Effect of Honey Bee Colony Strength on Foraging Productivity and Its Application to Precision Pollination

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

This is a very practical and useful study evident that stronger colonies have higher weight gains compared to weaker colonies, which benifit pollination either in pollination  or honey harvest season in beekeeping. Moreover, during periods of nectar dearth, strong colonies exhibited lower weight losses than the weak colonies, making them more efficient under resource limited conditions. This could happen in overwinter days, according to our beekeepers here, 

Simple Summary and Abstract: They were well organized and written with research aims and results. But the number of  key words should be no more than five, and I suggest them as: Honey bees; colony strength; foraging productivity; pollination efficiency; precision pollination.

Introduction

Now I found this part is too long and it needs to make it concise especially at the first 4 paragraphs. I would rather to convey the importance/value of honey bee pollination in agriculture and introduction to the challenge in bee pollination this field in the beginning.

Next (the 5th paragraph in original ms),  I agreed that the authors begined to focus on the research question-how colony performance scales with strength, environmental conditions, genetics, and management practices.

Materials and Methods

As the strong and weak colony strengths, how do you measure/scale them? Did you open the hive and check the bees?

Results

As to address the strong colony has better pollination capacity, it is necessary to make sure all gained weights are from the target plants (any non-target plants bloom at the same time? I suggest they add some information for this, for instance, they chcked the ).

 It makes sense that strong strength colonies have better productivity, but it does not mean they have better pollination capacity in target plants. For example, you need to make sure both the strong and the weak colonies only forage on sweet chestnuts, then you can compare the weight gains(pollination precision ) between the strong/weak colonies.

Author Response

Reviewer 1

Comment 1: This is a very practical and useful study evident that stronger colonies have higher weight gains compared to weaker colonies, which benifit pollination either in pollination  or honey harvest season in beekeeping. Moreover, during periods of nectar dearth, strong colonies exhibited lower weight losses than the weak colonies, making them more efficient under resource limited conditions. This could happen in overwinter days, according to our beekeepers here
Response 1: We thank the Reviewer 1 for the positive and encouraging evaluation of our manuscript. We appreciate the reviewer's constructive comments and suggestions which have helped us to improve the clarity and interpretation of the study. All comments have been carefully addressed, as detailed below.

Comment 2: Simple Summary and Abstract: They were well organized and written with research aims and results. But the number of  key words should be no more than five, and I suggest them as: Honey bees; colony strength; foraging productivity; pollination efficiency; precision pollination.
Response 2: Many thanks for this helpful suggestion. The keywords have now been revised as suggested. 

Comment 3: Introduction
Now I found this part is too long and it needs to make it concise especially at the first 4 paragraphs. I would rather to convey the importance/value of honey bee pollination in agriculture and introduction to the challenge in bee pollination this field in the beginning.
Next (the 5th paragraph in original ms),  I agreed that the authors begined to focus on the research question-how colony performance scales with strength, environmental conditions, genetics, and management practices.
Response 3: The reviewer evaluation of the introduction is much appreciated. The Introduction was refined to improve focus and with clearer emphasis on the importance and challenges of honey bee pollination at the beginning of the section. We agree that the length of this section is considerable, however, as this manuscript is submitted to a Special Issue focused on pollination, our aim was to provide a comprehensive background that situates the study within the broader context of pollination services, colony performance as well as applied beekeeping. We believe that this level of detail is appropriate for the readership of the Special Issue. 

Comment 4: Materials and Methods
As the strong and weak colony strengths, how do you measure/scale them? Did you open the hive and check the bees?
Response 4: In this study, colony strength was evaluated using two methods, as described in the Materials and Methods section. In both cases, hives were opened and frames were removed for visual assessment of adult bee population, brood area, and pollen and honey stores. Specifically, one approach followed the Liebefeld method, which provides a more detailed and repeatable assessment of colony strength and offers a good balance between speed and accuracy. The second approach consisted of a standard beekeeper inspection, which is faster and more approximate but commonly used in practical beekeeping and pollination service provision. This distinction between the two methods has now been clarified in the revised manuscript.

Comment 5: Results
As to address the strong colony has better pollination capacity, it is necessary to make sure all gained weights are from the target plants (any non-target plants bloom at the same time? I suggest they add some information for this, for instance, they chcked the ).
Response 5: We appreciate the question raised regarding the origin of colony weight gains. In the Italian study sites, the target plants (Robinia pseudoacacia and Castanea sativa) flowered at distinct, temporally separated periods. These are mass flowering forage crops that honey bees are very well adapted at exploiting. The contribution of the target plants was verified through analysis of organoleptic characteristics (e.g., colour, aroma, and crystallisation behaviour) of the harvested honey, and beekeeper experience, which confirmed that honey production was derived from the target plants (e.g., Robinia pseudoacacia and Castanea sativa). In the California study system, colonies were placed in a predominantly monoculture agricultural landscape. While alternative floral resources were present in 2023, these did not overlap temporally with the almond bloom. Thus, foraging activity and associated weight gains during the study period can be attributed primarily to the target crop (Prunus dulcis).This information has now been clarified in the revised manuscript to strengthen the interpretation of the results.

Comment 6: It makes sense that strong strength colonies have better productivity, but it does not mean they have better pollination capacity in target plants. For example, you need to make sure both the strong and the weak colonies only forage on sweet chestnuts, then you can compare the weight gains(pollination precision ) between the strong/weak colonies.
Response 6: We agree with the reviewer that increased colony productivity does not automatically imply improved pollination capacity unless foraging is directed toward the target crop. As clarified above, both weak and strong colonies produced honey derived from the target plants in the Italian sites, and colonies in California foraged exclusively on the target crops due to the monoculture setting. We have revised the Results and Discussion sections to make this distinction explicit and to avoid overgeneralisation of pollination efficiency beyond the study context.

Reviewer 2 Report

Comments and Suggestions for Authors

            The article “Effect of Honey Bee Colony Strength on Foraging Productivity and Its Application to Precision Pollination” is a good contribution especially to the study of the strength of the colonies of honey bees as important factor of efficient pollination.

            Keywords are a little too many, maybe they can be reduced to be more concise.

            The introduction is well done, with correct overview on the subject.

            Material and methods are accurate, with the descriptions of the study sites locations, the electronic equipment used, the statistical analysis etc.

            Results are concise, with many but well-done graphics and one table.

            Discussions and conclusions are a good summarising on the subject, with the correct comparations with other data from literature.

            References are accurate realised.

            Some other comments and small corrections are on the attached manuscript.

            The paper can be published with some minor revision.

Comments for author File: Comments.pdf

Author Response

Reviewer 2

General comments: The article “Effect of Honey Bee Colony Strength on Foraging Productivity and Its Application to Precision Pollination” is a good contribution especially to the study of the strength of the colonies of honey bees as important factor of efficient pollination.

Keywords are a little too many, maybe they can be reduced to be more concise.

The introduction is well done, with correct overview on the subject.

Material and methods are accurate, with the descriptions of the study sites locations, the electronic equipment used, the statistical analysis etc.

Results are concise, with many but well-done graphics and one table.

Discussions and conclusions are a good summarising on the subject, with the correct comparations with other data from literature.

References are accurate realised.

Some other comments and small corrections are on the attached manuscript.

The paper can be published with some minor revision.

 

General response: We thank the Reviewer 2 for the positive appraisal of the manuscript and the valuable comments and corrections. 

Comment 1: A little to much keywords, try be more concise
Response 1: We thank the reviewer for bringing this up, we have revised the keywords and reduced the number while retaining the key topics of the study. 

Reviewer 3 Report

Comments and Suggestions for Authors

Dear authors, 

this manuscript is very well written; minor comments in the attached document.

Comments for author File: Comments.pdf

Author Response

Reviewer 3

General comments: Dear authors, 
this manuscript is very well written; minor comments in the attached document.
General response: We thank Reviewer 3 for the positive evaluation of our manuscript and for the constructive comments provided. We greatly appreciate the reviewer’s careful reading of the manuscript, and we have addressed all comments below, using them to revise and improve the manuscript.

Comment 1: Reason for not including Russian and Pol-Line in 2024?
Response 1: We thank the reviewer for this question. While inclusion of Russian and Pol-Line colonies in the 2024 study would indeed have been desirable, these genetic lines were not available to us during that season. The study site and experimental setup were maintained, but the availability of specific bee stocks varied between years.

Comment 2: Why is this not aligned with any of the montioring periods in 2024?
Response 2: The in-field sensors are powered by specialised batteries with a limited operational lifespan. For this reason, sensors were deployed during the most critical period of interest, namely the almond bloom, to maximise data quality during peak pollination activity. This has now been clarified in the manuscript.

Comment 3: Assessments were performed at the beginning and the end of the study too?
Response 3: We thank the reviewer for pointing this out. Yes, colony strength assessments in the 2024 study were performed at both the beginning and the end of the study period. This has now been clarified in the Materials and Methods section.

Comment 4: Did you account for entrance orientation at all, since you specifically mentioned it in the previous section?Response 4: Hive entrance orientation was not included as a fixed-effect in the present analysis. We have previously published a dedicated study examining the effects of hive orientation on honey bee activity during almond pollination. In the Italian studies, all hives were oriented identically, and therefore orientation did not vary among colonies and could not be included as an explanatory factor. 

Comment 5: How come, in 2023 there was alternative forage after the almond bloom while there was a nectar dearth in 2024?
Response 5: The presence of alternative forage following almond bloom in 2023 was a result of agricultural management decisions on the surrounding farms and was outside the control of the study design. In 2023 neighbouring landowners established flowering cover crops that provided additional forage for honey bees. In contrast, in 2024 the same fields were planted with crops (onions) that did not provide floral resources during the study period, resulting in a pronounced post-bloom forage dearth. This contextual difference has now been clarified in the manuscript.

Comment 6: Typo in "Weight" in panel B
Comment 6: We thank the reviewer for noting this. It has now been corrected. 

Comment 7: This is misleading, as you were using different methods to estimate colony size (Liebefeld and quick inspection)
Response 7: We agree with the reviewer’s remark. We have revised the wording in the Discussion to clarify that colony strength was assessed using standard methods, rather than a single method, to avoid ambiguity.

Reviewer 4 Report

Comments and Suggestions for Authors

This is a worthwhile study. It is mostly clear and readable. Some punctuation needs improved throughout.

Methods- there is some inconsistency in the way key terms are given in different places, e.g. “unselected stock”- the capitalisation varies.

Some clarifications are needed also. In section 2.1, some text at the end would be helpful to summarise what the four trials are. The way the material is presented in this section could be clearer. Some reorganisation could make it clearer- see my comment on the text.

Section 2.3, line 208: what did you do if FOB was exactly equal to the median? Please add this.

Section 2.4, line 222: please make it clear what you mean by “ratio-variance artefacts”.

Results- various minor issues are noted on the text. The main issue is the need for correction of figure labelling: “strength” is misspelled in numerous places- Fig 3 A, B, E and Fig 7 A.

Section 3.4, line 347: please clarify “landraces”.

Table 1: please define efficiency in the legend or footnote, and clarify why there is a z value as well as a U statistic. Also in the z values sometimes a decimal point is used and sometimes a comma.

Discussion is long. I suggest using some headings to break it up.

The conclusions seem appropriate.

References – some tidying is required. Some start with a comma or full stop for example. Please check and tidy them.

Please see the annotated document for these and various suggested edits, mainly minor ones. 

Comments for author File: Comments.pdf

Comments on the Quality of English Language

Please see points marked on the text.

Author Response

Reviewer 4

General comments: This is a worthwhile study. It is mostly clear and readable. Some punctuation needs improved throughout.
General response: We thank the Reviewer 4 for their attentive reading of the manuscript and subsequently for the many useful comments and suggested edits. We have addressed all points raised and believe the revisions have improved the clarity and readability of the manuscript. Detailed responses to each comment are provided below.
We agree that some punctuation and formatting issues required attention. These have been corrected throughout the manuscript, including typographical errors, spacing, punctuation and reference formatting, as noted in the annotated manuscript.

Comment 1: Methods- there is some inconsistency in the way key terms are given in different places, e.g. “unselected stock”- the capitalisation varies.
Response 1: We have standardised the use and capitalisation of term “unselected stock” throughout the manuscript to ensure consistency.

Comment 2: Some clarifications are needed also. In section 2.1, some text at the end would be helpful to summarise what the four trials are. The way the material is presented in this section could be clearer. Some reorganisation could make it clearer- see my comment on the text.
Response 2:In Section 2.1, we have added text to explicitly summarise the four studies. and to make clear how they differ by year, location, and crop. The flow of this section has been revised to improve clarity and organisation, following the reviewer’s suggestion.

Comment 3: Section 2.3, line 208: what did you do if FOB was exactly equal to the median? Please add this.
Response 3: In Section 2.3, we have clarified how colonies were classified when Frames of Bees (FOB) values were equal to the median, and now explicitly state the rule applied in these cases.

Comment 4: Section 2.4, line 222: please make it clear what you mean by “ratio-variance artefacts”.
Response 4: In Section 2.4, we have clarified the meaning of “ratio-variance artefacts” by briefly explaining that these arise from variability in the denominator (FOB), which can artificially increase variance and affect the interpretation of group differences.

Comment 5: Results- various minor issues are noted on the text. The main issue is the need for correction of figure labelling: “strength” is misspelled in numerous places- Fig 3 A, B, E and Fig 7 A.
Response 5: We have addressed the minor issues noted in the text, including punctuation and wording corrections. The misspelling of “strength” in Figures 3 and 7 has been corrected, and figure labels have been carefully checked for consistency.

Comment 6: Section 3.4, line 347: please clarify “landraces”.
Response 6: We are thankful to the reviewer for bring this up. In Section 3.4 we have clarified terminology by replacing “landraces” with “locally adapted chestnut varieties” to better reflect the biological and management context of the study area.

Comment 7: Table 1: please define efficiency in the legend or footnote, and clarify why there is a z value as well as a U statistic. Also in the z values sometimes a decimal point is used and sometimes a comma.
Response 7: We have clarified how efficiency is calculated in the Table 1 footnote, defining it as the ratio of mean weight gain per unit colony strength (kg FOB⁻¹) in Strong colonies relative to Weak colonies within each study period. We have also clarified why both the Mann–Whitney U statistic and the corresponding standardised z value are reported, and standardised numerical formatting to use decimal points consistently throughout the table.

Comment 8: Discussion is long. I suggest using some headings to break it up.
Response 8: We agree with the reviewer’s comment and In response we have added thematic subheadings to the Discussion section to improve readability and to help guide the reader through the main topics addressed.

The conclusions seem appropriate.

Comment 9: References – some tidying is required. Some start with a comma or full stop for example. Please check and tidy them.
Response 9 We have checked and tidied the reference list throughly as well as addressed some inconsistencies in formatting. 

Comment 10: Please see the annotated document for these and various suggested edits, mainly minor ones. 
Response 10: From the comments in manuscript following actions were taken: 

1. Line 24 added ’ to beekeepers
2. Line 25 added comma 
3. Line 31 added a 
4. Line 46 and 47 keywords revised 
5. Line 72 added comma 
6. Unselected stock consistency on lines 139, 144 , revised and corrected throughout the document
7. Materials and Methods study sites define the four studies and reorganise the flow
   We have addressed this explicitly. 
8. Line 171 inserted full stop 
9. Line 206 inserted and 
10. Line 207 Were any equal to the median? If so, what did you do?
    We have clarified the classification rule in the manuscript and now explicitly state how colonies with FOB values equal to the median were assigned. 
11. Line 222 can you make it clearer what you mean by "ratio-variance artefacts”
    We have clarified what is meant by ratio-variance artefacts by briefly explaining that these arise from variability in the denominator (FOB), which can inflate variance and bias statistical comparisons. 
12. Line 239 add s to almond 
13. Line 255 as point 6 stock vs Stock 
14. Line 259 added and and space 
15. Figure 3 corrected spelling of strength 
16. Line 267 added comma
17. Line 274 added s almond
18. Line 278 added comma 
19. Line 291 removed unnecessary full stop 
20. Line 298 insert a before weak 
21. Line 299 moved the full stop to the end of the sentence 
22. Figure 7 corrected spelling of strength
23. Line 309 removed full stop from figure 
24. Line 317 removed full stop 
25. Line 320  corrected were instead of where
26. Line 322 inserted brackets 
27. Line 347 landraces definition
    We thank the reviewer for this comment. To improve clarity, we have replaced “landraces” with “locally adapted chestnut varieties” in the manuscript. 
28. Line 367 inserted compared to 
29. Line 379 deleted with 
30. Line 384 added full stop
31. Line 385 corrected 1 to 7 June
32. Line 393 inserted study
33. can you indicate how Efficiency is calculated her or in the footnote; also why do you have a z value as well as a Mann-Whitney statistic? Also sometimes in  the Z column you use a decimal point and sometimes a comma.
    We thank the reviewer for these comments. We have clarified in the Table 1 footnote how efficiency was calculated (as the ratio of mean weight gain per unit colony strength, kg FOB⁻¹, in Strong colonies relative to Weak colonies within each study period). We also clarified the reporting of the Mann–Whitney U statistic together with the corresponding standardised z value and associated two-tailed p value. Finally, we standardised numerical formatting throughout the table to use decimal points consistently. X
34. Discussion The discussion is long. Can some headings be used to make it easier to navigate?
    We have added subheadings to the discussion which has improved the readability of the section.
35. please check the formatting of all of these references - some begin with a full stop or a comma, for example
    we have throughly revised the references and corrected the formatting, punctuation and consistency as well as validity of DOIs.

Round 2

Reviewer 4 Report

Comments and Suggestions for Authors

The authors have attended carefully to the requested changes and I think that the paper has improved. 

In Methods, section 2.1, at the end of paragraph 4 beginning "In 2024,"  I suggest adding a citation to the previous study now referred to, which should be possible at the proof stage as I think the previous study is already referenced elsewhere.