Author response:
We thank all reviewers for the highly detailed review and the time and effort which has been invested in this review. We have read their perspectives, questions and suggested improvements with great interest. We have reflected on the public review in detail and have made the first provisional responses which are outlined below. First, we would like to respond to four main issues pointed out by the editor and reviewers:
(1) Lack of yield data in the manuscript: There have been yield data collected in most of the sites and years of our study, and these have already been published and cited in our manuscript. In the appendix of our manuscript, we included a table with yield data for the sites and years in which the beetle diversity was studied. These data show that strip cropping does not cause a systematic yield reduction.
(2) Sampling design clarification: Our paper combines data from trials conducted at different locations and years. On the one hand this allows an analysis of a comprehensive dataset, but on the other hand in some cases there were slight inconsistencies in how data were collected or processed (e.g. taxonomic level of species identification). We will explain the sampling design and data analysis in more detail to increase clarity and transparency.
(3) Additional data analysis: In the revised manuscript we will present an analysis on the responses of abundances of the 12 most common ground beetle genera to strip cropping. This will give better insight of the variation in responses among ground beetle taxa.
(4) Restrict findings to our system: We will nuance our findings further and will focus more strongly on the implications of our data on ground beetle communities, rather than on agrobiodiversity in a broader sense.
We will further work on improving the manuscript based on reviewers feedback in the coming weeks, aiming to submit a revised version of the manuscript at the end of February.
Detailed response to editor and reviewers:
Editor Comments:
(1) You only have analyzed ground beetle diversity, it would be important to add data on crop yields, which certainly must be available (note that in normal intercropping these would likely be enhanced as well).
Most yield data have been published in three previous papers, which we already cited or will cite (one was not yet published at the time of submission). Our argumentation is based on these studies. We had also already included a table in the appendix that showed the yield data that relates specifically to our locations and years of measurement. The finding that strip cropping does not majorly affect yield is based on these findings. We will consider changing the title of our manuscript to remove the explicit focus on yield.
(2) Considering the heterogeneous data involving different experiments it is particularly important to describe the sampling design in detail and explain how various hierarchical levels were accounted for in the analysis.
We agree that some important details to our analysis were not described in sufficient detail. Especially reviewer 2 pointed out several relevant points that we did account for in our analyses, but which were not clear from the text in the methods section. We are convinced that our data analyses are robust and that our conclusions are supported by the data. We will revise the methods section to make our approach clearer and more transparent.
(3) In addition to relative changes in richness and density of ground beetles you should also present the data from which these have been derived. Furthermore, you could also analyze and interpret the response of the different individual taxa to strip cropping.
With our heterogeneous dataset it was quite complicated to show overall patterns of absolute changes in ground beetle abundance and richness, especially for the field-level analyses. As the sampling design was not always the same and occasionally samples were missing, the number of year series that made up a datapoint were different among locations and years. However, we always made sure that for the comparison of a paired monoculture and strip cropping field, the number of year series was always made equal through rarefaction. That is, the number of ground beetle(s) (species) are always expressed as the number per 2 to 6 samples. Therefore, we prefer to stick to relative changes as we are convinced that this gives a fairer representation of our complex dataset.
We agree with the second point that both the editor and several reviewers pointed out. The indicator species analyses that we used were biased by rare species, and we now omit this analysis. Instead, we will include a GLM analysis on the responses of abundances of the 12 most common ground beetle genera to strip cropping. We chose for genera here (and not species) as we could then include all locations and years within the analysis, and in most cases a genus was dominated by a single species (but notable exceptions were Amara and Harpalus, which were made up of several species). We will illustrate these findings still in a similar fashion as we did for the indicator species analysis.
(4) Keep to your findings and don't overstate them but try to better connect them to basic ecological hypotheses potentially explaining them.
After careful consideration of the important points that reviewers point out, we decided to nuance our points about biodiversity conservation along two key lines: (1) the extent to which ground beetles can be indicators of wider biodiversity changes; and (2) our findings that are not as straightforward positive as our narrative suggests. We still believe that strip cropping contributes positively to carabid communities, and will carefully check the text to avoid overstatements.
Reviewer 1:
Summary:
This study demonstrates that strip cropping enhances the taxonomic diversity of ground beetles across organically-managed crop systems in the Netherlands. In particular, strip cropping supported 15% more ground beetle species and 30% more individuals compared to monocultures.
Strengths:
A well-written study with well-analyzed data of a complex design. The data could have been analyzed differently e.g. by not pooling samples, but there are pros and cons for each type of analysis and I am convinced this will not affect the main findings. A strong point is that data were collected for 4 years. This is especially strong as most data on biodiversity in cropping systems are only collected for one or two seasons. Another strong point is that several crops were included.
We thank reviewer 1 for their kind words and agree with this strength of the paper. The paper combines data from trials conducted at different locations and years. On the one hand this allows an analysis of a comprehensive dataset, but on the other hand in some cases there were slight inconsistencies in how data were collected or processed (e.g. taxonomic level of species identification).
Weaknesses:
This study focused on the biodiversity of ground beetles and did not examine crop productivity. Therefore, I disagree with the claim that this study demonstrates biodiversity enhancement without compromising yield. The authors should present results on yield or, at the very least, provide a stronger justification for this statement.
We acknowledge that we indeed did not formally analyze yield in our study, but we have good reason for this. The claim that strip cropping does not compromise yield comes from several extensive studies (Juventia et al., 2024; Ditzler et al., 2023; Carillo-Reche et al., 2023) that were conducted in nearly all the sites and years that we included in our study. We chose not to include formal analyses of productivity for two key reasons: (1) a yield analysis would duplicate already published analyses, and (2) we prefer to focus more on the ecology of ground beetles and the effect of strip cropping on biodiversity, rather than diverging our focus also towards crop productivity. Nevertheless, we have shown the results on yield in Table S6 and refer extensively to the studies that have previously analyzed this data.
Reviewer 2:
Summary:
The authors aimed to investigate the effects of organic strip cropping on carabid richness and density as well as on crop yields. They find on average higher carabid richness and density in strip cropping and organic farming, but not in all cases.
Strengths:
Based on highly resolved species-level carabid data, the authors present estimates for many different crop types, some of them rarely studied, at the same time. The authors did a great job investigating different aspects of the assemblages (although some questions remain concerning the analyses) and they present their results in a visually pleasing and intuitive way.
We appreciate the kind words of reviewer 2 and their acknowledgement of the extensiveness of our dataset. In our opinion, the inclusion of many different crops is indeed a strength, rarely seen in similar studies; and we are happy that the figures are appreciated.
Weaknesses:
The authors used data from four different strip cropping experiments and there is no real replication in space as all of these differed in many aspects (different crops, different areas between years, different combinations, design of the strip cropping (orientation and width), sampling effort and sample sizes of beetles (differing more than 35 fold between sites; L 100f); for more differences see L 237ff). The reader gets the impression that the authors stitched data from various places together that were not made to fit together. This may not be a problem per se but it surely limits the strength of the data as results for various crops may only be based on small samples from one or two sites (it is generally unclear how many samples were used for each crop/crop combination).
The paper indeed combines data from trials conducted at different locations and years. On the one hand this allows an analysis of a comprehensive dataset, but on the other hand in some cases there were slight differences in the experimental design. At the time that we did our research, there were only a handful of farmers that were employing strip cropping within the Netherlands, which greatly reduced the number of fields for our study. Therefore, we worked in the sites that were available and studied as many crops on these sites. Since there was variation in the crops grown in the sites, for some crops we have limited replication. In the revision we will explain this more clearly.
One of my major concerns is that it is completely unclear where carabids were collected. As some strips were 3m wide, some others were 6m and the monoculture plots large, it can be expected that carabids were collected at different distances from the plot edge. This alone, however, was conclusively shown to affect carabid assemblages dramatically and could easily outweigh the differences shown here if not accounted for in the models (see e.g. Boetzl et al. (2024) or Knapp et al. (2019) among many other studies on within field-distributions of carabids).
Point well taken and we will present a more detailed description of the sampling design in the methods. Samples were always taken at least 10 meters into the field, and always in the middle of the strip. This would indeed mean that there is a small difference between the 3- and 6m wide strips regarding distance from another strip, but this was then only a difference of 1.5 to 3 meters from the edge. A difference that, based on our own extensive experience with ground beetle communities, will not have a large impact on the findings of ground beetles. The distance from field/plot edges was similar between monocultures and strip cropped fields.
The authors hint at a related but somewhat different problem in L 137ff - carabid assemblages sampled in strips were sampled in closer proximity to each other than assemblages in monoculture fields which is very likely a problem. The authors did not check whether their results are spatially autocorrelated and this shortcoming is hard to account for as it would have required a much bigger, spatially replicated design in which distances are maintained from the beginning. This limitation needs to be stated more clearly in the manuscript.
This is a limitation that is hard to avoid in comparisons between strip cropping and monoculture systems because the use of a statistically robust design with sufficient replication and still using field sizes that are representative for farming practice are often not possible. We will acknowledge this limitation in the revised manuscript. To allow a fair comparison based on sufficient number of replications, we chose to combine data from several years and locations (despite this not being the ideal experimental design). This approach has the drawback that ground beetle communities are difficult to compare. Therefore, we chose to further investigate two years of data from Wageningen as the factorial design allowed a fair comparison between monocultures and strip cropping. We analyzed three crop combinations during two years, but we still cannot exclude a potential influence of spatial autocorrelation. We acknowledged this limitation in our original submission, and we will clarify this point further in the revision.
Similarly, we know that carabid richness and density depend strongly on crop type (see e.g. Toivonen et al. (2022)) which could have biased results if the design is not balanced (this information is missing but it seems to be the case, see e.g. Celeriac in Almere in 2022).
The samples size ranges between 2 and 6 per combination of cropping design, crop, location and year. We believe that this will allow a meaningful analysis. Moreover, our main focus is the comparison between monoculture and strip cropping, and not the comparison between different crops. Even though we show that crop types have different ground beetle communities, we are most interested in the contrast of ground beetle communities in strip cropping and monoculture systems.
A more basic problem is that the reader neither learns where traps were located, how missing traps were treated for analyses how many samples there were per crop or crop combination (in a simple way, not through Table S7 - there has to have been a logic in each of these field trials) or why there are differences in the number of samples from the same location and year (see Table S7). This information needs to be added to the methods section.
Point well taken. We will clarify this further in the revised manuscript. As we combined data from several experimental designs that originally had slightly different research questions, this in part caused differences between numbers of rounds or samples per crop, location or year.
As carabid assemblages undergo rapid phenological changes across the year, assemblages that are collected at different phenological points within and across years cannot easily be compared. The authors would need to standardize for this and make sure that the assemblages they analyze are comparable prior to analyses. Otherwise, I see the possibility that the reported differences might simply be biased by phenology.
We agree and we dealt with this issue by using year series instead of using individual samples of different rounds. While this approach is not perfect, it allows us to get the best possible impression of the entire ground beetle community across seasons. For our analyses we had the choice to only include data from sampling rounds that were conducted at the same time, or to include all available data. We chose to analyze all data, and made sure that the number of samples between strip cropping and monoculture fields per location, year and crop was always the same by pooling and rarefaction. In this way we have analyzed a complex multi-year, multi-crop and multi-location dataset as good as we could.
Surrounding landscape structure is known to affect carabid richness and density and could thus also bias observed differences between treatments at the same locations (lower overall richness => lower differences between treatments). Landscape structure has not been taken into account in any way.
We did not include landscape structure as there are only 4 sites, which does not allow a meaningful analysis of potential effects landscape structure. Studying how landscape interacts with strip cropping to influence insect biodiversity would require at least, say 15 to 20 sites, which was not feasible for this study. However, such an analysis may be possible in an ongoing project (CropMix) which includes many farms that work with strip cropping.
In the statistical analyses, it is unclear whether the authors used estimated marginal means (as they should) - this needs to be clarified.
In the revised manuscript we will further clarify this point.
In addition, and as mentioned by Dr. Rasmann in the previous round (comment 1), the manuscript, in its current form, still suffers from simplified generalizations that 'oversell' the impact of the study and should be avoided. The authors restricted their analyses to ground beetles and based their conclusions on a design with many 'heterogeneities' - they should not draw conclusions for farmland biodiversity but stick to their system and report what they found. Although I understand the authors have previously stated that this is 'not practically feasible', the reason for this comment is simply to say that the authors should not oversell their findings.
In the revised manuscript, we will nuance our findings by explaining that strip cropping is a potentially useful tool to support ground beetle biodiversity in agricultural fields, but the effects on other taxa still needs to be further explored.
Reviewer 3:
Summary:
In this paper, the authors made a sincere effort to show the effects of strip cropping, a technique of alternating crops in small strips of several meters wide, on ground beetle diversity. They state that strip cropping can be a useful tool for bending the curve of biodiversity loss in agricultural systems as strip cropping shows a relative increase in species diversity (i.e. abundance and species richness) of the ground beetle communities compared to monocultures. Moreover, strip cropping has the added advantage of not having to compromise on agricultural yields.
Strengths:
The article is well written; it has an easily readable tone of voice without too much jargon or overly complicated sentence structure. Moreover, as far as reviewing the models in depth without raw data and R scripts allows, the statistical work done by the authors looks good. They have well thought out how to handle heterogenous, yet spatially and temporarily correlated field data. The models applied and the model checks performed are appropriate for the data at hand. Combining RDA and PCA axes together is a nice touch.
We thank reviewer 3 for their kind words and appreciation for the simple language and analysis that we used.
Weaknesses:
The evidence for strip cropping bringing added value for biodiversity is mixed at best. Yes, there is an increase in relative abundance and species richness at the field level, but it is not convincingly shown this difference is robust or can be linked to clear structural and hypothesised advantages of the strip cropping system. The same results could have been used to conclude that there are only very limited signs of real added value of strip cropping compared to monocultures.
Point well taken. We agree that the effect of strip cropping on carabid beetle communities are subtle and we will nuance the text in the revised version to reflect this.
There are a number of reasons for this:
(1) Significant differences disappear at crop level, as the authors themselves clearly acknowledge, meaning that there are no differences between pairs of similar crops in the strip cropping fields and their respective monoculture. This would mean the strips effectively function as "mini-monocultures".
This is indeed in line with our conclusions. Based on our data and results, the advantages of strip cropping seem mostly to occur because crops with different communities are now on a same field, rather than that within the strips you get mixtures of communities related to different crops. We discussed this in the first paragraph of the discussion in the original submission.
The significant relative differences at the field level could be an artifact of aggregation instead of structural differences between strip cropping and monocultures; with enough data points things tend to get significant despite large variance. This should have been elaborated further upon by the authors with additional analyses, designed to find out where differences originate and what it tells about the functioning of the system. Or it should have provided ample reason for cautioning in drawing conclusions about the supposed effectiveness of strip cropping based on these findings.
We believe that this is a misunderstanding of our approach. In the field-level analyses we pooled samples from the same field (i.e. pseudo-replicates were pooled), resulting in a relatively small sample size of 50 samples. We will explain this better in the methods section. Therefore, the statement “with enough data points things tend to get significant” is not applicable here.
(2) The authors report percentages calculated as relative change of species richness and abundance in strip cropping compared to monocultures after rarefaction. This is in itself correct, however, it can be rather tricky to interpret because the perspective on actual species richness and abundance in the fields and treatments is completely lost; the reported percentages are dimensionless. The authors could have provided the average cumulative number of species and abundance after rarefaction. Also, range and/or standard error would have been useful to provide information as to the scale of differences between treatments. This could provide a new perspective on the magnitude of differences between the two treatments which a dimensionless percentage cannot.
We agree that this would be the preferred approach if we would have had a perfectly balanced dataset. However, this approach is not feasible with our unbalanced design and differences in sampling effort. While we acknowledge the limitation of the interpretation of percentages, it does allow reporting relative changes for each combination of location, year and crop. The number of samples on which the percentages were based were always kept equal (through rarefaction) between the cropping systems (for each combination of location, year and crop), but not among crops, years and location. The reason for this is that we did not always have an equal number of samples available between both cropping systems, and this approach allowed us to make a better estimation whenever more samples were available. For example, sometimes we had 2 samples from a strip cropped field and 6 from the monoculture, here we would use rarefaction up to 2 samples (where we would just have a better estimation from the monoculture). In other cases, we had 4 samples in both strip cropped and monoculture field, here we chose to use rarefaction to 4 samples to get a better estimation altogether. Adding a value for actual richness or abundance to the figures would have distorted these findings, as the variation would be huge (as it would represent the number of ground beetle(s) species per 2 to 6 pitfall samples). Furthermore, the dimension that reviewer 3 describes would thus be “The number of ground beetle species / individuals per 2 to 6 samples”, not a very informative unit either. We chose to trade-off better estimations of difference between cropping systems over a more readily interpretable unit.
(3) The authors appear to not have modelled the abundance of any of the dominant ground beetle species themselves. Therefore it becomes impossible to assess which important species are responsible (if any) for the differences found in activity density between strip cropping and monocultures and the possible life history traits related reasons for the differences, or lack thereof, that are found. A big advantage of using ground beetles is that many life history traits are well studied and these should be used whenever there is reason, as there clearly is in this case. Moreover, it is unclear which species are responsible for the difference in species richness found at the field level. Are these dominant species or singletons? Do the strip cropping fields contain species that are absent in the monoculture fields and are not the cause of random variation or sampling? Unfortunately, the authors do not report on any of these details of the communities that were found, which makes the results much less robust.
Thank you for raising this point. We have reconsidered our indicator species analysis and found that it is rather sensitive for rare species and insensitive for changes in common species. Therefore, we will replace the indicator species analyses with a GLM analysis for the 12 most common genera of ground beetles In the revised manuscript. This will allow us to go more in depth on specific traits of the genera which abundances change depending on the cropping system. In the revised manuscript, we will also discuss these common genera more in depth, rather than focusing on rarer species. Furthermore, we will add information on rarity and habitat preference to the table that shows species abundances per location (Table S2).
(4) In the discussion they conclude that there is only a limited amount of interstrip movement by ground beetles. Otherwise, the results of the crop-level statistical tests would have shown significant deviation from corresponding monocultures. This is a clear indication that the strips function more like mini-monocultures instead of being more than the sum of its parts.
This is in line with our point in the first paragraph of the discussion and an important message of our manuscript.
(5) The RDA results show a modelled variable of differences in community composition between strip cropping and monoculture. Percentages of explained variation of the first RDA axis are extremely low, and even then, the effect of location and/or year appear to peak through (Figure S3), even though these are not part of the modelling. Moreover, there is no indication of clustering of strip cropping on the RDA axis, or in fact on the first principal component axis in the larger RDA models. This means the explanatory power of different treatments is also extremely low. The crop level RDA's show some clustering, but hardly any consistent pattern in either communities of crops or species correlations, indicating that differences between strip cropping and monocultures are very small.
We agree and we make a similar point in the first paragraph of the discussion.
Furthermore, there are a number of additional weaknesses in the paper that should be addressed:
The introduction lacks focus on the issues at hand. Too much space is taken up by facts on insect decline and land sharing vs. land sparing and not enough attention is spent on the scientific discussion underlying the statements made about crop diversification as a restoration strategy. They are simply stated as facts or as hypotheses with many references that are not mentioned or linked to in the text. An explicit link to the results found in the large number of references should be provided.
We will streamline the introduction by omitting the land sharing vs. land sparing topic and better linking references to our research findings.
The mechanistic understanding of strip cropping is what is at stake here. Does strip cropping behave similarly to intercropping, a technique that has been proven to be beneficial to biodiversity because of added effects due to increased resource efficiency and greater plant species richness? This should be the main testing point and agenda of strip cropping. Do the biodiversity benefits that have been shown for intercropping also work in strip cropping fields? The ground beetles are one way to test this. Hypotheses should originate from this and should be stated clearly and mechanistically.
We agree with the reviewer and will clarify this research direction clearer in the introduction of the revised manuscript.
One could question how useful indicator species analysis (ISA) is for a study in which predominantly highly eurytopic species are found. These are by definition uncritical of their habitat. Is there any mechanistic hypothesis underlying a suspected difference to be found in preferences for either strip cropping or monocultures of the species that were expected to be caught? In other words, did the authors have any a priori reasons to suspect differences, or has this been an exploratory exercise from which unexplained significant results should be used with great caution?
Point well taken. We agree that the indicator species analysis has limitations and therefore now replaced this with GLM analysis for the 12 most common ground beetle genera.
However, setting these objections aside there are in fact significant results with strong species associations both with monocultures and strip cropping. Unfortunately, the authors do not dig deeper into the patterns found a posteriori either. Why would some species associate so strongly with strip cropping? Do these species show a pattern of pitfall catches that deviate from other species, in that they are found in a wide range of strips with different crops in one strip cropping field and therefore may benefit from an increased abundance of food or shelter? Also, why would so many species associate with monocultures? Is this in any way logical? Could it be an artifact of the data instead of a meaningful pattern? Unfortunately, the authors do not progress along these lines in the methods and discussion at all.
We thank reviewer 3 for these valuable perspectives. In the revised manuscript, we will further explore the species/genera that respond to cropping systems and discuss these findings in more detail.
A second question raised in the introduction is whether the arable fields that form part of this study contain rare species. Unfortunately, the authors do not elaborate further on this. Do they expect rare species to be more prevalent in the strip cropping fields? Why? Has it been shown elsewhere that intercropping provides room for additional rare species?
The answer is simply no, we did not find more rare species in strip cropping. In the revised manuscript, we will add a column for rarity (according to waarneming.nl) in the table showing abundances of species per location. We only found two rare species, one of which we only found a single individual and one that was more related to the open habitat created by a failed wheat field. We will discuss this more in depth in the discussion.
Considering the implications the results of this research can have on the wider discussion of bending the curve and the effects of agroecological measures, bold claims should be made with extreme restraint and be based on extensive proof and robust findings. I am not convinced by the evidence provided in this article that the claim made by the authors that strip cropping is a useful tool for bending the curve of biodiversity loss is warranted.
We believe that strip cropping can be a useful tool because farmers readily adopt it and it can result in modest biodiversity gains without yield loss. However, strip cropping is indeed not a silver bullet (which we also don’t claim). We will nuance the implications of our study in the revised manuscript.
