Microclimatic conditions and water content fluctuations experienced by epiphytic bryophytes in an Amazonian rain forest

Löbs, Nina; Walter, David; Barbosa, Cybelli G. G.; Brill, Sebastian; Alves, Rodrigo P.; Cerqueira, Gabriela R.; de Oliveira Sá, Marta; de Araújo, Alessandro C.; de Oliveira, Leonardo R.; Ditas, Florian; Moran-Zuloaga, Daniel; Pires Florentino, Ana Paula; Wolff, Stefan; Godoi, Ricardo H. M.; Kesselmeier, Jürgen; Mota de Oliveira, Sylvia; Andreae, Meinrat O.; Pöhlker, Christopher; Weber, Bettina

doi:https://doi.org/10.5194/bg-17-5399-2020

Articles | Volume 17, issue 21

https://doi.org/10.5194/bg-17-5399-2020

© Author(s) 2020. This work is distributed under
the Creative Commons Attribution 4.0 License.

https://doi.org/10.5194/bg-17-5399-2020

© Author(s) 2020. This work is distributed under
the Creative Commons Attribution 4.0 License.

Articles | Volume 17, issue 21

Research article

|

11 Nov 2020

Research article |

| 11 Nov 2020

Microclimatic conditions and water content fluctuations experienced by epiphytic bryophytes in an Amazonian rain forest

Nina Löbs, David Walter, Cybelli G. G. Barbosa, Sebastian Brill, Rodrigo P. Alves, Gabriela R. Cerqueira, Marta de Oliveira Sá, Alessandro C. de Araújo, Leonardo R. de Oliveira, Florian Ditas, Daniel Moran-Zuloaga, Ana Paula Pires Florentino, Stefan Wolff, Ricardo H. M. Godoi, Jürgen Kesselmeier, Sylvia Mota de Oliveira, Meinrat O. Andreae, Christopher Pöhlker, and Bettina Weber

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Final revised paper (published on 11 Nov 2020)
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Preprint (discussion started on 22 Jan 2019)
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Interactive discussion

Status: closed

AC: Author comment | RC: Referee comment | SC: Short comment | EC: Editor comment

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AC1: 'Correction of figures', Nina Löbs, 23 Jan 2019
RC1: 'Review of first version', Maaike Bader, 10 Feb 2019
- AC2: 'Answer to the review and description of changes', Nina Löbs, 12 Jun 2019
RC2: 'Review of bg-2018-521', Anonymous Referee #2, 15 Feb 2019
- AC3: 'Answer to the review and description of changes', Nina Löbs, 12 Jun 2019
RC3: 'Additional consideration', Maaike Bader, 19 Feb 2019
- AC4: 'Answer to the review and description of changes', Nina Löbs, 12 Jun 2019
RC4: 'Review for Löbs et al BGSCS', Anonymous Referee #3, 25 Feb 2019
- AC5: 'Answer to the review and description of changes', Nina Löbs, 12 Jun 2019

Peer-review completion

AR: Author's response | RR: Referee report | ED: Editor decision

ED: Reconsider after major revisions (30 Jul 2019) by Michael Bahn

AR by Nina Löbs on behalf of the Authors (14 Oct 2019) Author's response Manuscript

ED: Referee Nomination & Report Request started (21 Oct 2019) by Michael Bahn

RR by Maaike Bader (07 Nov 2019)

RR by Anonymous Referee #3 (12 Nov 2019)

Suggestions for revision or reasons for rejection

Dear Editor and authors

I have checked the rebuttal provided by Löbs et al. regarding the manuscript “Microclimatic conditions and water content fluctuations experienced by epiphytic bryophytes in an Amazonian rain forest” submitted to Biogeosciences.

My general opinion after reading the explanations provided and changes made is that authors are losing a very nice chance for publishing a top reference paper regarding bryophytes functional performance in tropical regions. Authors state that moving samples to the lab for gas exchange experiments could damage the physiological performance due to the exposition to dryness necessary for samples packing and transportation. This could be true for samples used to be always wet in the field, but I bet that many others not following these patterns could show values close to maximum after an adequate revitalization period under controlled conditions in the lab similar to those occurring in the field. I wonder if there is any paper or papers available with tropical bryophythes being measured in the lab in order to help in the methodological approach to solve this potential problem. Anyway, a solution to this can be to perform gas exchange experiments in the field. If authors are going to do this in the future extensively, a first approach could be done in this paper just to doublecheck predictions made. Even accepting that gas exchange is a next step in this research line and has no place in this first manuscript, I think that at least some chlorophyll a fluorescence measurements could have been done during some representative climatic conditions in order to have a rough idea about what happens in relation with WC and microclimate when real metabolic activity is being considered. This is not difficult to get and improves the manuscript substantially because it provides some reference points to metabolic activity assumptions. This extra measurementes would be neccesary only if extrapolation to functional performance are between the objectives of the research, the paper stands by itself with the microclimatic approach due to the novelty of the data.

As it is now, this research provides new and useful microclimatic data for tropical epiphytic cryptogamic covers, but extrapolations to functional performance with current data are very risky and should be kept to minimum and always highlighting clearly the caution linked to those assumptions. My point of view is not to block the publication of the manuscript because there are no similar data sets available in the literature. I really expect to see published a second part with real functional measurements that could close this interesting initiative despite of thinking that both objectives could be accomplished in one manuscript

I would like to mention some points that are still unclear to me :

- In the rebuttal letter, authors mention that “This indeed is planned for the future, but would go beyond the scope of the current study. For the present study, we found some very good data on lowland rain forest bryophytes, assessed by a group, which is well-experienced in CO2 gas exchange measurements. Thus, for the current study we decided to use their results in order to assess potential physiological activity patterns, but we also stress the potential sources of error and inaccuracy of this approach” This sounds to a likely alternative to real measurements but please state much more clearly in the text which are the sources of this information, which species were used at those papers (Lösch et at 1994 and Wagner et al. 2013), which accurate environmental conditions and habitats were the species used by those authors facing….In summary, all the functional part of the manuscript relies on this few measurements made by the authors mentioned, so I would give more emphasis to this fact in the introduction and, especially, in the final part of the discussion (the info is included partially in the results section, but I think that more details are neccesary)

- If I have understood ok, authors have removed the statistical analyses provided in the first version of the manuscript. If this is correct, I would like to know why has this been done and implications of this over the interpretation of the data sets

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ED: Reconsider after major revisions (25 Nov 2019) by Michael Bahn

AR by Nina Löbs on behalf of the Authors (01 Feb 2020) Author's response Manuscript

ED: Reconsider after major revisions (05 Feb 2020) by Michael Bahn

ED: Referee Nomination & Report Request started (05 Feb 2020) by Michael Bahn

RR by Anonymous Referee #3 (13 Feb 2020)

RR by Maaike Bader (25 Mar 2020)

Suggestions for revision or reasons for rejection

Dear authors,

In the new revised version a lot of the issues in the previous one have been addressed. I still think that the water-content data for the bryophytes are a unique and interesting data set. My main concern remains however, but I hope it can still be solved:

The impossibly high water contents of the air-dry liverworts in the canopy are still presented, and although the strangeness of the values is discussed (not convincingly), the values are not discarded or further corrected. I really think that data about the course of the water content of tropical bryophytes is very valuable and needs to be published, but these values must clearly be wrong, so they should NOT be presented as they are. Figure S5 gives a hint about what the cause of the strange values may be: Due to the unexplained short-term fluctuations, the water content, and thus apparently the electrical conductivity (EC) values, for the samples at 23m vary a lot around the half-hour mean. If we assume that the half-hour mean is the most realistic real EC value and that the short-term variations are noise, it is not a good idea to take the 5-minutes-based minimum and maximum (even not using a 1 or 5%, 95% or 99% or whatever percentile) values for the calibration, because that way the noise is going to determine the calculated water contents. I hope I made the problem clear.

Another possible problem is that the very high WCmax of Symbiezidium that you determined in your calibration measuerments (which does NOT mean that they would have a WC of 400% when air dry!) does cause a high calculated WC if a linear relationship between EC and WC is assumed, which is not realistic for the very high WCs. So here, you might need to start the linear part of the calibration curve at a lower WC.

I do not know if it will be possible to get a value for the water content that is reliable in absolute terms. Perhaps your best bet is to not even try and to only report on the fluctuations, i.e. wetting after rain (which I consider a clear and undisputed signal) and daily fluctuations at 23 m (which in my mind may reflect the equilibration with fluctuating air humidity, already indicating that it cannot be true that the WC is around 400, because at that value they would be wetter than in equilibrium with moist air. Information about such fluctuations is already interesting as a first bit of data, as it shows e.g. how long mosses stay wet after a rain. Because of the lack of replication and different positions of the bryophytes on the trunk it is indeed hard to attribute these patterns to the height on the tree, but even without that, it gives an indication of the patterns that are possible in rain forest epiphytes. In summary: either correct the values based on a new calibration (which should of course still be consistent and rational and not just a fine-tuning to get the desired result), or present the WC fluctuations without quantifying the absolute values.

You can really emphasize harder that the type of data you present is unique. Microclimate has been measured in vertical profiles in rain forests before, but data on the temperature and water content fluctuations inside mosses, which are very relevant for estimating or modelling their productivity, have never been measured for so long or along a height profile, as far as I know. In the last paragraph of the introduction, make clearer why these data are exciting. In the discussion (par 4.1) make clearer what the previous studies did and did not measure.

Another major point is that the presentation of the estimated potential physiological activity (Par 3.2 and 4.2) needs some reformulation in the sense that the compensation points should be consequently presented as rough proposals, not as values that you know to be valid for your environment or species. So try to use formulations like “If we assume a WCP of X (REF), the duration of activity would be Y”. Adjust in the caption of Fig 4 too. Also, 4.2. is quite long considering how little data you have to really be able to discuss this.

Some smaller remarks:

P2 L24-27 These introductory sentences are not really necessary.

P3 L15 a paragraph break is needed here. L15-17 are not necessary.

P5 L23 Expressing the oscillations in terms of WC would assume that the WC is correctly determined. Better express it as EC, and take it into consideration when calculating WC (see above)

P6 L10 what is this conversion factor base on?

P6 L15-25 This section does not yet describe the calibration. This is described on P7 L1-14

P7 L15 Explain the origin of the oscillations and take them into account for determining the WC

P7 L18-19 Huge error bars suggest that this averaging may not be justified. Can you argue that it is? How are different species at one height a uniform group?

P13 L13-16 You could use these results to your advantage by pointing out how they show the larger small-scale variation in environmental conditions du to shading and tree topography, which may cause conditions to be more variable within centimetres than the ´microclimate´ along the larger height gradient along the tree.

P15 L12 After reinstallation, without recalibration, these values are no longer usable, I would just not present them.

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ED: Reconsider after major revisions (06 Apr 2020) by Michael Bahn

AR by Nina Löbs on behalf of the Authors (08 Jun 2020) Author's response Manuscript

ED: Referee Nomination & Report Request started (08 Jul 2020) by Michael Bahn

RR by Maaike Bader (04 Aug 2020)

Suggestions for revision or reasons for rejection

(Line numbers based on the author response version with tracked changes: bg-2018-521-author_response-version3.pdf)

Dear authors,

Thank you for once again reviewing your manuscript and for seriously and effectively addressing my concerns. I think that you have now solved the main problem in the previous versions, the plausibility of the water content values. I think that the calibration method and the orders of magnitude of the results now make sense, and I am really pleased about this. Of course it still does not imply that they necessarily present the correct absolute values, but together with the other microclimatic data they do show nicely how the dynamics of the water contents in these bryophytes may respond to environmental conditions. I think this is an important contribution of this paper.

Now that the main issue is solved, I think the manuscript just needs one more round of polishing, highlighting and discussing the exciting findings more, correcting some mistakes, optimising some graphs and formulations and checking for style and grammar.

The WC values now look more plausible to me and in the examples shown (Figs 2 and S6) they show a wonderful reaction to rain events. Could you corroborate this impression by a correlation between the WC and the rain amount in the preceding 12 h (or something like that)? It is interesting that the WC of the samples as 23 m sometimes do (especially on 10-09-2016) and sometimes do not at all (March 2015) react to rain. Apart from possible umbrella effects of the canopy, could it also be due to a reinstallation and recalibration of the sensors around June 2015? There seems to be a large and systematic difference between the EC (and WC) values before and after this maintenance period for the sensors at 1.5 m (Fig S5). I guess this may be partly due to the drier season after this period, but I am not convinced that this explains the pattern completely. It may be worth elaborating a bit on this point.

The diel fluctuations (mentioned P17, L1) in WC are not mentioned clearly enough in the results. They can be seen a little bit in Fig S8 and better in S5c, but the former figure is referred to only in the context of condensation and the latter not at all in results or discussion. I think these daily fluctuations deserve more attention (especially as you use it as a main conclusion), so I would discuss them with reference to figure S5c, or add another figure similar to Fig S8 but showing more days (only on days without much rain so that the scale of the WC can be precise enough to show the fluctuations - these are hard to see in Fig 2 and S6). I like Figure S9, but it does not show whether reaching the dew point is related to the fluctuations in the WC. An interesting analysis would be to calculate a correlation between the distance below the dew point reached and the response in WC on that morning. The same could be done for the fog events. The difference in daily fluctuations between the seasons (mentioned in the conclusions) is also interesting and worth some more discussion (P15 L2-3: is this phenomenon more frequent in the dry season?). In fact, I think this point could perhaps make for an additional publication by itself!

I think Figure S5 is useful, but I recommend making the graphs larger. In the supplement I do not think that there is the need to save space, so I would go for clarity here. I also like the magnification shown in S5c, though judging from the rain amounts it does not really correspond to the box in the coarse-scale graph, which I would recommend stretching vertically to make clear that the entire graph (all parameters) are shown in the magnification.

The way in which stemflow is discussed could be improved. In my view, this is not ´additional´ water in the sense that moisture input from condensation may be (so I would not merge these two points into one sentence like you now do, P16 L 30), but it is redistributed rain water (mostly, as condensation and fog would hardly lead to stemflow) that benefits epiphytes on the tree stem (i.e. in your case those at 1.5 m in particular). As stemflow concentrates rainfall from a larger area to the stem, this could explain why the bryophytes on the stem respond so reliably to rainfall. For a recent review about this see Mendieta-Leiva, G., P. Porada and M.Y. Bader, 2020. Interactions of epiphytes with precipitation partitioning. In: Precipitation partitioning by vegetation. A global synthesis, J. T. Van Stan IIE. Gutmann and J. Friesen, (Eds.). Springer Nature Switzerland: pp: 133-145.

And I think I found one important mistake in your calculation of activity times, or possibly two (sorry I did not notice this in the previous round):

1. You assume that “For the net photosynthesis (NP) it is required that … T > TCP”. However, the TCP is an upper limit, so for a positive NP you need T to be below this compensation point!

2. The range for Topt can be considered a range within (not above or below!) which NP is optimal. Therefore I would expect only one value for the % of time where the bryophytes at a particular height in the tree are within this range, not a range of %. This is in contrast to the other ranges which are ranges of estimates for which we do not know which applies so that indeed it is useful to report on the estimated % of time if we assume one or the other value.

Small typos / grammar problems (not exhaustively reviewed) and needs for short clarifications:

P3 L31 …communities were conducted …

P4 L25: add the tree species and some information about tis phenology (it seems from the discussion that it is a semideciduous tree..?). This is quite relevant for extrapolating the results.

P5 L12: 26-m-high

P5 29: data that could be used…

P5 L33: The electrical conductivity (EC) values on which the WC calculations were based (see Paragraph 2.3 below) showed some unexplained oscillation, causing …

P6 L9: please explain this ´fluctuated´

P7 L17: I would add here that 0% was an approximation (simplification), as no moss would really reach 0% unless in a good drying oven… But they would dry to a minimum WC of a few %, so near enough to 0% for this model assumption.

P8 L24: Please start this point by explaining why you calculated this (to estimate the likelihood of water input by dew?). It also would not hurt to introduce this idea in the introduction. I think it is a very important and exciting point!

P9 L7: Fig S5 does not show PAR values…

P13 L8: remove in before 90%

P13 L10: relatively similar or similarly high

P16 L7: those at 23 m

P16 L23 remove the second ´during the dry season´

P17 L8: we observed (instead of ´observed by us´)

P17 L14-16: stating that Leucobryum may have a low water retention seems strange, as this genus has special water-retaining cells… I would think that it is not particularly good at capturing water (e.g. from fog), but then very good at retaining it.

P17: I would consider removing L5-32, as it does not really add much to your story. The life-from discussion seems too much discussion for the amount of data you have per life form and does not sound like you have profoundly researched it yet. Similarly, with the number of samples you studied it seems unjustified to draw any conclusions about the pattern of distributions among height zones. You could mention this in the methods section where you present the species studied, to justify your choice by showing that you chose typical species for the ecosystem.

P22 L 1: I would not say that the WC has “turned out to be” the key parameter controlling the overall physiological activity of the organisms, because you did not measure this activity. Better use a more cautious formulation like “appears to be”

P22 L3 remove the comma after major rain events

P22 L8: here also remove the speculative remark about thallus morphology. This is, by the way, not a seasonal feature anyway…

P22 L13-14: do you really know whether this nightly condensation activates physiological processes? Is it enough for photosynthesis, for example? I do not think that we know this, and I do think it would be very important to know it, so perhaps formulate it as a research need rather than a finding.

Table 1b: please help the reader by providing the number of days for which the fog sensor was operational (in addition to the sensor outage times)

Table 3: please make clearer what data were used: the averages of the different samples per height zone? Or the individual samples (i.e. is the range shown a function only of the range of possible parameter values for the cardinal points, or also a function of the differences between samples?).

Fig 4 caption: I do not think that the ´Estimated´ is appropriate here.

Figure S8 caption: Exemplary

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ED: Publish subject to minor revisions (review by editor) (04 Aug 2020) by Michael Bahn

AR by Nina Löbs on behalf of the Authors (28 Aug 2020) Author's response Manuscript

ED: Publish as is (10 Sep 2020) by Michael Bahn

AR by Nina Löbs on behalf of the Authors (16 Sep 2020)

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Short summary

Cryptogamic organisms, such as bryophytes, lichens, and algae, cover major parts of vegetation in the Amazonian rain forest, but their relevance in biosphere–atmosphere exchange, climate processes, and nutrient cycling is largely unknown. Over the duration of 2 years we measured their water content, temperature, and light conditions to get better insights into their physiological activity patterns and thus their potential impact on local, regional, and even global biogeochemical processes.