Sounds of Soil: A New World of Interactions under Our Feet?

Round 1

Reviewer 1 Report

This short opinion piece proposes to investigate a so far untapped dimension of the soil ecosystem. Indeed, vibrations have not been explored as mode of sensing the surrounding environment by soil biota, reacting to its changes or communicating between individual organisms. As the authors point out, several methodological challenges have to be overcome, including development of novel sensors and recording devices, especially field devices for in situ investigations. In my opinion one of the biggest challenge might be isolating signals from a noisy background. If producing vibrations and reacting to them is a general feature, in the diverse soil environment the signals will also be diverse. Moreover, even in environments far from human disturbance, vibrations are always produced from above: thunder, wildlife, falling trees, etc. As pointed out by the authors, other interfering (physical) processes also exists, all these producing a noisy background. However, we will not know what to find until we explore; in that sense the idea is interesting and worthy of publication.

Listed below are a few minor comments and suggestions:

L26 Information: ‘i’ should be in lower case

L45 - 48 “There is plenty of evidence that ….” This statement would be more convincing with more than just one example on earthworms producing sounds. Here is one that you may not be aware of: the terrestrial isopod Armadillio officinalis has been known to both producing sound (in the audible range) and react to vibrations. Even though this species in not typically endogeic, many isopods are. Check out the following two papers for more details.  The reference list of the first paper will give you more examples on this subject.     

Cividini S, Montesanto G (2018) Changes in turn alternation pattern in response to substrate-borne vibrations in terrestrial isopods. Behavioural Processes 146: 27–33. doi:10.1016/j.beproc.2017.11.005

Cividini S, Montesanto G (2018) Aggregative behavior and intraspecific communication mediated by substrate-borne vibrations in terrestrial arthropods: An exploratory study in two species of woodlice. Behavioural Processes. doi:10.1016/j.beproc.2018.07.006

L102 Again, an example from isopods, which are known to respond to vibration and other environmental stimuli to altering their locomotory behavior:

Houghtaling K, Kight SL (2006) Turn alternation in response to substrate vibration by terrestrial isopods, Porcellio laevis (Isopoda: Oniscidea) from rural and urban habitats in New Jersey, USA. Entomological News 117 (2): 149–154.

Author Response

1) Thanks for these positive comments.

2) information lower case, fixed.

3) Thanks for your suggestions for papers on isopods. We have added the suggested information and reference, for Cividini & Montesanto, eve though it is not a strictly soil-inhabiting animal.

Reviewer 2 Report

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The opinion paper of Rillig et al. discusses an interesting and novel perspective in soil sciences: using the sound of soil to better study soil biodiversity. I found that the paper original and overall well written, but a bit superficial in its current form. I believe that the manuscript can be improved and provide here minor comments that I hope will be of help:

The authors particularly insist on how sound could be interpreted by microbial (and to a lesser extent mesofauna) communities as a communication signal to anticipate potential events occurring in their environment (e.g. predation risk, sources of nutrients). As disentangling sound having effects on vs. being a response of the soil biota is likely to be extremely challenging - as the author state - I see two potential ways of dealing with this issue and expand the scope a bit: Acoustic vibrations can induce modifications in soil organisms through biophysical constraints per se, e.g. modify cell membrane permeability, with potential implications for the organism’s fitness, as shown in microbes (Sarvaiya & Kothari 2015, Murphy et al. 2016) or plants (Jung et al. 2018). These modifications do not necessarily involve a communication signal, they could also be seen as a direct abiotic controlling factor (such as e.g. soil pH or nutrient availability, but as a mechanical constraint) or an indirect one, through modification of other chemical/physical parameters. The authors discuss this aspect very briefly in their section 4, but I believe that this part could be more general and expanded: e.g. how sound per se can select or be detrimental to certain organisms, or how much do we know about the sensitivity of organisms (and particularly soil ones) to vibrations? and then, what could be the impact on the soil biota diversity and its associated functions, the anthropogenic vibrations being one particular case of such issues.

Somehow related to the above, I found that the overall paper was unclear about how soil sound could inform us on the state of soil biodiversity, soil functioning or health, e.g. typically for bio monitoring purposes. Current section 3 is quite superficial on this, and the authors may consider expanding the discussion by better presenting how sound is currently used in other systems (e.g. Farina et al. 2019, Gibb et al. 2019,  for reviews). An interesting aspect that would deserve to be mentioned is that - provided we are able to disentangle biological from physical/antropogenic vibrations - this very signal is energy, and may perhaps could be used as a proxy to inform on the soil ecological network activity, structure, and on ecosystem functioning.

On the potential of using sound as a pest control agent (which is somehow related to the discussion above), I’m surprise that the authors did not considered the work being conducted in medical sciences, where acoustic vibrations are seen as a promising tool to limit biofilm formations (e.g. reviewed in Sadekuzzaman et al 2015).

References:

Farina, A. (2019). Ecoacoustics: A Quantitative Approach to Investigate the Ecological Role of Environmental Sounds. Mathematics, 7(1), 21.

Gibb, R., Browning, E., Glover‐Kapfer, P., & Jones, K. E. (2019). Emerging opportunities and challenges for passive acoustics in ecological assessment and monitoring. Methods in Ecology and Evolution, 10(2), 169-185.

Jung, J., Kim, S. K., Kim, J. Y., Jeong, M. J., & Ryu, C. M. (2018). Beyond chemical triggers: evidence for sound-evoked physiological reactions in plants. Frontiers in plant science, 9, 25.

Murphy, M. F., Edwards, T., Hobbs, G., Shepherd, J., & Bezombes, F. (2016). Acoustic vibration can enhance bacterial biofilm formation. Journal of bioscience and bioengineering, 122(6), 765-770.

Sadekuzzaman, M., Yang, S., Mizan, M. F. R., & Ha, S. D. (2015). Current and recent advanced strategies for combating biofilms. Comprehensive Reviews in Food Science and Food Safety, 14(4), 491-509.

Sarvaiya, N., & Kothari, V. (2015). Effect of audible sound in form of music on microbial growth and production of certain important metabolites. Microbiology, 84(2), 227-235.

Author Response

1) Thanks for the supportive comments about the manuscript.

2) Sound as a biophysical constraint rather than communication. Thanks for this comment. We believe our use of the word 'information' in the manuscript already covers these sort of cases the reviewer mentions, i.e. sound as another abiotic parameter. However, we did like the paper (Murphy et al.) the reviewer suggests for biofilm formation, and have added this piece of information and the respective reference to the manuscript in section 2.

3) Sound and state of biodiversity. Thanks for this comment. We agree that more references could have been used in this section. We have added the references he reviewer suggested (Farina et al. 2019, Gibb et al. 2019).

4) Biocontrol. Thanks for this suggestion. Thanks for this comment, however, we do not believe that the case of medical control of biofilms translates to soil, since what this paper the reviewer mentions talks about is ultrasound.