Does delaying the first mowing date benefit biodiversity in meadowland?

Background

Meadows are regularly mown in order to provide fodder or litter for livestock and to prevent vegetation succession. However, the time of year at which meadows should be first mown in order to maximize biological diversity remains controversial and may vary with respect to context and focal taxa. We carried out a systematic review and meta-analysis on the effects of delaying the first mowing date upon plants and invertebrates in European meadowlands.

Methods

Following a CEE protocol, ISI Web of Science, Science Direct, JSTOR, Google and Google Scholar were searched. We recorded all studies that compared the species richness of plants, or the species richness or abundance of invertebrates, between grassland plots mown at a postponed date (treatment) vs plots mown earlier (control). In order to be included in the meta-analysis, compared plots had to be similar in all management respects, except the date of the first cut that was (mostly experimentally) manipulated. They were also to be located in the same meadow type. Meta-analyses applying Hedges’d statistic were performed.

Results

Plant species richness responded differently to the date to which mowing was postponed. Delaying mowing from spring to summer had a positive effect, while delaying either from spring to fall, or from early summer to later in the season had a negative effect. Invertebrates were expected to show a strong response to delayed mowing due to their dependence on sward structure, but only species richness showed a clearly significant positive response. Invertebrate abundance was positively influenced in only a few studies.

Conclusions

The present meta-analysis shows that in general delaying the first mowing date in European meadowlands has either positive or neutral effects on plant and invertebrate biodiversity (except for plant species richness when delaying from spring to fall or from early summer to later). Overall, there was also strong between-study heterogeneity, pointing to other major confounding factors, the elucidation of which requires further field experiments with both larger sample sizes and a distinction between taxon-specific and meadow-type-specific responses.

Farmland biodiversity has been affected by the green revolution [1] and concern about its decline already emerged in the late 1960s [2]. Concern has amplified during the past decade [e.g. [3-7] as it is now recognized that farmland biodiversity plays a major role in many agroecosystem processes, such as grassland productivity, crop pollination, pest control and soil fertility [e.g. [8-12]. As a response, most countries have implemented agri-environment schemes (AES), in which farmers are subsidised to modify their farming practice to provide environmental benefits. AES mostly aim at protecting and restoring farmland biodiversity [13,14]. They are voluntary programmes in which farmers usually receive direct payments for providing services that go beyond conventional agricultural practices, such as management of semi-natural habitats. Currently, about 30% of European farmland is under some sort of agri-environmental contract [15].

Low input (extensively managed) hay and litter meadows are among the most commonly implemented agri-environmental measures [13,16]. The most important management action on these grasslands is mowing. Mowing vegetation at least once a year has a positive effect on vascular plant species richness, especially when cuttings are removed [17,18]. However, since it has been demonstrated that early-summer mowing often has a detrimental effect on species richness of flowering plants, as it hampers completion of the reproductive cycle [17], later mowing is generally found to be more favourable for vascular plant biodiversity [19,20].

Annual mowing has a contrasting effect on invertebrates [21,22]. Although detrimental to many insects in the short term [23-28], mowing is beneficial to a large number of heliophilous and thermophilous species because it prevents the growth of bushes and trees and thus maintains semi-natural grasslands [29]. It has also been suggested that delaying the date of first mowing could be positive for a multitude of invertebrates, including butterflies, spiders, grasshoppers and ground beetles that depend on various vegetation structures [30-35]. For vertebrates, the situation is different: mowing renders food resources suddenly available (e.g. insects and rodents) that were previously hidden in the sward. Foragers may congregate towards these rich, although ephemeral food supplies [36,37]. On the other hand, ground-breeding birds are likely to be heavily penalised by early mowing [e.g. [38].

While most AES have the clear objective of restoring biodiversity and ecosystem services [13,14,39], they often bind farmers to threshold dates for agricultural operations. The date of the first mowing of meadows is usually defined as a trade-off between expected agricultural yield and supposed effects on wildlife. Given that this first mowing date is the most easily changed management practice [7,31], it appropriate adjustment is the most likely to provide environmental benefits at little economical cost. Using a meta-analytical framework, we studied the currently available scientific literature about the pros and cons for biodiversity of delaying mowing in farmed European meadowland; we also identified major gaps in knowledge related to this theme. The synthesis will be useful to both agro-ecologists and policy-makers involved in farmland management.

The primary objective of the review was to answer the following question: Does delaying the first mowing date increase biodiversity in European farmland meadows?

We followed the review methodology of the Collaboration for Environmental Evidence partnership [40,41] and published an a-priori protocol [41].

Search strategy

The following web databases were searched for relevant documents: ISI Web of Science, Science Direct, JSTOR, Google (100 first hits), Google Scholar (100 first hits). Searches were conducted in English, French and German using translations of the following logical search string: (mowing OR cutting) AND (meadow OR grassland) AND (biodiversity OR richness). The term “Europe” was not included in the search keywords as stated in the Review Protocol [41], because European studies that do not mention the term Europe may have been missed. Studies originating from extra European regions were later excluded from the review. Any apparently relevant citations or links were followed one step away from the original hit. In addition, national and international experts on the subject were asked for any relevant literature and unpublished data.

Article screening

All references retrieved from the web search were scanned at the title, abstract and full text filter level by a first reviewer. From the 367 initial references, 200 (randomly selected) were rescanned by a second reviewer in order to check for inclusion consistency. The following study inclusion criteria were used:

• Relevant subjects: semi-natural grasslands that are mown annually, including conventionally managed grasslands, AES meadows, hay or litter meadows.

• Types of intervention: first mowing date delayed (treatment).

• Types of comparator: comparison with similar meadows or plots that are first mown on an earlier date (control). Treatment and control plots must be similar in all management respects, except the date of the first cut, and must be located in the same habitat type.

• Types of outcome: species richness and/or abundance (any taxa).

Inclusion consistency was checked with kappa statistics, and agreement between the reviewers was satisfactory (k = 0.81) [42].

Study quality assessment

All articles accepted met the requirements of category II-2 and above of the classification system of [43]. This allowed for both experimental and observational studies to be included, but excluded studies that provided only qualitative evidence.

Data extraction

Some studies reported more than one treatment (two or more delayed cuts) or more than one type of measurable outcome (e.g. species richness and abundance, or different taxonomic groups such as plants and invertebrates). In these cases, all comparisons were recorded as independent data points, and this is why there are more data points (units of analysis) than articles [44,45] (Figure 1; Table 1).

The following information was extracted from the studies for each data point: (1) taxon, (2) species richness or abundance, (3) standard deviation, (4) sample size, (5) study duration in years, (6) plot size of vegetation relevés or sampling methodology for invertebrates, (7) ordinal days of the early cut and (8) delayed cut, and finally (9) meadow type, classified as dry, mesophilous or wet. Additional potential sources of heterogeneity were also extracted such as fertilizer application, number of cuts per year, grazing activity, and biogeographical region where the study was carried out. Diversity indexes such as the Shannon index were recorded when present, but did not lead to sufficient data points for a meta-analysis (MA).

Taxa were plants, invertebrates or a specific group of invertebrates. Standard deviations (SD) were usually retrieved from standard errors (SE) or variances. If no estimate of variance was provided, we requested it from the original authors. If original authors could not provide SD, or sample size was equal to one (i.e. no variance), the corresponding study was included only in the unweighted analyses (see statistical analysis section below). The ordinal days (day 1 = January 1^st) of the early cut (control) and delayed cut (treatment) were used to calculate the number of days between the two mowing regimes. If the exact date of the early or delayed cut was unknown, but only the month was given, then the 15^th of the month was used for calculations. If the terms “early” or “late” in a given month were mentioned, then the 7^th or 24^th, respectively, of that corresponding month were used.

Delaying cutting is often studied within a broader context of agricultural extensification for biodiversity, including reduced number of mowing events, changes in fertilizer inputs and/or type of fertilizer, oversowing, etc. Studies of cases in which delaying mowing occurred in the presence of such confounding factors could not be included in the MA as the effect of delaying the first cut cannot be separated from these other confounding factors [e.g. [32].

Statistical analysis

Meta-analyses were conducted on three groups of studies according to their measurable outcomes: 1) plant species richness; 2) invertebrate species richness; 3) invertebrate abundances. Studies on plant species richness lasted between two and 40 years, and if multiple time-points were available along the time series, only the data for the last year (longest time period) were considered. Studies on invertebrates were usually shorter, mostly three to four years, and due to a high inter-annual variation, these studies often reported biodiversity responses averaged across the years. Here we used these reported average values.

The Hedges’d statistic was used to estimate effect size, Hedges’d equalling to the standardized mean difference between delayed and early cuts [46]:

where and are the means of the delayed and early cut outcomes, S is their pooled standard deviation, while the term J corrects for small sample bias [47]. It was calculated using the function escalc of the R package metafor[48].

Random- and mixed-effects models (mixed-effects models are random-effects models with covariates) were chosen as it is now common practice for this kind of analysis [47]. Under random- and mixed-effects models, the true effect size, i.e. the effect size as if there were no sampling errors, can vary from study to study, but usually do so under a normal distribution [49,50]. Here the Q test and I² statistic were used to assess heterogeneity between studies. The Q test is the test of significance, and the I² statistic estimates how much of the total variability in the mean effect size (composed of heterogeneity and sampling error) can be attributed to heterogeneity among the true effect size [48,50].

First, the null model was generated. Then all univariate models including the following moderators (effect modifiers) were tested: ordinal day, time lapse (in days) between the early and the delayed cuts, study duration (in years), meadow type and plot size of the vegetation relevés. Multivariate models (various combinations of the above mentioned variables) were also explored. Further subgroup analyses were conducted to investigate the influence of key moderators separately. Models were ranked based on their AIC values (Akaike Information Criterion) and on the level of significance of the estimates [51]. Permutation tests were not always possible due to an insufficient number of data points, which limits the number of possible iterations. Therefore test statistics of the effect sizes and corresponding confidence intervals (CIs) referred to the normal distribution (Z test). Publication bias was assessed using funnel plots, by applying a regression test for funnel plot asymmetry [46,48].

In addition to the proper weighted meta-analyses, unweighted meta-analyses were performed using the response ratio as effect size. Response ratio (lr) is equal to the natural logarithm of the ratio of the delayed on the early cut date [46]. Note that this way a positive value means a positive effect of delaying mowing.

Although less powerful than proper-weighted meta-analyses, this approach allows the inclusion of studies that did not report SD or where sample size was one, i.e. studies for which no Hedges’d could be calculated. Bootstrapping was used to calculate 95% confidence intervals (CI); if CI overlapped zero, the effect size was considered to be non significant. All statistics were performed using R version 2.13.0 [52].

On the 16^th of March 2011, 367 articles were retrieved from the web searches. The influence on biodiversity of delaying the first mowing date could be investigated in 27 articles that matched inclusion criteria (Figure 1). Subsequently, twelve articles were excluded due to duplication or unsuitable data for a MA. Duplication happened when it was obvious that two studies based on the same experimental set up were looking at the same metric while either addressing different questions or considering different times. For example, the articles [53] and [54] reported studies investigating the impact of different mowing regimes on plant species richness in the same experimental set up, same plots, but one after 15 years, and the other after 22 years of management, respectively. In such cases, only the latest study (longest duration) was included in the MA. Nine additional studies were found in bibliography sections of the selected papers or obtained after contacting experts, which makes a total of 24 suitable studies submitted to the present MA (Figure 1). In some studies more than one delayed cut or more than one invertebrate group were investigated, resulting in a total of 55 data points (Table 1). All studies were experimental but three that used an observational approach [31,55,56], though the observational studies were well replicated (9 or 18 times, see Table 1). From these 55 data points, 35 deal with plant species richness, ten with invertebrate species richness, and ten with invertebrate abundance. In eleven cases (nine for plant species richness, one for invertebrate species richness and one for invertebrate abundance), the study did not report SD, or sample size equalled one. Consequently, these data points could only be included in the MA assessing response ratio. Two suitable studies on seed shed and seed bank were also found, but not included because their very specific focus was too marginal with respect to our main research question [20,57]. There was no single study on birds that complied with our selection criteria. In effect, all bird studies consisted of observational studies with potential confounding factors. An additional file shows the included data points in more detail [see Additional file 2].

Postponing the first mowing date is a widespread agri-environmental measure in Europe, though it is usually coupled with other measures such as reduction of fertilizer applications. This makes sense from an agronomical point of view since postponing mowing must be accompanied by reduced hay productivity in order to avoid over-mature grass laying on the ground and/or mouldering at the time of mowing. It would then be difficult to separate the effects of postponing mowing from the effect of fertilizer reduction. Therefore, most of the studies included in the present MA concern extensively managed grasslands with no fertilizer application and a single cut per year.

Effects on plant species richness

Results based on the response ratio were qualitatively the same as the results based on the Hedges’d. Therefore, only the results of the weighted meta-analysis based on the Hedges’d are presented below due to their superior explanatory power. An additional file shows the results of the unweighted meta-analysis based on the response ratio [see Additional file 3].

In the null model, no overall significant effect of delaying the first mowing date was supported as regards plant species richness (mean Hedges’d = 0.017 with 95% CI −0.237 – 0.2716, z = 0.134, P = 0.882, Figure 2). However, heterogeneity between studies was significant (Q = 56.88, d.f. = 25, P < 0.001, I² = 54%), indicating that the true effect size does vary from one study to the next. With study duration (in years) included in the model as a moderator, no significant influence of that moderator on the effect size was discerned (slope = 0.016 with 95% CI -0.019 – 0.051, z = 0.878 P = 0.380, Figure 3a).

In further univariate models, a significant negative influence of the date of the early cut (control) was established (slope = −0.015 with 95% CI −0.025 – −0.005, z = −2.878, P = 0.004, Figure 3b). This means that the earlier the cut in the year, the more pronounced the effect on biodiversity of delaying the first cut. On the other hand, when the early cut occurred late in the season (July to August), delaying it had no, or even a negative, effect on plant species richness. Between studies heterogeneity was significant (Q = 43.12, d.f. = 24, P = 0.010), indicating again that other moderators may also influence the effect sizes. On the contrary, the date of the delayed cut did not significantly influence the effect size (slope = −0.007 with 95% CI −0.013 – 0.001, z = −1.805, P = 0.071), although it did explain some of the heterogeneity.

In order to further investigate this issue and to evaluate the extent to which heterogeneity can be explained by variation in this moderator (first mowing date), two subset MAs were conducted. The first included only the data points with an early cut in spring (before July 1) associated with a delayed cut in summer (July to September); the second included all other combinations of early and delayed cuts (spring to fall, early summer to late summer and summer to fall, but excluded one early spring to late spring study [58]). In the first case, mean Hedges’d became significantly positive (mean Hedges’ d = 0.388 with 95% CI 0.092 – 0.684, z = 2.569, P = 0.010, Figure 2b). Between studies heterogeneity was significant (Q = 24.88, d.f. = 14, P = 0.036), while I² (40%) was not. In the second case, mean Hedges’d became significantly negative (mean Hedges’d = −0.504 with 95% CI −0.763 – −0.246, z = −3.828, P < 0.001, Figure 2c). Heterogeneity was not significant (Q = 4.56, d.f. = 9, P = 0.871), indicating that these latter studies provided consistent results.

Note that none of the models including one or more moderators (study duration, mowing date, time interval between mowings, habitat type, and plot size of the vegetation relevés) performed better that the null model according to AIC values [Additional file 4]. In addition, no asymmetry was detected in any funnel plots, which rules out any publication bias effect [Additional file 5].

Effects on invertebrate species richness

A significant positive effect of delaying the first mowing date on invertebrate species richness was found (mean Hedges’d = 0.511 with 95% CI 0.129 – 0.893, z = 2.6217, P = 0.009, Figure 4). Heterogeneity was not significant (Q = 14.97, d.f. = 8, P = 0.060). No significant influence was found concerning the number of years during which a study was carried out (slope = 0.154 with 95% CI −0.074 to 0.382, z = 0.117, P = 0.186). No models including a moderator performed better than the null model according to AIC values [Additional file 4]. No asymmetry was detected in funnel plots [Additional file 5].

Effects on invertebrate abundance

Delaying the first mowing date had no significant effect on invertebrate abundance (mean Hedges’d = −0.053 with 95% CI −0.889 – 0.783, z = −0.1249, P = 0.901, Figure 5). However, the resulting Q-Q plot was not satisfactory, while the funnel plot showed a significant asymmetry in the distribution of the data points due to the two outlying studies of Morris [59,60]. Excluding Morris’s studies from the analysis resulted in model assumptions and funnel plot becoming satisfactory, with a significant positive effect of delaying the first mowing date (mean Hedges’d = 0.533 with 95% CI 0.222 – 0.844, z = 3.3564, P = 0.001, Figure 5a), even in the absence of heterogeneity (Q = 6.59, d.f. = 6, P = 0.360). The apparent generality of this result must be treated with caution, however, as it is based on only two independent experiments. Model ranking accounting for all studies, including Morris’s studies, showed that the model that included the dates of both early and delayed mowing had a lower AIC value, with a negative effect for early mowing (slope = −2.130 with 95% CI −3.017 – −1.241, z = −4.6989, P < 0.001) and a positive effect of delayed mowing (slope = 5.607 with 95% CI 3.283 – 7.930, z = 4.730, P < 0.001) [see Additional file 4. This means that effect size is greater the earlier the first mowing and later the delayed mowing. The influence of study duration was not investigated because all study durations were either 3 or 4 years.

Limitations of available information

The main limitation of this systematic review is the low number of data points stemming from an even lower number of studies (Table 1), which precluded investigations on specific invertebrate taxa, and on the influence of several moderators. As a consequence, only the main general effects of postponing mowing could be clearly investigated. Moreover, in the MA there was great heterogeneity in plant species richness, indicating that other factors (moderators) than delaying the first mowing probably influence the effect size. While the date of the first mowing was found to be an important factor, study duration was not (Figure 3). It was also expected that heterogeneity would be influenced by the great variety of meadow types involved. However, no analyses could be conducted on this factor due to the highly unbalanced distribution of the habitats among the data points (n = 36 mesophilous meadows; 16 wet meadows; 3 dry meadows). Moreover, from the sixteen wet meadow data points, nine could not be included in the weighted MA. Additional management factors such as fertilizer application, occurrence of a second cut, seed oversowing, and autumn grazing would also influence the effect size, but they could not be investigated for the same reasons. Note that the most common management practice (42 data points out of 55) was no fertilizer application, no grazing and a single cut per year.

Study design could also play a role. While most studies were experimental, three used a purely observational approach [31,55,56]. Experimental frameworks also differed greatly in sample sizes, plot sizes and sampling methodologies, which additionally affect the probability of detecting changes. Publication bias was not apparent from the funnel plots; however, some biogeographical bias might be present as most studies originated from the UK [see Additional file 2].

The present study shows that, in most cases, delaying the first mowing date in European meadows has either positive or neutral effects on plant and invertebrate biodiversity. Our MA also provides evidence of between-study heterogeneity, emphasizing that factors other than mowing date might play an important role, a topic which deserves further investigations. These findings have particular relevance to all agri-environment schemes (AES) where the date of first mowing is strictly regulated. They are also important for the management of low input meadows, where delaying mowing may improve and secure primary production. It is has been shown that primary productivity in more diverse plant communities is more stable and resilient to disturbances [61]. In addition to agricultural grasslands, open nature reserves are often mown [e.g. [62,63]. When conservation is the primary goal of such management, the first possible mowing date should be considered carefully.

Plant species richness reacted differently according to the way mowing was postponed. Delaying mowing from spring to summer had a positive effect, while delaying either from spring to fall, or from early summer to late summer, or from summer to fall had a negative effect (Figure 2). The time interval between two mowing events was expected to have a greater positive impact the longer the time interval between cuts, though the time interval, in fact, appeared to be not significant.

Invertebrates were expected to show an even stronger response to delayed mowing than plants, due to their heavy dependence on vegetation structure [33,64,65] and high susceptibility to mechanized harvesting processes [66]. However, only invertebrate species richness showed a clear overall significant positive response (Figure 4), while no effect was detected on invertebrate abundance. It was only after removing two studies [59,60] contradicting basic MA assumptions that delaying the first mowing date was found to have a positive effect on invertebrate abundance (Figure 5).

The types of meadow considered in this review – both from a phytosociological viewpoint (e.g. Arrhenatherion, Mesobromion, Filipendulion or Caricion) and a functional perspective (e.g. hay or litter meadow) – are also believed to interact with the effects of delaying mowing. Unfortunately, the variety of meadow types across studies yielded an insufficiently balanced sample to enable investigation of the influence of that moderator. For the same reason, we were unable to consider effects on specific invertebrate taxa, notwithstanding that responses are also expected to vary with respect to taxa body size, mobility, and life history traits [27,62,67,68].

Extensification of grassland management practices is reported to positively affect general plant and invertebrate biodiversity [e.g. [32,69,70], which is confirmed by this MA. However, contrary to some other studies [e.g. [71], we could not detect any conservation conflicts between our two main focal taxa (plants and invertebrates), when some practices benefit one taxon to the detriment of the other.

Evidence of effectiveness and management recommendations

This review confirms that postponing of mowing from spring (May-June) to summer (July-September) is appropriate to promote plant and invertebrate diversity. In contrast, postponing mowing from spring to fall (October-November) or from early summer (July) to late summer or fall may have a negative impact on the vegetation species richness. Invertebrates might still benefit from it but these two postponing schemes could not be differentiated due to small sample size. Regarding wet and litter meadows, a late cut (September or later) is usually recommended [72], but unfortunately we are not in a position to confirm this recommendation, in the absence of habitat specific analyses.

When postponing mowing cannot be done at the field scale, leaving uncut grass areas within the cultivated landscape matrix can be an alternative solution to favour plants and animals [see also [73-76]. At the landscape scale, creating a mosaic of different mowing regimes will increase species diversity, as there is no single appropriate mowing time that suits all organisms [33,54,77]. In addition to the date of first mowing, a low annual cutting frequency also promotes wild plants [78] and invertebrates [79,80]. There was no single study on birds that complied with our selection criteria. However, all studies on ground-nesting birds recommend postponing mowing until after fledgings have left the nests [e.g. [81-85]. These management recommendations do not apply everywhere and must be related to the socio-economic context. For example, in highly fertilized systems (high intensity management) biodiversity is generally too low for these measures to have positive effects [e.g. [86].

Implications for further research

Our review focuses solely on the general effect of delaying the first mowing date upon plant and invertebrate species richness as well as invertebrate abundance. Some general trends could be extracted from the scientific literature, but there is still considerable uncertainty concerning the estimated effect sizes, since the influence of several moderators has barely been investigated. Altogether, invertebrates were far less documented than plants, with only seven studies of the impact of delaying mowing on species richness and/or abundance, and even these showed a major geographical bias (six studies from the UK and one from Finland). Clearly this is not sufficient to get the full picture: further long-term, experimental investigations of target taxonomic groups and species regarding responses to mowing regimes are needed. This lack of invertebrate studies is true not only for mowing but also for all factors that may influence grassland invertebrates, such as grazing, habitat fragmentation and management intensity [87]. Only experimental work can disentangle the effects of various, often concomitant management practices (e.g. mowing date and fertilizer application). We thus encourage experiments where management practices are investigated in a full factorial design or where a single management practice is tested against a control plot or field that differs only in regard to this practice. Field scale experiments should be preferred to plot scale, especially when investigating animals that can move from a plot to another. Additionally, landscape characteristics are known to influence communities of plants and animals within farmland, and should therefore be accounted for in any attempt to model the effects of management practices on those communities [88].

The authors declare that they have no competing interests.

JYH and JP carried out the literature search, JYH performed the statistical analyses and wrote the manuscript. JP conceived the systematic review, wrote the protocol and advised on the analyses. PB checked for consistency in the study inclusion (second reviewer). RA supervised the work and provided thorough editing of the manuscript. All authors commented and approved the final manuscript.

We are grateful to Judith Wunderlin for a pre-literature research on the topic. We would like to thanks all the following authors who provided extra information on their studies: Barbara Pietragalla (former B. Köhler), Ben A. Woodcock, Carol A. Marriott, Jure Čop, Kalle Hellström, Robin A. Blake, Robin Pakeman, Simon G. Potts, Stein J. Hegland, and Stephanie Bissels.

1. Wilson JD, Morris AJ, Arroyo BE, Clark SC, Bradbury RB: A review of the abundance and diversity of invertebrate and plant foods of granivorous birds in northern Europe in relation to agricultural change.

   Agric Ecosyst Environ 1999, 75:13-30.

2. Carson R: Silent Spring. Boston: Houghton Mifflin; 1962.

3. Kleijn D, Kohler F, Baldi A, Batary P, Concepcion ED, Clough Y, Diaz M, Gabriel D, Holzschuh A, Knop E, et al.: On the relationship between farmland biodiversity and land-use intensity in Europe.

   P Roy Soc B-Biol Sci 2009, 276:903-909.

4. Krebs JR, Wilson JD, Bradbury RB, Siriwardena GM: The second silent spring.

   Nature 1999, 400:611-612.

5. Robinson RA, Sutherland WJ: Post-war changes in arable farming and biodiversity in Great Britain.

   J Appl Ecol 2002, 39:157-176.

6. Scherr SJ, McNeely JA: Biodiversity conservation and agricultural sustainability: towards a new paradigm of ‘ecoagriculture’ landscapes.

   Philos T R soc B 2008, 363:477-494.

7. Chamberlain DE, Fuller RJ, Bunce RGH, Duckworth JC, Shrubb M: Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales.

   J Appl Ecol 2000, 37:771-788.

8. Altieri MA: The ecological role of biodiversity in agroecosystems.

   Agric Ecosyst Environ 1999, 74:19-31.

9. Bianchi F, Booij CJH, Tscharntke T: Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control.

   P Roy Soc B-Biol Sci 2006, 273:1715-1727.

10. Carvalheiro LG, Veldtman R, Shenkute AG, Tesfay GB, Pirk CWW, Donaldson JS, Nicolson SW: Natural and within-farmland biodiversity enhances crop productivity.

    Ecol Lett 2011, 14:251-259.

11. DeHaan LR, Weisberg S, Tilman D, Fornara D: Agricultural and biofuel implications of a species diversity experiment with native perennial grassland plants.

    Agric Ecosyst Environ 2010, 137:33-38.

12. Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, Reich PB, Scherer-Lorenzen M, Schmid B, Tilman D, van Ruijven J, et al.: High plant diversity is needed to maintain ecosystem services.

    Nature 2011, 477:199-202.

13. Kleijn D, Sutherland WJ: How effective are European agri-environment schemes in conserving and promoting biodiversity.

    J Appl Ecol 2003, 40:947-969.

14. Aviron S, Nitsch H, Jeanneret P, Buholzer S, Luka H, Pfiffner L, Pozzi S, Schupbach B, Walter T, Herzog F: Ecological cross compliance promotes farmland biodiversity in Switzerland.

    Front Ecol Environ 2009, 7:247-252.

15. Gay SH, Osterburg B, Baldock D, Zdanowicz A: Recent evolution of the EU Common Agricultural Policy (CAP): state of play and environmental potential.

    Research report MEACAP WP6-D4b 2005

    Available at: http://www.ieep.eu/assets/224/WP6D4B_CAP.pdf webcite.

    

16. Herzog F, Dreier S, Hofer G, Marfurt C, Schüpbach B, Spiess M, Walter T: Effect of ecological compensation areas on floristic and breeding bird diversity in Swiss agricultural landscapes.

    Agric Ecosyst Environ 2005, 108:189-204.

17. Parr TW, Way JM: Management of roadside vegetation: the long-term effects of cutting.

    J Appl Ecol 1988, 25:1073-1087.

18. Bakker JP, Elzinga JA, de Vries Y: Effects of long-term cutting in a grassland system: perspectives for restoration of plant communities on nutrient-poor soils.

    Appl Veg Sci 2002, 5:107-120.

19. Smith RS, Shiel RS, Millward D, Corkhill P: The interactive effects of management on the productivity and plant community structure of an upland meadow: an 8-year field trial.

    J Appl Ecol 2000, 37:1029-1043.

20. Smith RS, Shiel RS, Millward D, Corkhill P, Sanderson RA: Soil seed banks and the effects of meadow management on vegetation change in a 10-year meadow field trial.

    J Appl Ecol 2002, 39:279-293.

21. Morris MG, Rispin WE: Abundance and diversity of the coleopterous fauna of a calcareous grassland under different cutting régimes.

    J Appl Ecol 1987, 24:451-465.

22. Völkl W, Zwölfer H, Romstöck-Völkl M, Schmelzer C: Habitat management in calcareous grasslands, effects on the insect community developing in flower heads of Cynarea.

    J Appl Ecol 1993, 30:307-315.

23. Erhardt A: Diurnal Lepidoptera: sensitive indicators of cultivated and abandoned grassland.

    J Appl Ecol 1985, 22:849-861.

24. Feber RE, Smith H, Macdonald DW: The effects on butterfly abundance of the management of uncropped edges of arable fields.

    J Appl Ecol 1996, 33:1191-1205.

25. Valtonen A, Saarinen K: A highway intersection as an alternative habitat for a meadow butterfly: effect of mowing, habitat geometry and roads on the ringlet (Aphantopus hyperantus).

    Ann Zool Fenn 2005, 42:545-556.

26. Humbert J-Y, Ghazoul J, Richner N, Walter T: Hay harvesting causes high orthopteran mortality.

    Agric Ecosyst Environ 2010, 139:522-527.

27. Humbert J-Y, Ghazoul J, Sauter GJ, Walter T: Impact of different meadow mowing techniques on field invertebrates.

    J Appl Entomol 2010, 134:592-599.

28. Thorbek P, Bilde T: Reduced numbers of generalist arthropod predators after crop management.

    J Appl Ecol 2004, 41:526-538.

29. Grime JP: Plant Strategies, Vegetation Processes, and Ecosystem Properties. 2nd edition. Chichester: John Wiley; 2001.

30. Gardiner T, Hassall M: Does microclimate affect grasshopper populations after cutting of hay in improved grassland?

    J Insect Conserv 2009, 13:97-102.

31. Valtonen A, Saarinen K, Jantunen J: Effect of different mowing regimes on butterflies and diurnal moths on road verges.

    Anim Bio Conserv 2006, 29:133-148.

32. Knop E, Kleijn D, Herzog F, Schmid B: Effectiveness of the Swiss agri-environment scheme in promoting biodiversity.

    J Appl Ecol 2006, 43:120-127.

33. Morris MG: The effects of structure and its dynamics on the ecology and conservation of arthropods in British grassland.

    Biol Conserv 2000, 95:129-142.

34. Koller N, Pearson S, Pozzi S, Godat S, Herzog F, Wermeille E: Evaluation des mesures de compensation écologique sur la diversité de la flore et des papillons dans la région de Nuvilly-Combremont.

    Revue suisse Agric 2000, 32:265-271.

35. Pozzi S: Evaluation des mesures de compensation écologique dans la région de Nuvilly-Combremont par le biais des araignées.

    Revue suisse Agric 2004, 36:57-64.

36. Arlettaz R: Feeding behaviour and foraging strategy of free-living mouse-eared bats, Myotis myotis and Myotis blythii.

    Anim Behav 1996, 51:1-11.

37. Hoste-Danylow A, Romanowski J, Zmihorski M: Effects of management on invertebrates and birds in extensively used grassland of Poland.

    Agric Ecosyst Environ 2010, 139:129-133.

38. Tyler GA, Green RE, Casey C: Survival and behaviour of Corncrake Crex crex chicks during the mowing of agricultural grassland.

    Bird Stud 1998, 45:35-50.

39. Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C: Landscape perspectives on agricultural intensification and biodiversity - ecosystem service management.

    Ecol Lett 2005, 8:857-874.

40. Collaboration for Environmental Evidence: Guidelines for Systematic Review in Environmental Management. Version 4.0.

    Environmental Evidence 2010.

    www.environmentalevidence.org/Authors.htm webcite.

    

41. Pellet J, Wunderlin J: Does delaying the first mowing date increase biodiversity in European farmland meadows? CEE protocol 09-011 (SR72).

    Collaboration for Environmental Evidence 2009.

    www.environmentalevidence.org/SR72.html webcite.

    

42. Pullin AS, Stewart GB: Guidelines for systematic review in conservation and environmental management.

    Conserv Biol 2006, 20:1647-1656.

43. Pullin AS, Knight TM: Support for decision making in conservation practice: an evidence-based approach.

    J Nat Conserv 2003, 11:83-90.

44. Prieto-Benitez S, Mendez M: Effects of land management on the abundance and richness of spiders (Araneae): A meta-analysis.

    Biol Conserv 2011, 144:683-691.

45. Barrientos R, Alonso JC, Ponce C, Palacin C: Meta-analysis of the effectiveness of marked wire in reducing avian collisions with power lines.

    Conserv Biol 2011, 25:893-903.

46. Gurevitch J, Curtis PS, Jones MH: Meta-analysis in ecology.

    Adv Ecol Res 2001, 32:199-247.

47. Gurevitch J, Hedges LV: Meta-analysis: combining the results of independent experiments. In Design and Analysis of Ecological Experiments. 2nd edition. Edited by Scheiner SM, Gurevitch J. New York: Chapman and Hall; 2001:347-369.

48. Viechtbauer W: Conducting meta-analyses in R with the metafor package.

    J Stat Softw 2010, 36:1-48.

49. Perera R: Interpreting meta-analyses in systematic reviews.

    Ann Intern Med 2009, 13:67-69.

50. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR: Introduction to Meta-Analysis. Chichester: Wiley; 2009.

51. Johnson JB, Omland KS: Model selection in ecology and evolution.

    Trends Ecol Evol 2004, 19:101-108.

52. R Development Core Team: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2011.

53. Ryser P, Langenauer R, Gigon A: Species Richness and Vegetation Structure in a Limestone Grassland after 15 Years Management with Six Biomass Removal Regimes.

    Folia Geobot Phytotax 1995, 30:157-167.

54. Köhler B, Gigon A, Edwards PJ, Krüsi B, Langenauer R, Lüscher A, Ryser P: Changes in the species composition and conservation value of limestone grasslands in Northern Switzerland after 22 years of contrasting managements.

    Perspect Plant Ecol Evol Syst 2005, 7:51-67.

55. Bissels S, Holzel N, Otte N: Population structure of the threatened perennial Serratula tinctoria in relation to vegetation and management.

    Appl Veg Sci 2004, 7:267-274.

56. Hegland SJ, Van Leeuwen M, Oostermeijer JGB: Population structure of Salvia pratensis in relation to vegetation and management of Dutch dry floodplain grasslands.

    J Appl Ecol 2001, 38:1277-1289.

57. Smith RS, Pullan S, Shiel RS: Seed shed in the making of hay from mesotrophic grassland in a field in northern England: Effects of hay cut date, grazing and fertilizer in a split-split-plot experiment.

    J Appl Ecol 1996, 33:833-841.

58. Cop J, Vidrih M, Hacin J: Influence of cutting regime and fertilizer application on the botanical composition, yield and nutritive value of herbage of wet grasslands in Central Europe.

    Grass Forage Sci 2009, 64:454-465.

59. Morris MG: Responses of grassland invertebrates to management by cutting. II. Heteroptera.

    J Appl Ecol 1979, 16:417-432.

60. Morris MG: Responses of grassland invertebrates to management by cutting. III. Adverse effects on Auchenorhyncha.

    J Appl Ecol 1981, 18:107-123.

61. Tilman D, Downing JA: Biodiversity and stability in grasslands.

    Nature 1994, 367:363-365.

62. Cattin M-F, Blandenier G, Banašek-Richter C, Bersier L-F: The impact of mowing as a management strategy for wet meadows on spider (Araneae) communities.

    Biol Conserv 2003, 113:179-188.

63. Bobbink R, Willems JH: Impact of different cutting regimes on the performance of Brachypodium pinnatum in Dutch chalk grassland.

    Biol Conserv 1991, 56:1-21.

64. Dennis P, Young MR, Gordon IJ: Distribution and abundance of small insects and arachnids in relation to structural heterogeneity of grazed, indigenous grasslands.

    Ecol Entomol 1998, 23:253-264.

65. Woodcock BA, Potts SG, Tscheulin T, Pilgrim E, Ramsey AJ, Harrison-Cripps J, Brown VK, Tallowin JR: Responses of invertebrate trophic level, feeding guild and body size to the management of improved grassland field margins.

    J Appl Ecol 2009, 46:920-929.

66. Humbert J-Y, Ghazoul J, Walter T: Meadow harvesting techniques and their impacts on field fauna.

    Agric Ecosyst Environ 2009, 130:1-8.

67. Reinhardt K, Kohler G, Maas S, Detzel P: Low dispersal ability and habitat specificity promote extinctions in rare but not in widespread species: the Orthoptera of Germany.

    Ecography 2005, 28:593-602.

68. Walter T, Schneider K, Gonseth Y: Schnittzeitpunkt in Ökowiesen: Einfluss auf die Fauna.

    Agrarforschung 2007, 14:114-119.

69. Klimek S, Kemmermann ARG, Hofmann M, Isselstein J: Plant species richness and composition in managed grasslands: The relative importance of field management and environmental factors.

    Biol Conserv 2007, 134:559-570.

70. Britschgi A, Spaar R, Arlettaz R: Impact of grassland farming intensification on the breeding ecology of an indicator insectivorous passerine, the Whinchat Saxicola rubetra: Lessons for overall Alpine meadowland management.

    Biol Conserv 2006, 130:193-205.

71. Kruess A, Tscharntke T: Contrasting responses of plant and insect diversity to variation in grazing intensity.

    Biol Conserv 2002, 106:293-302.

72. Wettstein W, Schmid B: Conservation of arthropod diversity in montane wetlands: effect of altitude, habitat quality and habitat fragmentation on butterflies and grasshoppers.

    J Appl Ecol 1999, 36:363-373.

73. Dover JW, Rescia A, Fungariño S, Fairburn J, Carey P, Lunt P, Dennis RLH, Dover CJ: Can hay harvesting detrimentally affect adult butterfly abundance?

    J Insect Conserv 2010, 14:413-418.

74. Marini L, Fontana P, Battisti A, Gaston KJ: Agricultural management, vegetation traits and landscape drive orthopteran and butterfly diversity in a grassland-forest mosaic: a multi-scale approach.

    Insect Conserv Diver 2009, 2:213-220.

75. Schmidt MH, Rocker S, Hanafi J, Gigon A: Rotational fallows as overwintering habitat for grassland arthropods: the case of spiders in fen meadows.

    Biodiversity Conserv 2008, 17:3003-3012.

76. Humbert J-Y, Ghazoul J, Richner N, Walter T: Uncut grass refuges mitigate the impact of mechanical meadow harvesting on orthopterans.

    Biol Conserv 2012, 152:96-101.

77. Cizek O, Zamecnik J, Tropek R, Kocarek P, Konvicka M: Diversification of mowing regime increases arthropods diversity in species-poor cultural hay meadows.

    J Insect Conserv 2012, 16:215-226.

78. Zechmeister HG, Schmitzberger I, Steurer B, Peterseil J, Wrbka T: The influence of land-use practices and economics on plant species richness in meadows.

    Biol Conserv 2003, 114:165-177.

79. Helden AJ, Leather SR: Biodiversity on urban roundabouts-Hemiptera, management and the species-area relationship.

    Basic Appl Ecol 2004, 5:367-377.

80. Blake RJ, Woodcock BA, Ramsay AJ, Pilgrim ES, Brown VK, Tallowin JR, Potts SG: Novel margin management to enhance Auchenorrhyncha biodiversity in intensive grasslands.

    Agric Ecosyst Environ 2011, 140:506-513.

81. Olsson O, Brady M, Hart R: Optimal delay of harvest – implications for bird populations and economic compensation.

    Asp Appl Biol 2010, 100:1-8.

82. Green RE: Factors affecting the population density of the corncrake Crex crex in Britain and Ireland.

    J Appl Ecol 1996, 33:237-248.

83. Müller M, Spaar R, Schifferli L, Jenni L: Effects of changes in farming of subalpine meadows on a grassland bird, the whinchat (Saxicola rubetra).

    J Ornithology 2005, 146:14-23.

84. Bretagnolle V, Villers A, Denonfoux L, Cornulier T, Inchausti P, Badenhausser I: Rapid recovery of a depleted population of Little Bustards Tetrax tetrax following provision of alfalfa through an agri-environment scheme.

    Ibis 2011, 153:4-13.

85. Nocera JJ, Parsons GJ, Milton GR, Fredeen AH: Compatibility of delayed cutting regime with bird breeding and hay nutritional quality.

    Agric Ecosyst Environ 2005, 107:245-253.

86. Haddad NM, Haarstad J, Tilman D: The effects of long-term nitrogen loading on grassland insect communities.

    Oecologia 2000, 124:73-84.

87. Littlewood NA, Stewart AJ, Woodcock BA: Science into practice – how can fundamental science contribute to better management of grasslands for invertebrates?

    Insect Conserv Diver 2012, 5:1-8.

88. Schmidt MH, Roschewitz I, Thies C, Tscharntke T: Differential effects of landscape and management on diversity and density of ground-dwelling farmland spiders.

    J Appl Ecol 2005, 42:281-287.

89. Beltman B, van den Broek T, Martin W, ten Cate M, Gusewell S: Impact of mowing regime on species richness and biomass of a limestone hay meadow in Ireland.

    Bull Geobot Inst ETH 2003, 69:17-30.

90. Fenner M, Palmer L: Grassland management to promote diversity: creation of a patchy sward by mowing and fertiliser regimes.

    Field Stud 1998, 9:313-324.

91. Hellstrom K, Huhta AP, Rautio P, Tuomi J: Search for optimal mowing regime - slow community change in a restoration trial in northern Finland.

    Ann Bot Fenn 2006, 43:338-348.

92. Kirkham FW, Tallowin JRB: The influence of cutting date and previous fertilizer treatment on the productivity and botanical composition of species-rich hay meadows on the Somerset Levels.

    Grass Forage Sci 1995, 50:365-377.

93. Marriott CA, Bolton GR, Fisher JM: Changes in species composition of abandoned sown swards after imposing seasonal cutting treatments.

    Grass Forage Sci 2003, 58:37-49.

94. Smith RS, Buckingham H, Bullard MJ, Shiel RS, Younger A: The conservation management of mesotrophic (meadow) grassland in northern England .1. Effects of grazing, cutting date and fertilizer on the vegetation of a traditionally managed sward.

    Grass Forage Sci 1996, 51:278-291.

95. Woodcock BA, Potts SG, Pilgrim E, Ramsay AJ, Tscheulin T, Parkinson A, Smith REN, Gundrey AL, Brown VK, Tallowin JR: The potential of grass field margin management for enhancing beetle diversity in intensive livestock farms.

    J Appl Ecol 2007, 44:60-69.

96. Oomes MJM, Mooi H: The effect of cutting and fertilizing on the floristic composition and production of an Arrhenatherion elatioris grassland.

    Vegetatio 1981, 46–7:233-239.

97. Selinger-Looten R, Muller S: Restoration of grassland in old maize-cultivated land: impact of mowing and role of soil seed bank.

    Revue D Ecologie-La Terre Et La Vie 2001, 56:3-19.

98. Potts SG, Woodcock BA, Roberts SPM, Tscheulin T, Pilgrim ES, Brown VK, Tallowin JR: Enhancing pollinator biodiversity in intensive grasslands.

    J Appl Ecol 2009, 46:369-379.