodological and ecological aspects of soil acoustic studies. I have some major comments regarding the manuscript, but I hope to see it published soon as it is a very good addition to the currently available soil acoustic literature. Major comments I see a bias in the reference list. For me it looks like the authors came from a perspective of acoustics in aboveground ecology and then transferred this perspective to the soil. I am missing references to some relevant soil acoustic studies which someone would cite coming from a belowground perspective (see minor comments for examples). The discussion has some repetition in the first part (lines 448 – 480). Lines 459 – 463 would actually be a better start sentence for the entire discussion and then the first three paragraphs could be merged and restructured. You write a lot about the relationship between ACI and microclimatic conditions. It sounds kind of general, like you did it for the entire study period, but you only modeled it for 35 days. Do you think, you would have gotten another result if you modeled it for example for April 2019? Minor comments Line 80: Reference 16 doesn’t really refer to the acoustic detection of soil pests. Referencing one of the papers from Mankin et al. or “Zhang et al. (2003): Acoustic estimation of infestations and population densities of white grubs (Coleoptera: Scarabaeidae) in turfgrass.” would be more fitting here. Line 82 – 84: I would see the paper of “Mankin et al. (2007): Acoustic Indicators for Mapping Infestation Probabilities of Soil Invertebrates” as already one of the papers going into the direction of acoustically surveying soil animal biodiversity on spatial and temporal scales, although they didn’t target the entire soil fauna. Lines 117 – 118: Would you still stand by this after looking at, for example, Mankin et al. (2007) and “Inyang et al. (2019): Subterranean Acoustic Activity Patterns of Vitacea polistiformis (Lepidoptera: Sesiidae) in Relation to Abiotic and Biotic Factors”? Lines 142 – 149: This paragraph would fit better in the introduction. Line 162: Which soil depth did they cover? Line 166: Just to make sure I understand it correctly: You recorded the soundscape every 10 minutes for 10 seconds? Why are there 20 seconds in Fig. 2? Check if all products have a complete reference, e.g. line 176: PlantCare Miniloggers (PlantCare AG, Russikon, Switzerland). (What sensor length did you get for the Miniloggers? ST?) Line 209: What does ‘selectively’ mean here? Did you just randomly pick out audio recordings or was there still any kind of selection criteria involved? Line 243: Why does this reduce the influence of the distance between microphones? Line 249: Is there a reference for Pieretti’s method? What did your own function contribute to calculating the ACI which was not already included in the function acoustic complexity? Line 294: Which version of ‘rstan’? It is not in the reference list. Line 303: Why this specific interval of 35 days for the analysis? Line 362 ff.: What uncertainty measures are shown in the brackets? Looking at Fig. 3, the 95 % is missing as information in the text. Lines 492f.: “Different taxa most likely produce different sounds…” Do you think different taxa could not only be producers of sound, but also passively affect sound properties in the same way as soil particles do (sound dispersion and attenuation)? See also line 509. Lines 494 – 496: Really? Don’t quite get the argument here. Line 499: Did you also have experience with strong wind effects on audio recordings? Line 520: Possible reference for sound identification: Görres & Chesmore (2019): Active sound production of scarab beetle larvae opens up new possibilities for species-specific pest monitoring in soils Line 522: You don’t really discuss the limitations of your study. Lines 623-625: Remove highlighting. Between reference 54 and 55, there is one more reference. Reviewer #2: Ths is an original study in soil biodiversity, showing for the first time that soil acoustic diversity is strongly correlated with diversity and species composition of soil fauna. Even though it would have been better to sample more accurately macroinvertebrates (e.g. on a wider surface), I think that we have serious reasons to think that macroinvertebrates were scarcely represented in these dry Scots pine forest stands, but providing soil fauna data would have allowed the reader to better evaluate the quality of faunal sampling. Thus faunal data are required before final acceptance. Another (minor) concern is with the assessment (lines 82-83) that "To our knowledge, there have been no attempts to analyze soil soundscapes across temporal and spatial scales and to relate them to soil animal biodiversity". This not entirely true. Many assays have been done to investigate soil biodiversity by acoustic methods, even if these methods were less sophisticated. Among others, please refer to: https://www.nature.com/articles/s41598-018-28582-9 https://www.mdpi.com/2571-8789/3/3/45 ****** 6. 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If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0263618.r001
Revision 1
14 Jan 2022 Author Response Response to reviewers Answers Reviewer #1 I see a bias in the reference list. For me it looks like the authors came from a perspective of acoustics in aboveground ecology and then transferred this perspective to the soil. I am missing references to some relevant soil acoustic studies which someone would cite coming from a belowground perspective (see minor comments for examples). - Many thanks for the reference to the additional literature. We included most of your reference suggestions (see below). The discussion has some repetition in the first part (lines 448 – 480). Lines 459 – 463 would actually be a better start sentence for the entire discussion and then the first three paragraphs could be merged and restructured. You write a lot about the relationship between ACI and microclimatic conditions. It sounds kind of general, like you did it for the entire study period, but you only modeled it for 35 days. Do you think, you would have gotten another result if you modeled it for example for April 2019? - We are grateful for this comment as it shows that we were not clear enough in our line of arguments. In the first paragraph of the discussion we focus on seasonal and diurnal patterns and in the second we discuss the relations of ACI to microclimate. To make this clearer we now refer to the second paragraph when mentioning microclimate in the first paragraph (new manuscript line 433). - It is true that we have only modelled the relationship between ACI and microclimate for a period of 35 days in 2019. However, we have done this deliberately. We selected the time period of highest activity because we expected the clearest relationships in this period, based on our data from 2018. As we discovered in 2018 that microclimate is likely an important factor influencing the soil soundscapes at our study site, we started our microclimate measurements in 2019. We added this information in the methods. It now reads (new manuscript lines 178-179): “This time period was chosen because we expected highest activity of soil fauna during this period based on data from 2018.“ We are quite confident that we would have found the same but weaker relationships in periods of lower activity. Line 80: Reference 16 doesn’t really refer to the acoustic detection of soil pests. Referencing one of the papers from Mankin et al. or “Zhang et al. (2003): Acoustic estimation of infestations and population densities of white grubs (Coleoptera: Scarabaeidae) in turfgrass.” would be more fitting here. - Thank you for this helpful suggestion, we replaced the reference with the reference of Zhang et al. (2003). Line 82 – 84: I would see the paper of “Mankin et al. (2007): Acoustic Indicators for Mapping Infestation Probabilities of Soil Invertebrates” as already one of the papers going into the direction of acoustically surveying soil animal biodiversity on spatial and temporal scales, although they didn’t target the entire soil fauna. - We revised the sentence to make the novelty of our approach clearer. The sentence now reads (new manuscript , lines 89-92): “In addition, there have been no attempts to analyze soil soundscapes across temporal and spatial scales and to relate them to soil animal biodiversity, although the potential of such research has already been pointed out [18] and first studies on individual soil animal species support this (see references 34/35).” Lines 117 – 118: Would you still stand by this after looking at, for example, Mankin et al. (2007) and “Inyang et al. (2019): Subterranean Acoustic Activity Patterns of Vitacea polistiformis (Lepidoptera: Sesiidae) in Relation to Abiotic and Biotic Factors”? - We are aware that such relationships have been studied for individual species, but to our knowledge not studied for meso- and macrofauna at the community level. To make this clearer, we rephrased the sentence (new manuscript, lines 125-129): “There have been first attempts to relate subterranean acoustic activity patterns of individual species to abiotic and biotic factors [34] [35] . However, to our knowledge, the present study is the first to investigate the spatial and temporal dynamics of sounds produced by soil mesofauna and macrofauna at the community level and to relate them to abiotic/microclimatic parameters.” Lines 142 – 149: This paragraph would fit better in the introduction. - We agree and integrated this in the Introduction (new manuscript, lines 70-80). Line 162: Which soil depth did they cover? - Approx. 10 cm, now noted in the text (new manuscript, line 165): “…covering a soil depth of approx. 10 cm and a volume of approx. 1000 cm3.” Line 166: Just to make sure I understand it correctly: You recorded the soundscape every 10 minutes for 10 seconds? Why are there 20 seconds in Fig. 2? - Thank you for noting this, this was actually an error in the text, we recorded for 20s. The text has been changed accordingly (new manuscript, line 169). Check if all products have a complete reference, e.g. line 176: PlantCare Miniloggers (PlantCare AG, Russikon, Switzerland). (What sensor length did you get for the Miniloggers? ST?) - Thank you for pointing this out. We now referenced the products correctly (new manuscript, lines 177-180). Line 209: What does ‘selectively’ mean here? Did you just randomly pick out audio recordings or was there still any kind of selection criteria involved? - We selected the audio files randomly. We now clarify this (new manuscript, lines 208- 210): “This was done by listening to randomly selected audio recordings of different times of days, months and seasons.” Line 243: Why does this reduce the influence of the distance between microphones? We think that this is a misunderstanding. The method reduces the influence of the distance between the microphone and the recorded organism (if very close, sum(I) is very large and ACI is reduced accordingly). We have changed the text slightly to make this clearer (new manuscript, lines 244-245). Line 249: Is there a reference for Pieretti’s method? What did your own function contribute to calculating the ACI which was not already included in the function acoustic complexity? - We apologize for not citing the method of Pieretti. The reference is is now added to the manuscript (new manuscript, line 249). We closely followed this method and just adapted it to our data. Line 294: Which version of ‘rstan’? It is not in the reference list. - The reference including version number was now added to the reference list. Line 303: Why this specific interval of 35 days for the analysis? - Microclimatic variables were only assessed during the growing season 2019 because we discovered in 2018 that microclimate might be an important factor influencing soundscapes at the study site. The period of expected highest activity of soil fauna was chosen. We clarify this in the revised text (new manuscript, lines 301-303). Line 362 ff.: What uncertainty measures are shown in the brackets? Looking at Fig. 3, the 95 % is missing as information in the text. - Thank you for pointing this out. These are 95% highest density intervals, the information has been added to the text (new manuscript, line 362). Lines 492f.: “Different taxa most likely produce different sounds…” Do you think different taxa could not only be producers of sound, but also passively affect sound properties in the same way as soil particles do (sound dispersion and attenuation)? See also line 509. - No, we don’t think that this is the case since the soil faunal biomass makes a very small physical part of the soil matrix, maybe with the exception of a mass occurrence of soil pest species or an ant nest nearby the acoustic sensors for example. However, this was neglectable in our case. Lines 494 – 496: Really? Don’t quite get the argument here. - We analyzed the taxa diversity based on different q-levels. With increasing q-levels from 0 (taxa richness) to 1 (taxa Shannon diversity) to 2 (taxa Simpson diversity) dominant taxa are more strongly weighted. As q=0 showed the strongest relationship with ACI the rare taxa seem to contribute to this relationship substantially. We made this clearer in the discussion by rephrasing this part (new manuscript, lines 471-474): “As among the different q-levels, q=0 (taxa richness) showed the strongest relationship with ACI, rare taxa seem to contribute to the relationship with ACI substantially. Our findings thus suggest that the acoustic complexity also accurately captured the rare taxa in the community, indicating its value for conservation-oriented monitoring programs.” Line 499: Did you also have experience with strong wind effects on audio recordings? - Yes, wind also affected audio recordings (see Supporting Information S5f Fig), but did not affect our main finding. Strong wind events occurred rarely and were statistically not significant. Line 520: Possible reference for sound identification: Görres & Chesmore (2019): Active sound production of scarab beetle larvae opens up new possibilities for species-specific pest monitoring in soils. - Thank you for this useful reference, it has been integrated in the text (revised document, line 550). Line 522: You don’t really discuss the limitations of your study. - Here we disagree with the reviewer. The limitations of our study are discussed in line 476-492. Lines 623-625: Remove highlighting. - This has been done. Between reference 54 and 55, there is one more reference. - Thank you for pointing us on this. It’s a redundant reference which has been removed. Answers Reviever #2 This is an original study in soil biodiversity, showing for the first time that soil acoustic diversity is strongly correlated with diversity and species composition of soil fauna. Even though it would have been better to sample more accurately macroinvertebrates (e.g. on a wider surface), I think that we have serious reasons to think that macroinvertebrates were scarcely represented in these dry Scots pine forest stands, but providing soil fauna data would have allowed the reader to better evaluate the quality of faunal sampling. Thus faunal data are required before final acceptance. - We appreciate the general positive evaluation of our manuscript. Regarding the faunal data requested by the reviewer we are not completely sure what is meant. We provided a table in the Supporting Information (Table S2. Sampled taxa and total number of individuals per taxon) were we show the taxonomic level on which we identified soil fauna and in addition give the total abundance of all taxa. Another (minor) concern is with the assessment (lines 82-83) that "To our knowledge, there have been no attempts to analyze soil soundscapes across temporal and spatial scales and to relate them to soil animal biodiversity". This not entirely true. Many assays have been done to investigate soil biodiversity by acoustic methods, even if these methods were less sophisticated. - Based on the comments of reviewer 1 we added a few references of studies that addressed the relationship of soil acoustics and single species (see response to comments of reviewer 1). However, we for the first time address the relationship of soil soundscapes and soil biodiversity at the community level. We made this clearer in our new manuscript (lines 87-93). - Regarding your specific suggestions: Among others, please refer to: https://www.nature.com/articles/s41598-018-28582-9 - Also in this paper the authors do not address soil biodiversity at the community level, but focus on earthworms exclusively. We added this paper to our introduction (new manuscript, line 87). https://www.mdpi.com/2571-8789/3/3/45 - We already cited this paper (line 84 in the original version, line 91 in the new manuscript). This is however rather a perspectives paper than based on an empirical study. Attachments Attachment Submitted filename: Response_to_Reviewers.docx https://doi.org/10.1371/journal.pone.0263618.r002
24 Jan 2022 Decision Letter - Haru Matsumoto, Editor Temporal and spatial dynamics in soil acoustics and their relation to soil animal diversity PONE-D-21-32125R1 Dear Dr. Maeder, We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. Kind regards, Haru Matsumoto Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0263618.r003
Formally Accepted
31 Jan 2022 Acceptance Letter - Haru Matsumoto, Editor PONE-D-21-32125R1 Temporal and spatial dynamics in soil acoustics and their relation to soil animal diversity Dear Dr. Maeder: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org. If we can help with anything else, please email us at plosone@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Haru Matsumoto Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0263618.r004

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