Review of InteractionFrostDroughtPCIFWS_v3

General comments

I am overall very satisfied with the significant revisions to the manuscript. I have no major suggestions, but have offered many instances below where the wording could be corrected or clarified. All my suggestions are very minor, and I have offered alternative text in all cases, to make it easier for the authors. I think the document reads well and that the structure has been much improved. Also, please note that my editing suggestions have been made from the “InteractionFrostDroughtPCIFWSv2finalapp_changes.pdf” document, not the “...v3.pdf” doc (my line numbers won’t patch the v3.pdf doc). I would like to thank the editors and handlers at PCI and the authors for giving me another opportunity to learn from their interesting research.

Kind regards,

Sean M. Gleason

Specific comments

Please note that these suggestions are from the “...changes.pdf” document, not the “...v3.pdf” document.

89: I would suggest using the transition “However” OR “On the other had”, but not stringing both together.

165: “...both constraints…” [plural]

176: “...pit membranes” [plural]. Though I might suggest “bordered pit membranes” or just “bordered pits” might be a bit more accurate.

177: Given the current disagreement among research groups on this issue (refilling) I might suggest, “However, it is likely…” or However, it is possible…” to acknowledge that this is still an open area of research.

178: Ditto – I would suggest “One possible refilling mechanism…”

179: “...involves osmoregulation via…” [delete “an”]

179: I would suggest “...generating low osmotic potential…”

181: I would suggest “A refilling mechanism has not yet been identified for conifers, but there is evidence that refilling likely occurs within several species…”

185: Lots of herbaceous plants generate root pressure as well. We’ve measured root pressure in maze in excess of 150kPa… which would be sufficient to lift water 15m high, in the absence of transpiration.

187: It’s not clear why bubbles would “expand at lower tension” after freezing. The sentence that follows explains why gas would spread more widely (from conduit-to-conduit through damaged pit membranes), but not why an individual bubble within a conduit would “expand at lower tension”. This would require a decrease in bubble surface tension (not a change in membrane characteristics). I might suggest a slight modification of the first sentence to bring it aligned with the second: “Embolism arising from the freezing of xylem sap and high tension arising from drought may interact such repeated freeze-thaw and drought events may lead to reduced embolism resistance (cite 10.1104/pp.106.085704 and 10.1007/s00425-003-0997-4). This is because the initial exposure to freezing temperatures may result in the deformation of the ultrastructure of bordered pit membranes, which are critical for preventing the spread of gas from one conduit into another (Christensen-Dalsgaard & Tyree 2014).”

192: “...to cause plant death…”

194: “...without impairing their survival, which suggests…”

196: “High xylem embolism may be an empirical correlate with plant death, rather than a physiological cause…”

201: “...alternative hypotheses…” [plural]

208: “”Memory” (aka “priming”) relates to a defensive plant response to either biotic or abiotic stress (Savvides et al., 2016), and is considered an active process that shifts or enhances the basal of resistance, but at the cost…”

212: “Memory requires… acclimation, which occurs prior to stress exposure.”

226: “...such an increase…”

253 “...vulnerability from frost-induced…”

278: “...promote aboveground dehydration…” [delete “the”]

300: “...plant transpiration, lower leaf water potential, and lower stomatal conductance.” [lower T does not lead to lower psi_leaf and gs]

310 “...eliminate this potential benefit.”

406 “...physiological drivers…” [plural]

410: “...climate...”

419: “...processes have been only studied…”

422: “Notably, do critical…”

447: “...function of the previous level of damage…”

450: delete “in interaction”

In this paper, Charrier et al. discuss the interaction between drought and frost impacts on tree ecophysiology, focusing on the relative timing of these two stress factors in relation to each other and to key phenological processes, and stressing their impact on the tree water and carbon economy. I concur with the authors that the study of the interactions between drought and frost in a temporal context is clearly underrepresented in the literature, and yet it is critical to understand plant responses to climatic constrains in the wild. The topic is thus timely and important. I have to say, however, that I had a hard time reading the text and found it difficult to follow several of the arguments and to understand the general flow of ideas. The paper as currently written is a combination of a review and an opinion piece, but in my view it lacks a clear message that would be effective at moving the field forward. The authors do not provide a common framework that unifies drought and frost impacts on a temporal context, nor give clear indication of what they think should be done in order to improve our understanding of this important interaction. Some of the figures seem a bit disconnected from the text and Figure 1 in particular does not convey a clear message (or I fail to grasp it; see specific suggestions below).

In my opinion the paper needs to be restructured to provide a clearer and more coherent contribution. In many instances the authors mix different temporal, spatial and organizational scales without properly acknowledging the different factors at play. To give just an example, in the paragraph starting in L325 the authors start discussing freeze/thaw-induced embolism and frost cracks, end up by discussing stand-level effects on competition for water (L331-332) and start the next paragraph referring to changes in the density and porosity of the pit membrane (L333-…). I find it essential to clarify the scale of the mechanisms being discussed from the beginning of the paper (perhaps narrowing the focus to within-year seasonal patterns) and then organize the text in a logical way so that the reader knows what to expect in each section. It seems to me that it would be much more effective to consider several scenarios regarding the order and seasonal timing of drought and frost and discuss the key knowns and unknowns in each case. Somehow the paper now fails to provide a clear agenda to advance the study of drought – frost interactions.

The text also needs a careful revision by the authors to improve English usage and the clarity of several sentences. I provide specific suggestions below, but they are not exhaustive.

More detailed or technical comments: Title: you mean ‘...rethinking the timing of risk’?

L17: ‘areas’

L25, 26, 30, …: I think that something like ‘stress factors’ would be more appropriate than ‘constraints’ here and elsewhere in the ms.

L34-35: I do not understand this sentence.

L48: I would tone down a bit the text, for example ‘abiotic factors are typically more relevant…’

L53-55: that seems to be very a temperate-centered view, which is fine, but the biome or ecosystem type you are referring to should be clear from the beginning.

L79: ‘composition’ better than ‘biodiversity’?

L85: and ecologists?

L91: I would limit the use of Latin phrases, as they tend to make the text unnecessarily obscure.

L101: delete ‘can’.

L101-104: this is not exact. See, for instance: Miao et al. 2009 (American Naturalist 173: 113-118), Anderegg et al. 2013 (Tree Physiology 33: 701–712), Batllori et al. 2017 (Ecosphere 8: e01906), Hossain et al. 2018 (Tree Physiology 39: 6–18).

L114: ‘chaotic behavior’ has a very specific mathematical definition, so I suggest using a more general term here (e.g., ‘complex behavior’).

L121-122: simplify text (e.g., ‘to promote an integrative perspective…’).

L123: replace ‘damages’ by ‘stress factors’?

L126: ‘How do…’

Frames #1 and #2: it seems to me that these boxes should be synthesized substantially and simply provide a short summary of our current understanding of drought and frost stress, if possible in a single paragraph for each stress factor. In the case of drought the framework seems to be almost entirely based on McDowell et al. (2008), which was obviously an extremely influential paper but that in my opinion no longer reflects the consensus view on drought-induced mortality. When a water balance approach and consideration of tissue dehydration is advocated for, a reference to Martínez-Vilalta et al. 2019 (New Phytologist 223: 22-32) would seem appropriate. In Frame #2 (2nd paragraph) you seem to imply that water in plant tissues freezes as temperatures go below 0 ºC, which is not the case (substantially lower temperatures are required in many cases).

Frame #3: similarly, I think the arguments here could be greatly synthesized (e.g., the text in L148-153 could be deleted). In addition, I would consider moving the key ideas developed in this box to the main text of the ms. instead of presenting them in a box.

L202: what does ‘structural vs annual’ mean?

L207-208: the theory underlying the relationship between water content and water potential in plant tissues have been developed extensively for at least 50 years; why refer to an equation developed for soils?

L250: ‘approximation’ instead of ‘approach’?

L251: ‘make’.

L253-255: but this seems to contradict the previous sentence.

L256: you mean ‘concepts’ instead of ‘hypotheses’? In any case, it is important to clarify the terminology you introduce. For instance, what is the difference between ‘memory’ as you define it and ‘acclimation’, a much more widely used concept in plant ecophysiology?

L279-280: you mention that on passing, but this is quite critical, right? (Autumns tend to be very wet in many if not most temperate systems).

L290, 297: it is totally unclear to me what this ‘drought stress intensity’ is exactly.

L304: please explain all abbreviations (‘FT’).

L316: but this section deals with the opposite effect, right? Please clarify the text.

L329: why ‘should result’?

L333-348: this whole paragraph is confusing to me.

L387-388: ‘diurnal dynamics’ of what?

L395. ‘Keenan’.

L398: delete ‘thus’?

L411: ‘events’.

L412-415: but reduced leaf area should be advantageous under drought, right?

L436: ‘interaction’ instead of ‘crossing effects’?

L449: delete ‘as mentioned’ and refer to ‘(Frame 3)’.

Figure 1: there are several aspects of this figure I don’t fully understand. For instance, why is ‘frost hardiness’ between ‘summer’ and ‘winter’? why is starch associated to ‘summer’ and solutes to ‘winter’? What does a positive effect of ‘Budburst’ on water stress mean? Are you referring to the timing of budburst? Please be more clear and specific. In addition, using solid and dashed lines for positive and negative relationships would make the diagram clearer, I think.

Figure 3: a more explicative caption and a clearer connection with the main text is required here, I believe.

Figure 4: a ‘Late drought’ in February?

General comments

The authors offer a theory and framework for developing process-based models with the aim to provide better prediction of species distribution limits in the face of climate change. This is certainly an important topic and I found their approach intuitive and well-thought-out. The figures were also helpful in explaining their ideas and I enjoyed reading the manuscript. Although it could be argued that much of what is presented is not especially novel in itself (e.g., modeling interactions, drought tolerance vs frost tolerance, etc), I don’t think this detracts from the manuscript. For example, the fact that there has yet been no successful attempt to model these kinds of interactions (hydraulics, carbon, phenology) to predict the outcome of climate change, does indeed suggest that the manuscript and topic are timely.

One suggestion I have would be to explain a little better how the empirical relationships they so well-describe could be used (or are being used) to build models representing underlying processes and their interactions. For example, the end of the introduction states, “This framework would be crucial to understand local mortality dynamics and ultimately to improve actual species distribution models”. I agree strongly with this. And although they discuss the theory and conceptual steps needed to develop such a model (and identify important obstacles) (Frame 3), it’s not clear to me exactly how this would happen… and I think the authors’ thoughts on this would be very helpful to others. Do the authors see this a being a grass-roots effort to build a model from scratch, which has all the ingredients (e.g., processes, functions, sub-models, etc) needed to examine these interactions, or do they see this more like a patchwork effort that would take models or parts of them (the actual code) and integrate these together into one massive model such that all interactions can be assessed? Would this be a land-surface model or an ESM then? If so, should we start with something like CLM5 and modify it such that it has all the bits and pieces needed to assess these important interactions (this seems contrary to Frame #3)? Or do we start somewhere else entirely? I guess I’m looking for a paragraph that lays out the way (or ways) forward. Are there models and labs out there that could start working together on this issue (maybe they already are?). Would this require additional funding, or additional leadership? Where could these resources potentially come from? I’m not looking for much – just a paragraph or two about how all this could potentially happen (or is already happening). On the other hand, maybe this is beyond the scope of what the authors want to accomplish with this manuscript.

On lines 447 – 449 the authors suggest it is a “prerequisite” that we first improve our understanding of these interactions (presumably via field experiments/observations). Do they really mean this, i.e, that model development should wait until we can improve our understanding of the biology. It seems to me that a properly parameterized model with even a few of the discussed process would help inform our understanding the biology itself, or at least re-direct our experimental efforts.

Specific comments

16: Really? Do we know this? For example, considering the second sentence (“heat waves and drought”) have the competitive interactions between species been experimentally eliminated from the effects of heat and drought in these studies? ...seems like this should still be a very open area of research (environment vs competition). That said, I agree with the authors that models examining the interactions discussed here should not (at least initially) consider competition.

34: I might suggest, “...exposure to a constraint”.

42: Rather than “the tree”, I might suggest something more general (e.g., “plants”, “species”, etc).

45-47: The authors should be allowed their interpretation of the literature. However, for me, it’s a very bold statement to suggest that abiotic factors are in fact the main drivers of distribution limits and evolution. I’m not saying that I think they are definitely wrong (in fact, I’m incline to at least partially agree), but I don’t think the evidence is very strong for their claim. For example, the cited Klanderud et al paper suggests that there is a shift in the relative importance of abioitc and biotic drivers across the temperature gradient, and also emphasized interaction between biotic and abiotic factors. I would also question the efficacy of correlative analysis to address this question altogether. Just to make my point, I can very easily find two papers (the number cited by the authors) in support of the opposite claim, i.e., that competitive exclusion is the main factor defining distribution boundaries (e.g., doi.org/10.1111/jbi.12907). Perhaps it would be more fair to point out that this is still an open question, and an important one. I’m also not sure it’s really necessary to eliminate competition as a important factor at the edges of distributions. I think the authors’ aims with this work and their analyses are just as valid and important.

Box 1: “...depends to a large extent…”

Box 1: It’s not clear what is meant by “hydric insulation”.

Frame 2: Delete extra “)” after “...Koerner 2015).”

Frame 3(ii): By “based on experimental data” do the authors mean that this initial model should be wholly empirical, or should it be mechanistic but validated using experimental data? Or, is this a recipe for building models more generally (process-based and empirical)? I’m just trying to understand the gory details of how the linkages between responses and inputs (or independent variables) work.

205: “McDowell”

207: I would think that the main difficulty would not be water-release relationships so much (i.e., psi ~ soilwatercontent), but rather, the unsaturated soil water conductance (i.e., solution of the Richards equation), and thus, water flux within the soil and between the soil and root (xylem).

310: I might suggest a very short definition of what is meant by “fatigue”, at least the explanation provided in the cited reference. Maybe something like, “...fatigue, i.e., physical or chemical deformation of the pit ultrastructure.”

327: It is not clear what is meant by “punctuations of the vessels [conduits]”. Do the authors mean that the frost crack is bringing air in closer proximity to conduits under tension, and therefore, facilitating air entry? If so, I don’t think this would result in the spread of gas from “conduit to conduit” (i.e., air-seeding through the bordered pit connections).

368-369: Damn… I never considered this.

Figure 3. I might suggest replacing the Christian symbol here with something secular to represent cell death… skull and bones, perhaps? A picture of a McDonalds restaurant? Or perhaps just the words “death”, to be clear?

I would like to thank the authors and editor for giving me the opportunity to review this interesting review. I sincerely hope that at least a few of my comments will be helpful towards revising their manuscript.

Kind regards,

Sean M. Gleason