Heat Wave, Cone Crops, Forest-Floor Small Mammals, and Mustelid Predation in Coniferous Forests of Southern British Columbia

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

This manuscript addresses the connection between a heat wave in forests in Canada and the subsequent responses of small mammals and their predators, due to an increase in coniferous cone crops. The work tests specific predictions related to the variation in demographic parameters of seed-eating mammals in different types of forests. In general, the paper is well-written and presents interesting results related to the potential consequences of climate change.    The paper contains valuable data about the variation of different demographic parameters of three species of rodents, presents information about other small mammals,  analyses the variation in the abundance of small mammals and examines the activity of predators. The paper includes nine figures and four tables. My main concern about the document is that its current presentation obscures the main messages the authors are trying to convey because of the large amount of information presented and the length of the document. The amount of results makes ideas hard to follow. Consider making sections of the paper based on each of the hypotheses you are evaluating. Make sure you link the results with particular predictions. Also, I feel that some of the data are underused. For example, the authors could write a robust contribution using only the results in Table 2. That may allow them to look in more detail at the particular responses of demographic parameters of each of the three species of rodents.    I also find room for improvement in the statistical analyses. Based on the values presented in Table 2, I  expected several parameters of the three species to have significant differences. However, in the table, only abundance/ha of Peromyscus maniculatus shows significant differences among the years. This is peculiar because, for example, the Total number of juvenile recruits for P. maniculatus in 2023 is almost five times the number in 2022. I suggest the authors use ANOVAs for each demographic parameter as the dependent variable and the year and the species as independent variables.    Understanding the message each figure wants to deliver would be much easier if the authors included a sentence indicating to the reader what to look at. I suggest the authors follow the suggestions to improve the legends of tables and figures presented in: Kroodsma DE. 2000. A quick fix for figure legends and table headings. The Auk 117: 10811081.   Tables 3 and 4 present results from repeated-measures ANOVA. It is recommended that the final model include only the significant predictors. For example, in Table 3, the final statistical model should not include the interaction "Treatment x Time" (p=0.25). Removing the interaction in this case may allow the authors to evaluate whether other main effects are statistically significant, e.g., "Treatment"(p=0.12) for P. maniculatus. The authors should consider using a general linear model as an alternative analysis.   Figures 4-6 suggest a potential effect related to the month of the year. Therefore, the authors should consider including this factor nested in the year in the analyses. In the graphs, it is necessary to show the reader where the significant differences are. Consider using different letters to show this, as in Table 2, or including in the graphs 95% confidence intervals   In the Introduction, the authors indicate that the heat wave that originated the "natural experiment" was a product of climate change. Consequently, I was expecting in the Discussion a paragraph about the potential consequences of this type of phenomenon on the ecology of the forests and maybe some recommendations for their management, considering that the results are about areas with different characteristics. I also suggest analysing the need for future studies to evaluate the predictions that received only partial support from the data.   I like the content of the paper very much and I hope the authors can use these comments to build a solid contribution.   Additional specific comments are included in the pdf.

Comments for author File: Comments.pdf

Author Response

This manuscript addresses the connection between a heat wave in forests in Canada and the subsequent responses of small mammals and their predators, due to an increase in coniferous cone crops. The work tests specific predictions related to the variation in demographic parameters of seed-eating mammals in different types of forests. In general, the paper is well-written and presents interesting results related to the potential consequences of climate change.  The paper contains valuable data about the variation of different demographic parameters of three species of rodents, presents information about other small mammals, analyses the variation in the abundance of small mammals and examines the activity of predators.

 

The paper includes nine figures and four tables. My main concern about the document is that its current presentation obscures the main messages the authors are trying to convey because of the large amount of information presented and the length of the document. The amount of results makes ideas hard to follow. Consider making sections of the paper based on each of the hypotheses you are evaluating. Make sure you link the results with particular predictions.

 

The number of figures has been reduced from 9 to 6 and this change has helped to streamline the Results section. In addition, as noted below, Table 2 has reduced content and statistical analysis has helped to highlight important results.

Also, I feel that some of the data are underused. For example, the authors could write a robust contribution using only the results in Table 2. That may allow them to look in more detail at the particular responses of demographic parameters of each of the three species of rodents. I also find room for improvement in the statistical analyses. Based on the values presented in Table 2, I expected several parameters of the three species to have significant differences. However, in the table, only abundance/ha of Peromyscus maniculatus shows significant differences among the years. This is peculiar because, for example, the total number of juvenile recruits for P. maniculatus in 2023 is almost five times the number in 2022. I suggest the authors use ANOVAs for each demographic parameter as the dependent variable and the year and the species as independent variables. 

 

Lines 323-351: Revised as suggested. Table 2 reduced in content and ANOVA results added for all three species.

 

Understanding the message each figure wants to deliver would be much easier if the authors included a sentence indicating to the reader what to look at. I suggest the authors follow the suggestions to improve the legends of tables and figures presented in: Kroodsma DE. 2000. A quick fix for figure legends and table headings. The Auk 117: 10811081.

 

Additional information added to figure captions.

 

Tables 3 and 4 present results from repeated-measures ANOVA. It is recommended that the final model include only the significant predictors. For example, in Table 3, the final statistical model should not include the interaction "Treatment x Time" (p=0.25). Removing the interaction in this case may allow the authors to evaluate whether other main effects are statistically significant, e.g., "Treatment"(p=0.12) for P. maniculatus. The authors should consider using a general linear model as an alternative analysis.  

 

The RM-ANOVA has been retained to test the important factor of time: 2023 versus 2024 for mean values of abundance and demographic attributes.

 

Figures 4-6 suggest a potential effect related to the month of the year. Therefore, the authors should consider including this factor nested in the year in the analyses. In the graphs, it is necessary to show the reader where the significant differences are. Consider using different letters to show this, as in Table 2, or including in the graphs 95% confidence intervals.  

 

Figures 4-6 have been deleted with important mean annual values and results of analyses given in Tables 3 and 4. This change has helped to streamline the Results section, reducing the number of figures from 9 to 6.

 

In the Introduction, the authors indicate that the heat wave that originated the "natural experiment" was a product of climate change. Consequently, I was expecting in the Discussion a paragraph about the potential consequences of this type of phenomenon on the ecology of the forests and maybe some recommendations for their management, considering that the results are about areas with different characteristics.

 

Lines 645-648: Additional information added here.

 

I also suggest analysing the need for future studies to evaluate the predictions that received only partial support from the data.   I like the content of the paper very much and I hope the authors can use these comments to build a solid contribution.  

 

Lines 621-623: Additional comment here on possible future studies.

 

Additional specific comments are included in the pdf.

 

These are very helpful suggestions in the marked pdf and, where appropriate, they have been incorporated in the text. Thank you.

Reviewer 2 Report

Comments and Suggestions for Authors

This study collected and analyzed natural data from four consecutive years, which is a large amount of work, and the research content is somewhat appealing, but the angle of entry for the main idea of the article may be less than ideal, and the following are some of my modifications to this article, which I hope will be helpful to the authors:

1. The abstract section is overly descriptive about the study area, and it is recommended that this section be deleted. In addition, the abstract only mentions the three hypotheses and findings in the text, but does not reflect the research methodology, so it is recommended that the authors use concise text in the abstract to summarize the main research methodology in the text.
2. The article defines the rodents studied as seed predators versus small mammals, and I would suggest that the authors use one designation in the text if possible, standardizing on either seed predators or small mammals.
3. The main hypothesis of the article is that growth in plant production causes growth in the number of seed predators, which in turn leads to a rise in the number of predators, which in turn leads to a further decline in the number of seed predators. This is actually the role of upward and downward effects co-regulating in the ecosystem, but the preface of the article does not center on these two types of ecological effects. The preface gives too much background on the phenomenon of fruit abundance, but this does not seem to be ultimately relevant to the scientific question the article is trying to address. It is recommended that the authors reorganize the logic of the preface by simplifying the first five paragraphs to two or three paragraphs with a brief text about climate change affecting fruit production and thus ecological effects on organisms at higher trophic levels. In addition, it is recommended that the preface focus on the ecological role of upward and downward effects, which in turn introduces the main research thrust of the paper.
4. The Methods section is overly cluttered; the article begins with an introduction to the study area, but there is still more text about the study area in subsequent paragraphs.The title of 2.2 looks like a design total of the research methodology for the full text, but the actual content is a delineation of the study area, and it is recommended that the authors revise the subheading of 2.2.The content of Demographic Analysis looks like it should be categorized under Data Analysis. In general, it is recommended that the authors reorganize the text in the Methods section according to the logic of Vegetation Data Collection - Animal Data Collection - Measurement of Relevant Indicators - Data Analysis.
5. Table 2 of the results contains too much data, which makes it difficult to visualize the important contents, so it is suggested that the authors can choose only the important data contents to be reflected in the text, and the complete charts can be put in the annex. In addition, this kind of continuous change data can be more intuitively reflected by using visual pictures to show the trend of change in different years, and it is suggested that the authors can consider selecting important indicators and reflecting this part of the data in the form of line graphs.
6. In section 3.2 of the results, it is mentioned that the high occurrence of predators led to a decrease in the density of flowerback rats, and in 3.5 it is mentioned that the change in the number of predators could be due to an increase in the number of rats. There are many factors affecting wildlife populations, such as climate change, food changes, etc. Because the authors' methodology does not mention strict control variables, it is difficult to attribute the decline in rodent populations to predators or changes in predators due to changes in prey.
7. In the results section of the article, the authors will explain some of the results, but it should be in the discussion section, and it is recommended that the authors simplify some of the text of the results, and visualize the changes in the data and the correlation between the various types of data more visually in the results section.
8. There is a lot of text in the discussion, but the discussion as a whole does not go far enough. The authors in the text mention three hypotheses and claim that they are partially supported, but based on the results of the analysis, I think the authors' validation mainly relies on observation of data and indirect evidence, for example, the rise in predator numbers cannot be directly attributed to the increase in rodent populations, which is only a reflection of the epigenetic data and does not exclude the analysis of the correlation of other factors. Various factors such as climate change, human disturbance, disease, etc. may have an impact on animal population sizes, but in the discussion it is more centered around the effects of seed abundance and changes in predator-prey populations. Also I noticed in the text that there is a difference in the response of different species to seed abundance, which is a very worthwhile point of discussion, but there is a lack of in-depth discussion and analysis in this area, and it is recommended that the authors explore the reasons for the differences in the responses of different species in more depth.

Author Response

This study collected and analyzed natural data from four consecutive years, which is a large amount of work, and the research content is somewhat appealing, but the angle of entry for the main idea of the article may be less than ideal, and the following are some of my modifications to this article, which I hope will be helpful to the authors:

1. The abstract section is overly descriptive about the study area, and it is recommended that this section be deleted. In addition, the abstract only mentions the three hypotheses and findings in the text, but does not reflect the research methodology, so it is recommended that the authors use concise text in the abstract to summarize the main research methodology in the text.

The abstract has just two sentences describing the focal species of study and these are essential.

Lines 25-27: Additional information on methodology has been added.

1. The article defines the rodents studied as seed predators versus small mammals, and I would suggest that the authors use one designation in the text if possible, standardizing on either seed predators or small mammals.

Small mammals standardized throughout the text as appropriate.

1. The main hypothesis of the article is that growth in plant production causes growth in the number of seed predators, which in turn leads to a rise in the number of predators, which in turn leads to a further decline in the number of seed predators. This is actually the role of upward and downward effects co-regulating in the ecosystem, but the preface of the article does not center on these two types of ecological effects. The preface gives too much background on the phenomenon of fruit abundance, but this does not seem to be ultimately relevant to the scientific question the article is trying to address. It is recommended that the authors reorganize the logic of the preface by simplifying the first five paragraphs to two or three paragraphs with a brief text about climate change affecting fruit production and thus ecological effects on organisms at higher trophic levels. In addition, it is recommended that the preface focus on the ecological role of upward and downward effects, which in turn introduces the main research thrust of the paper.

Lines 84-96:  Introduction revised in accordance with these comments.

1. The Methods section is overly cluttered; the article begins with an introduction to the study area, but there is still more text about the study area in subsequent paragraphs.The title of 2.2 looks like a design total of the research methodology for the full text, but the actual content is a delineation of the study area, and it is recommended that the authors revise the subheading of 2.2.The content of Demographic Analysis looks like it should be categorized under Data Analysis. In general, it is recommended that the authors reorganize the text in the Methods section according to the logic of Vegetation Data Collection - Animal Data Collection - Measurement of Relevant Indicators - Data Analysis.

One sub-heading 2.1. is now used for this section. The other subheadings are appropriate as is.

1. Table 2 of the results contains too much data, which makes it difficult to visualize the important contents, so it is suggested that the authors can choose only the important data contents to be reflected in the text, and the complete charts can be put in the annex. In addition, this kind of continuous change data can be more intuitively reflected by using visual pictures to show the trend of change in different years, and it is suggested that the authors can consider selecting important indicators and reflecting this part of the data in the form of line graphs.

Table 2 has been revised to include only the important components. Mean abundance is shown visually in Figs. 1-3. Demographic variables followed the same pattern as abundance for P. maniculatus and M. gapperi.

1. In section 3.2 of the results, it is mentioned that the high occurrence of predators led to a decrease in the density of flowerback rats, and in 3.5 it is mentioned that the change in the number of predators could be due to an increase in the number of rats. There are many factors affecting wildlife populations, such as climate change, food changes, etc. Because the authors' methodology does not mention strict control variables, it is difficult to attribute the decline in rodent populations to predators or changes in predators due to changes in prey.

Not sure where “flowerback rats” come from in this comment? The premise of the manuscript is our prediction that masting of coniferous trees, ostensibly caused by a heat wave event, led to high populations of seed-eating rodents which in turn stimulated an increase in weasel predation. This pulsed resource (conifer seed) appeared to elicit a bottom-up effect (rodent seed predators) that was accompanied by a top-down trophic cascade (mustelid predation).   

1. In the results section of the article, the authors will explain some of the results, but it should be in the discussion section, and it is recommended that the authors simplify some of the text of the results, and visualize the changes in the data and the correlation between the various types of data more visually in the results section.

To assist with clarification of results, original Figs. 4-6 have been deleted. Text has been reduced wherever possible. Changes in mean abundance for major small mammal species, total of all species, and activity of mustelids are shown visually in Figs. 1-3 and new 4-6, respectively.

1. There is a lot of text in the discussion, but the discussion as a whole does not go far enough. The authors in the text mention three hypotheses and claim that they are partially supported, but based on the results of the analysis, I think the authors' validation mainly relies on observation of data and indirect evidence, for example, the rise in predator numbers cannot be directly attributed to the increase in rodent populations, which is only a reflection of the epigenetic data and does not exclude the analysis of the correlation of other factors. Various factors such as climate change, human disturbance, disease, etc. may have an impact on animal population sizes, but in the discussion it is more centered around the effects of seed abundance and changes in predator-prey populations. Also I noticed in the text that there is a difference in the response of different species to seed abundance, which is a very worthwhile point of discussion, but there is a lack of in-depth discussion and analysis in this area, and it is recommended that the authors explore the reasons for the differences in the responses of different species in more depth.

Lines 577-597: We provide three caveats to rationalize our partial support for H₂ that the increased presence of mustelids would follow high populations of small mammal prey, and mustelid predation would result in a decline in small mammals in 2024.

Lines 606-609: It may also be possible that other predator species such as hawks and owls may have contributed to the decline in prey numbers at our two study areas in the overwinter of 2023-24 and summer 2024. However, we do not have any data on these other predators to support or refute this explanation.

 

Lines 520-525: Abundance of N. amoenus may have been slightly enhanced in 2023 by availability of coniferous seed. N. amoenus has general affinity for early successional habitats, edges, strips of residual forest, and “open” thinned stands in managed landscapes (12,75). In general, chipmunk (Tamias, Neotamias) species are not common in managed second-growth and uncut mature-older coniferous forests with reduced understory shrub cover (76,77).

Round 2

Reviewer 1 Report

Comments and Suggestions for Authors

The new version of the document is a great improvement. I only have some minor comments.

• I authors measured an index of the activity of mustelid predators in the forests. However, they refer to this measurement as presence. I find this problematic because presence-absence is a binary measurement, whereas the measurement of activity is not.
• I still think that figures should be more informative and should indicate which comparisons were significantly different.
• Line 299. Alfa, not p, corresponds to the level of significance.

Author Response

The new version of the document is a great improvement. I only have some minor comments.

• Authors measured an index of the activity of mustelid predators in the forests. However, they refer to this measurement as presence. I find this problematic because presence-absence is a binary measurement, whereas the measurement of activity is not.

Lines 21, 114, 123, 234-236, 285, 287, 290, 458, 461, 466, 558, 565, 570, 632. The term “presence” has been replaced with “activity”.

• I still think that figures should be more informative and should indicate which comparisons were significantly different.

All figures have been revised accordingly.

• Line 299. Alfa, not p, corresponds to the level of significance.

This is the correct description and has been used in all of our publications: the level of significance was at p = 0.05.