Dwarf Mistletoe and Drought Contribute to Growth Decline, Dieback and Mortality of Junipers

Round 1

Reviewer 1 Report

This study explores the effect of the increasingly hotter and drier climate and mistletoe infection on juniper growth, dieback, and mortality in eastern Spain. This topic is highly relevant in the context of global climate change and its impacts on forests and shrublands. This study also sheds light on the interactive effects of a little-studied biotic agent (dwarf mistletoe) with drought in a little-studied ecosystem (early seral shrubland/woody plant encroachment following abandoned agricultural land). It is well written, designed, and executed.

General comments:

1. It would be good to clarify which site was considered wet vs. dry in the Methods, section 2.1, and also on the graph labels.
2. It might be worth mentioning at the beginning of the Discussion that the climate has changed at these sites within the lifetime of these trees, according to results on lines 223-224, which is relevant to the aims of the study.
3. The last 2 sentences in the Abstract could use some work.

Abstract

Line 18: I suggest change to “...moisture), an index of drought severity, and mistletoe infection.” for clarity.

Lines 21-22: “prior to mistletoe infestation” does not seem correct. As I understood it, trees were assessed in 2017 or 2020 as to their mistletoe infestation status, and it was not known when they first became infected. Mistletoe is a slow grower, so these trees were probably infected for several years or decades. Please clarify/revise. Maybe change “prior to mistletoe infestation” to “early in development” or something similar.

Final sentence: Please revise. It is vague and doesn’t seem entirely correct or useful. I suggest replacing it with something more meaningful, similar to lines 388-390 or 408-410.

Introduction

Line 66: I suggest change to “mistletoe-infected hosts” from “infected hosts” for clarity.

Lines 77-78: the way these variables are listed reads as somewhat confusing and/or contradictory. I suggest changing to “…as a function of variations in temperature, precipitation, soil moisture, an index of drought severity, and infestation degree by dwarf mistletoe…”

Methods

Lines 131-132: Did all dead junipers have confirmed evidence of mistletoe infestation? Please clarify.

Results

Line 299: please include months considered as summer for summer precipitation.

Lines 308-309: It’s probably not appropriate to interpret main effects for Ribazada, since interactions were significant. Please revise.

Lines 314-318: This section is hard to follow, especially since it is not clear whether the color scale on the graph refers to growth or growth reduction. Please clarify and revise. Also, it appears that the effect of mistletoe cover is weaker in this interaction than the effect of precipitation - please address this here in the revision (although I appreciate it is included in the Conclusions).

Lines 308-319 and Table 2: Was the effect of crown cover also tested? It was my impression from section 2.6 that crown cover and mistletoe infestation were tested separately? Please clarify.

Discussion

Line 374: synergistically?

Conclusions

Lines 406-407: Drought during wet summers? Seems contradictory. Please clarify/revise.

Line 408: same comment as lines 21-22 in Abstract.

Figures & Tables

Table 1: Is “Ring width (mm)” really “Mean ring width (mm)” over the entire time span or best-replicated time span? Please clarify.

Fig. 3 caption: add +/- before SE

Author Response

Reviewer 1

English language and style

( ) Extensive editing of English language and style required
( ) Moderate English changes required
(x) English language and style are fine/minor spell check required
( ) I don't feel qualified to judge about the English language and style

 

	Yes	Can be improved	Must be improved	Not applicable
Does the introduction provide sufficient background and include all relevant references?	(x)	( )	( )	( )
Is the research design appropriate?	(x)	( )	( )	( )
Are the methods adequately described?	(x)	( )	( )	( )
Are the results clearly presented?	(x)	( )	( )	( )
Are the conclusions supported by the results?	(x)	( )	( )	( )

 

Comments and Suggestions for Authors

This study explores the effect of the increasingly hotter and drier climate and mistletoe infection on juniper growth, dieback, and mortality in eastern Spain. This topic is highly relevant in the context of global climate change and its impacts on forests and shrublands. This study also sheds light on the interactive effects of a little-studied biotic agent (dwarf mistletoe) with drought in a little-studied ecosystem (early seral shrubland/woody plant encroachment following abandoned agricultural land). It is well written, designed, and executed.

• We thank you for the positive comments on our manuscript.

General comments:

1. It would be good to clarify which site was considered wet vs. dry in the Methods, section 2.1, and also on the graph labels.
2. It might be worth mentioning at the beginning of the Discussion that the climate has changed at these sites within the lifetime of these trees, according to results on lines 223-224, which is relevant to the aims of the study.
3. The last 2 sentences in the Abstract could use some work.

• We clarified the wet-dry sites in the section 2.1.
• We also mentioned in the Discussion the drying climate trend of the study sites as presented in lines 223-224.
• We also rephrased the last 2 sentences of the abstract.

 

Abstract

Line 18: I suggest change to “...moisture), an index of drought severity, and mistletoe infection.” for clarity.

•  

 

Lines 21-22: “prior to mistletoe infestation” does not seem correct. As I understood it, trees were assessed in 2017 or 2020 as to their mistletoe infestation status, and it was not known when they first became infected. Mistletoe is a slow grower, so these trees were probably infected for several years or decades. Please clarify/revise. Maybe change “prior to mistletoe infestation” to “early in development” or something similar.

• We changed it since we do not know the start of infestation.

 

Final sentence: Please revise. It is vague and doesn’t seem entirely correct or useful. I suggest replacing it with something more meaningful, similar to lines 388-390 or 408-410.

• We revised and changed it.

 

Introduction

Line 66: I suggest change to “mistletoe-infected hosts” from “infected hosts” for clarity.

•  

 

Lines 77-78: the way these variables are listed reads as somewhat confusing and/or contradictory. I suggest changing to “…as a function of variations in temperature, precipitation, soil moisture, an index of drought severity, and infestation degree by dwarf mistletoe…”

•  

 

Methods

Lines 131-132: Did all dead junipers have confirmed evidence of mistletoe infestation? Please clarify.

 

• All dead junipers showed remains of dead mistletoe and infected branches. This was stated in the text.

 

Results

Line 299: please include months considered as summer for summer precipitation.

•  

 

Lines 308-309: It’s probably not appropriate to interpret main effects for Ribazada, since interactions were significant. Please revise.

• We revised and changed the text.

 

Lines 314-318: This section is hard to follow, especially since it is not clear whether the color scale on the graph refers to growth or growth reduction. Please clarify and revise. Also, it appears that the effect of mistletoe cover is weaker in this interaction than the effect of precipitation - please address this here in the revision (although I appreciate it is included in the Conclusions).

• The color scale refers to growth (BAI) so the interaction between infestation and summer precipitation is interpreted as being stronger, i.e. reducing more growth, during wet than during dry periods for mistletoe cover values high enough. We also commented the weaker effect of mistletoe as you suggested.

 

Lines 308-319 and Table 2: Was the effect of crown cover also tested? It was my impression from section 2.6 that crown cover and mistletoe infestation were tested separately? Please clarify.

• We did not test the effect of crown cover since this variable was inversely related to mistletoe infestation, i.e. they were redundant. We indicate this in the revised. Methods

Discussion

Line 374: synergistically?

 

• We corrected it.

 

Conclusions

Lines 406-407: Drought during wet summers? Seems contradictory. Please clarify/revise.

• We rephrased it.

 

Line 408: same comment as lines 21-22 in Abstract.

• We rephrased it

 

Figures & Tables

 

Table 1: Is “Ring width (mm)” really “Mean ring width (mm)” over the entire time span or best-replicated time span? Please clarify.

• We clarified it.

 

Fig. 3 caption: add +/- before SE

• We added it.

Reviewer 2 Report

The study by Tamudo et al. assesses how climate and mistletoe infection effect basal area growth at two locations with contrasting microclimate. It is an interesting study, particularly because they focus on smaller and shrubbier junipers that are typically overlooked as most studies that use dendrochronology focus on tall, infected trees. The authors construct a dendrochronological record from trees with contrasting mistletoe loads at the time of sampling, and use gridded climate data for further analysis between BAI and climate variables. The manuscript is well written and the data is well presented.

Overall, the manuscript could be improved by clarifying some of the key terminology and by incorporating SPEI and rainfall anomalies into the mixed effects linear model. Currently, some of the conclusions are not supported by the presented analysis, particularly any references to drought, which appear to be used interchangeably with summer rainfall. I’d also like to see a brief discussion about the shortcomings of using coarsely gridded climate data for the climate analysis, and about potential issues that arise from using a fixed grouping (declining, non-declining, dead) that was determined at the time of sampling (the mistletoe load cannot be assumed stable over 100 years). Lastly, I think the manuscript could gain appeal to a broader, international readership if the authors discuss succession dynamics in relation to mistletoe-induced juniper death in more detail.  

I’m looking forward to receiving the revised manuscript.

 

Detailed comments:

L18-19: can you be more specific and name a temperature and precipitation threshold?

L 37-40: name a few species

L43-44: Explain how they are vulnerable to high air temperatures and high VPD. Why would they be more vulnerable as shrubs than as trees? And wouldn’t low stomatal regulation result in evaporative cooling that protects leaves against temperature damage (see e.g. Drake et al., 2018)?

L51-54: It currently sounds like dieback has been observed in Scots pine that were infected with Viscum album, but it’s been documented across a diverse range of ecosystems and host-mistletoe combinations. See e.g. Bell et al., 2020, Gea-Izquierdo et al., 2019, Griebel et al., 2021). Please include some of the international studies to strengthen the relevance of your study to an international audience.

L60: hosts (plural)

L63: So it has been studied at shrubs before? Can you summarize key differences to trees (if there were any)?

L65-67: Can you give examples for anatomical defenses and explain how mistletoes reduce water use efficiency?

L69-71: Did you mean carbon reservoirs instead of sources? Given your focus on growth declines, it would be useful to highlight some specific processes how mistletoe infection leads to a reduction in carbon sources (such as increased stomatal closure and thus reduced photosynthetic period of host leaves; see e.g. Zweifel et al., 2012)?

L73-75: It’s a bit weak to justify the study just because the interaction of mistletoe and drought stress hasn’t been assessed in juniper shrubs yet. Can you think of a stronger justification and highlight why your study would be relevant for the global community of researchers assessing mistletoe-host interactions? Does your study provide any implications for land management and stand succession?

L97: Provide the reference period for the climate data, the location of the weather station and the distance of the station to your sites. How far apart were the two sites?

Section 2.2: This general description of mistletoe-host interaction does not belong to the methods section and should be moved to the introduction. Please avoid duplication, e.g. between L110-113 and L61-71.

L123: Since when does crown cover equal tree vigour?! Maybe this is just ill-termed, can you think of a better term (maybe canopy health classes?)?

L.124-132: I’m having troubles understanding how trees were classified and with the chosen terminology for the three groups. Declining in what? Tree health/vigour? Can you please provide the details specifically for each category (it’s very confusing with the current presentation)? And what exactly do the percentages relate to? The ratio of mistletoe:host leaf area? Please also clarify what exactly you mean with ‘crown cover’, and why you have classified trees as high infestation starting with 15%. I’m presuming from here on that this value refers to mistletoe:host foliage ratio as e.g. in Griebel et al., 2021.

Section 2.5: Is this grid-cell size appropriate for the topography of the study site and does it account for differences between the two aspects at that resolution? I’d like to see Figure 2 replicated for each of your two study locations in the appendix, if the two sites don’t fall into the same grid cell.

L183: Please find a better naming convention than ‘declining’ and ‘non-declining’, and clarify ‘growth rate’. Is this mean annual BAI?

L193-197: Did you remove this part from the results section? I can’t seem to find any dedicated statistical test that links drought to BAI, particularly none that would support your conclusion about growth responsiveness to summer precipitation peaking during dry periods (L387-388). Am I missing something here? Why did you not include this into your mixed-effects model? Then you could statistically assess the interaction between summer rainfall and drought (and mistletoe infection).

L199: Why was a 20-month interval chosen for SPEI and a 20-year interval chosen for rainfall? The latter seems overly excessive. Are there any climate circulations that might affect Precipitation at a 20-year interval? Please justify or revise interval size to align with SPEI.

L205: Is this now summer precipitation from the current year or the previous 20 years? Please clarify. You could also consider calculating rainfall anomalies.

L217: Please explain the bootstrapping approach in the methods section.

L223-224: They correlate, but you can’t attribute this to the warming trend.

L238-242: This is awkwardly worded, please clarify ‘mean correlation among series’.

Table 1: Define ‘mistletoe infestation (%)’ and correct typo in the last cell value

Figure 3: I suggest to highlight periods where growth rates differed significantly by grey shading of the white space.

L356-258: Is any of that significant?

Figure 5: This is cool, well presented!

Figure 6: Why were dead trees omitted here?

L317: Please correct typo of ‘grow los’

L314-316: I’m not sure this is a correct interpretation. Looking at Figure 7, it seems more likely that high summer precipitation only had a positive effect when mistletoe cover was low, and the negative influence of mistletoe cover on BAI dominated any amount of summer precipitation once it exceeded 50%. Please clarify if I misinterpreted this.

Table 2: So mistletoe infestation alone had no effect and only summer precipitation affected BAI at Aliaga? That’s important and should be highlighted in L308-319.

L337-341: Please see my suggestion above relating to this interpretation. I also doubt that you can make any inferences to microclimate here when you only use one set of climate data to compare both sites.

L342-346: You have assessed summer rainfall, not drought, so your analysis does not support any conclusion about the interaction of drought and mistletoe. You have clearly demonstrated that summer rainfall significantly affected BAI at both study sites, which is still an important finding. But please don’t use that interchangeably with drought throughout the discussion.

L346-347: You could start your discussion with this finding, no need to bury it that far down in the paragraph.

L387-388: Where did you show that? This would actually be an interesting analysis that you could, and should, look into. Couldn’t you add a moving interval of SPEI and/or precipitation (maybe a moving average or rainfall anomalies over the past 24-months) to your linear mixed-effects model to check if there is a two-way or three- way interaction between summer precipitation and drought (and mistletoe infection)?

L390-396: Can you elaborate further on potential stand-replacing dynamics that would follow increased mortality rates of infected junipers? I’m not familiar with Mediterranean vegetation successions, but I assume there should be several publications on this given that tree mortality following drought is an emerging issue in Mediterranean ecosystems. There are not many publications around that specifically discuss succession dynamics in relation to mistletoes, but there is a dedicated section in a review by Griebel et al., 2017 that might provide some relevant insights. Strengthening this aspect would also help to extend the implications of your study to the international audience.

 

References:

Bell, DM et al. (2020). Tree growth declines and mortality were associated with a parasitic plant during warm and dry climatic conditions in a temperate coniferous forest ecosystem. Global Change Biology, 26(3), 1714-1724

Gea-Izquierdo G, et al. 2019. Synergistic abiotic and biotic stressors explain widespread decline of Pinus pinaster in a mixed forest. Science of the Total Environment 685, 963–975.

Griebel, A., Watson, D., & Pendall, E. (2017). Mistletoe, friend and foe: synthesizing ecosystem implications of mistletoe infection. Environmental Research Letters, 12(11), 115012.

Griebel, A et al. (2021). Recovery from Severe Mistletoe Infection After Heat-and Drought-Induced Mistletoe Death. Ecosystems, 1-16.

Zweifel R et al. (2012). Pine and mistletoes: how to live with a leak in the water flow and storage system? Journal of Experimental Botany 63(7), 2565–2578.

Author Response

Reviewer 2

English language and style

( ) Extensive editing of English language and style required
( ) Moderate English changes required
(x) English language and style are fine/minor spell check required
( ) I don't feel qualified to judge about the English language and style

 

	Yes	Can be improved	Must be improved	Not applicable
Does the introduction provide sufficient background and include all relevant references?	( )	(x)	( )	( )
Is the research design appropriate?	( )	(x)	( )	( )
Are the methods adequately described?	( )	( )	(x)	( )
Are the results clearly presented?	( )	(x)	( )	( )
Are the conclusions supported by the results?	( )	(x)	( )	( )

 

Comments and Suggestions for Authors

The study by Tamudo et al. assesses how climate and mistletoe infection effect basal area growth at two locations with contrasting microclimate. It is an interesting study, particularly because they focus on smaller and shrubbier junipers that are typically overlooked as most studies that use dendrochronology focus on tall, infected trees. The authors construct a dendrochronological record from trees with contrasting mistletoe loads at the time of sampling, and use gridded climate data for further analysis between BAI and climate variables. The manuscript is well written and the data is well presented.

 

• We thank you for the positive comments on our manuscript.

 

Overall, the manuscript could be improved by clarifying some of the key terminology and by incorporating SPEI and rainfall anomalies into the mixed effects linear model. Currently, some of the conclusions are not supported by the presented analysis, particularly any references to drought, which appear to be used interchangeably with summer rainfall. I’d also like to see a brief discussion about the shortcomings of using coarsely gridded climate data for the climate analysis, and about potential issues that arise from using a fixed grouping (declining, non-declining, dead) that was determined at the time of sampling (the mistletoe load cannot be assumed stable over 100 years). Lastly, I think the manuscript could gain appeal to a broader, international readership if the authors discuss succession dynamics in relation to mistletoe-induced juniper death in more detail.  

 

I’m looking forward to receiving the revised manuscript.

 

• We used summer precipitation in the mixed models of growth because it provided better and more meaningful explanations than using the SPEI drought index or rainfall anomalies.
• We also discussed the shortcomings of using gridded climate data, which are evident in the case of Mediterranean mountain areas where local precipitation records are scarce or heterogeneous, but very important for dendroecological studies.
• We are also aware that we did not know the year of infestation so using fixed groups or categories is based on the final vigor status observed in the field. We can reconstruct growth changes and related them to recent defoliation, but we cannot reconstruct the degree of mistletoe infestation. We added these aspects to the revised discussion and also some final lines to the impacts of mistletoe and drought on succession dynamics of juniper shrublands.

 

Detailed comments:

L18-19: can you be more specific and name a temperature and precipitation threshold?

 

• This is not an easy question. We cannot provide such threshold values since our analyses do not allow calculating them. For instance, growth increases as precipitation does and the relationship is linear, so a rainfall threshold cannot be directly obtained.

 

L 37-40: name a few species

•  

 

L43-44: Explain how they are vulnerable to high air temperatures and high VPD. Why would they be more vulnerable as shrubs than as trees? And wouldn’t low stomatal regulation result in evaporative cooling that protects leaves against temperature damage (see e.g. Drake et al., 2018)?

• Some juniper species have been shown to be very sensitive to elevated temperatures and VPD. This has been demonstrated by analyzing ring growth and leaf O isotopes which showed that junipers presented dieback and reduced growth as air temperatures rose above certain thresholds leading to excessive water loss through leaves (e.g., Altieri et al. 2015). This explanation was added to the revised ms. Evaporative cooling may protect leaves but does not avoid water loss.

 

L51-54: It currently sounds like dieback has been observed in Scots pine that were infected with Viscum album, but it’s been documented across a diverse range of ecosystems and host-mistletoe combinations. See e.g. Bell et al., 2020, Gea-Izquierdo et al., 2019, Griebel et al., 2021). Please include some of the international studies to strengthen the relevance of your study to an international audience.

 

•  

 

L60: hosts (plural)

 

•  

 

L63: So it has been studied at shrubs before? Can you summarize key differences to trees (if there were any)?

• We rephrased the sentence since the reduction of radial growth by dwarf mistletoe was studied in tree species.

 

L65-67: Can you give examples for anatomical defenses and explain how mistletoes reduce water use efficiency?

 

• We think commenting on anatomical defense is out of the scope of the introduction since our study focused on radial growth. Mistletoes reduce water use efficiency by promoting a profuse water use by host trees (we rephrased the sentence).

 

L69-71: Did you mean carbon reservoirs instead of sources? Given your focus on growth declines, it would be useful to highlight some specific processes how mistletoe infection leads to a reduction in carbon sources (such as increased stomatal closure and thus reduced photosynthetic period of host leaves; see e.g. Zweifel et al., 2012)?

 

• We rephrased the sentence following your suggestion. We refer to carbon sources (photosynthesis) vs. carbon sinks (growth, meristems).

 

L73-75: It’s a bit weak to justify the study just because the interaction of mistletoe and drought stress hasn’t been assessed in juniper shrubs yet. Can you think of a stronger justification and highlight why your study would be relevant for the global community of researchers assessing mistletoe-host interactions? Does your study provide any implications for land management and stand succession?

 

• We think our justification is strong enough since assessing the interactions of two stress factors such as mistletoe and drought on juniper growth is relevant for land management of pioneer shrublands which could show a allowing down of succession dynamics towards forests (this is indicated in the revised Discussion and here as you suggested).

 

L97: Provide the reference period for the climate data, the location of the weather station and the distance of the station to your sites. How far apart were the two sites?

 

• The two sites are located about 1.5 km far apart from each other.

 

Section 2.2: This general description of mistletoe-host interaction does not belong to the methods section and should be moved to the introduction. Please avoid duplication, e.g. between L110-113 and L61-71.

 

• We disagree on your comment since this sections refers to the mistletoe-host interaction for this specific study case. We prefer keeping here this section and describing each species of the study interaction, and removing redundant information.

 

L123: Since when does crown cover equal tree vigour?! Maybe this is just ill-termed, can you think of a better term (maybe canopy health classes?)?

 

• We used crown cover as a surrogate of vigour. This is widely accepted by many forest scientists, including the ICP-forests European network which monitors crown defoliation every year in thousands of trees and plots across Europe to assess their changes in vigour. To avoid confusion, we replaced the term “vigour” by “health class”.

 

L.124-132: I’m having troubles understanding how trees were classified and with the chosen terminology for the three groups. Declining in what? Tree health/vigour? Can you please provide the details specifically for each category (it’s very confusing with the current presentation)? And what exactly do the percentages relate to? The ratio of mistletoe:host leaf area? Please also clarify what exactly you mean with ‘crown cover’, and why you have classified trees as high infestation starting with 15%. I’m presuming from here on that this value refers to mistletoe:host foliage ratio as e.g. in Griebel et al., 2021.

 

• The percentages refer to crown cover and they were used to define the health classes. We clarified this issue and rephrased the related sentences. We defined mistletoe abundance and crown cover as two different variables and they differ from the mistletoe:host foliage ratio since we were unable to estimate the mistletoe foliage cover, only its relative cover in the shrub (see Figs. 1b & 1c). Junipers with low mistletoe abundance had percentages between 0 and 5%, not 15% (we corrected this mistake). This low threshold was considered to account for estimating errors of mistletoe abundance.

 

Section 2.5: Is this grid-cell size appropriate for the topography of the study site and does it account for differences between the two aspects at that resolution? I’d like to see Figure 2 replicated for each of your two study locations in the appendix, if the two sites don’t fall into the same grid cell.

 

• We discussed this aspect in the revised Discussion. As stated before, gridded climate data may provide a too low resolution of local precipitation variability in the case of Mediterranean mountain areas. However, since local precipitation records are scarce, short or heterogeneous in the study sites, we used gridded data with the best available resolution. The two study sites fall into the same grid cell.

 

L183: Please find a better naming convention than ‘declining’ and ‘non-declining’, and clarify ‘growth rate’. Is this mean annual BAI?

 

• Growth rate refers to ring width (we clarified it). We have used in several previous papers the naming of declining vs. non-declining individuals. We think it is clear enough to distinguish different health classes.

 

L193-197: Did you remove this part from the results section? I can’t seem to find any dedicated statistical test that links drought to BAI, particularly none that would support your conclusion about growth responsiveness to summer precipitation peaking during dry periods (L387-388). Am I missing something here? Why did you not include this into your mixed-effects model? Then you could statistically assess the interaction between summer rainfall and drought (and mistletoe infection).

• These analyses correspond to Figs. 4, 5 & 6.We removed lines 387-388 to avoid confusion. We only considered summer rainfall in the models because models provided a better explanatory power and were more parsimonious than using SPEI or rainfall anomalies.

L199: Why was a 20-month interval chosen for SPEI and a 20-year interval chosen for rainfall? The latter seems overly excessive. Are there any climate circulations that might affect Precipitation at a 20-year interval? Please justify or revise interval size to align with SPEI.

 

• These two criterions are not related. Using a 20-year interval for moving correlations is conservative enough to assess the significance of correlations with growth (see Fig. 6). Using a 20-month interval for SPEI analyses allows including long enough droughts which can also affect growth at shorter time scales (1-2 years; see Pasho et al. 2011 in Agric For Meteorol. for a comparison of SPEI windows in several tree species).

 

L205: Is this now summer precipitation from the current year or the previous 20 years? Please clarify. You could also consider calculating rainfall anomalies.

 

• We used current year summer precipitation in the models (we indicated it in the revised text).

 

L217: Please explain the bootstrapping approach in the methods section.

 

• Thank you.

 

L223-224: They correlate, but you can’t attribute this to the warming trend.

 

• Done, we rephrased it.

 

L238-242: This is awkwardly worded, please clarify ‘mean correlation among series’.

 

• Done, we reworded it. We refer to the mean correlation of individual growth (ring-width) series. This terminology is widely used by dendroecologists.

 

Table 1: Define ‘mistletoe infestation (%)’ and correct typo in the last cell value

 

• We refer to mistletoe crown cover.

 

Figure 3: I suggest to highlight periods where growth rates differed significantly by grey shading of the white space.

 

• We think these periods are clearly indicated in the text and showing them in the figure would make it less clear. Nevertheless, we have highlighted as you suggested.

 

L256-258: Is any of that significant?

 

• We left in the revised text only the significant differences.

 

Figure 5: This is cool, well presented!

• Thanks a lot.

 

Figure 6: Why were dead trees omitted here?

• Because they were not well replicated so as to show strong enough correlations. We commented this fact in the revised Methods.

 

L317: Please correct typo of ‘grow los’

 

• We reworded this part.

 

L314-316: I’m not sure this is a correct interpretation. Looking at Figure 7, it seems more likely that high summer precipitation only had a positive effect when mistletoe cover was low, and the negative influence of mistletoe cover on BAI dominated any amount of summer precipitation once it exceeded 50%. Please clarify if I misinterpreted this.

 

• We agree on your interpretation and we have reworded this part accordingly.

 

Table 2: So mistletoe infestation alone had no effect and only summer precipitation affected BAI at Aliaga? That’s important and should be highlighted in L308-319.

 

• We agree and we emphasize it.

 

L337-341: Please see my suggestion above relating to this interpretation. I also doubt that you can make any inferences to microclimate here when you only use one set of climate data to compare both sites.

 

• We agree again and we have reworded the Discussion following your suggestions.

 

L342-346: You have assessed summer rainfall, not drought, so your analysis does not support any conclusion about the interaction of drought and mistletoe. You have clearly demonstrated that summer rainfall significantly affected BAI at both study sites, which is still an important finding. But please don’t use that interchangeably with drought throughout the discussion.

 

• We assessed drought impacts on growth in the analyses considering the SPEI drought index. Nevertheless, we rephrased the sentence commenting on summer rainfall.

 

L346-347: You could start your discussion with this finding, no need to bury it that far down in the paragraph.

 

• Thank you again.

 

L387-388: Where did you show that? This would actually be an interesting analysis that you could, and should, look into. Couldn’t you add a moving interval of SPEI and/or precipitation (maybe a moving average or rainfall anomalies over the past 24-months) to your linear mixed-effects model to check if there is a two-way or three- way interaction between summer precipitation and drought (and mistletoe infection)?

 

• We removed the sentence. As explained before, adding SPEI or rainfall anomalies lead to redundant growth models with more complexity and less explanatory power than using summer precipitation alone.

 

L390-396: Can you elaborate further on potential stand-replacing dynamics that would follow increased mortality rates of infected junipers? I’m not familiar with Mediterranean vegetation successions, but I assume there should be several publications on this given that tree mortality following drought is an emerging issue in Mediterranean ecosystems. There are not many publications around that specifically discuss succession dynamics in relation to mistletoes, but there is a dedicated section in a review by Griebel et al., 2017 that might provide some relevant insights. Strengthening this aspect would also help to extend the implications of your study to the international audience.

 

• We discussed the implications following some of the ideas exposed by Griebel et al. (2017). Thanks a lot for your constructive and detailed review.

 

References:

Bell, DM et al. (2020). Tree growth declines and mortality were associated with a parasitic plant during warm and dry climatic conditions in a temperate coniferous forest ecosystem. Global Change Biology, 26(3), 1714-1724

Gea-Izquierdo G, et al. 2019. Synergistic abiotic and biotic stressors explain widespread decline of Pinus pinaster in a mixed forest. Science of the Total Environment 685, 963–975.

Griebel, A., Watson, D., & Pendall, E. (2017). Mistletoe, friend and foe: synthesizing ecosystem implications of mistletoe infection. Environmental Research Letters, 12(11), 115012.

Griebel, A et al. (2021). Recovery from Severe Mistletoe Infection After Heat-and Drought-Induced Mistletoe Death. Ecosystems, 1-16.

Zweifel R et al. (2012). Pine and mistletoes: how to live with a leak in the water flow and storage system? Journal of Experimental Botany 63(7), 2565–2578.

Round 2

Reviewer 2 Report

The revised manuscript has greatly improved from the original version, as the authors could remove most ambiguities via rephrasing and the terminology has been clarified. I thank the authors for considering many of my suggestions, and can follow their reasoning where suggested changes were not implemented. The authors didn’t provide responses to some individual comments, but it seems that they were still considered in the revised manuscript. Thorough spell checking might remove some remaining minor grammar errors, and these queries should be addressed:

1. The abstract is missing conclusions based on their findings and a statement about the broader implications
2. The bootstrapping approach is still insufficiently explained and it is unclear what the authors mean with ‘SPEI rate’.
3. The referencing in L458 and L524 needs updating after the latest changes

Author Response

Dear reviewer, we thank you for your second review of the manuscript. We have incorporated the new changes as you suggested by:

1-adding conclusions and broader implications to the abstract,

2-better explaining the bootstrapping approach and removing the expression “SPEI rate”, which was replaced by “SPEI trend”,

3-updating references shown in lines 458 and 524.

Thanks again for your detailed and helpful reviews.