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Effects of an agri-environment scheme on bumblebee reproduction at local and landscape scales
Claire Carvella,*, Andrew F. G. Bourkeb, Juliet L. Osbornec, Matthew S. Hearda
aNERC Centre for Ecology & Hydrology, Maclean Building, Crowmarsh Gifford, Wallingford, Oxfordshire OX10 8BB, UK
bSchool of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK
cEnvironment & Sustainability Institute, University of Exeter, Penryn, Cornwall TR10 9FE, UK
*Corresponding author: Tel: +44 (0)1491 838800; email address: ccar@ceh.ac.uk
Running title: Bumblebee reproduction on sown flower mixtures
Article type: Research article
Abstract
Agri-environment schemes (AES) have been implemented across Europe, aiming to mitigate effects of habitat loss in agro-ecosystems for a range of declining species. These include pollinating insects such as bumblebees, for which positive effects of AES on abundance and species richness have been shown. However, there is a lack of evidence for effects of AES on reproduction of target species, at either local or landscape scales. We conducted a large-scale study across a gradient of agricultural landscapes to investigate the effects of a targeted flower mixture, sown in patches of three different sizes, on bumblebee reproduction. We used an index of the total biomass of bumblebee sexuals (males and queens) observed on replicated transects within each landscape. After controlling for floral density on transects, we found that sexual biomass (MQ) was significantly higher on sown flower patches than on conventionally managed control patches at local scales throughout the three-year study. While sown flower patches did not significantly increase MQ in surrounding landscapes, MQ was higher in landscapes surrounding larger (1 ha) than smaller (0.25 ha) sown patches. Our results suggest that, while responses of different bee species may vary depending on the plant species sown, targeted flower mixtures can enhance bumblebee reproduction by providing locally attractive forage resources at key lifecycle stages. If established at large enough scales, sown flower patches can lead to a detectable spill-over of reproductives into surrounding landscapes. Furthermore, effects of sown patches on MQ were moderated by landscape context, the strongest positive responses being detected at sites with high proportions of arable land. This supports previous findings that AES can deliver greater net benefits for pollinators in more intensively farmed landscapes.
Keywords: Bombus, agri-environment, floral density, pollinators, sexual biomass, foraging, landscape scale
Introduction
Population declines in many native species within agro-ecosystems have been attributed to the loss and fragmentation of suitable habitats resulting from agricultural intensification ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_37" \o "Tilman, 2001 #520" Tilman, Fargione, Wolff, D'Antonio, Dobson et al. 2001; HYPERLINK \l "_ENREF_41" \o "Winfree, 2009 #820" Winfree, Aguilar, Vazquez, LeBuhn & Aizen 2009). In response to these declines, a number of government-funded agri-environment schemes (AES) have been implemented (European Economic Community regulation 2078/92). These compensate farmers for undertaking farming practices considered favourable to biodiversity, including less intensive management within cropped areas and creating new habitats on uncropped land. AES have been shown to benefit birds, bees, butterflies, and plants, in terms of leading to increased species richness and abundance of individuals on focal habitat patches ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_8" \o "Carvell, 2007 #745" Carvell, Meek, Pywell, Goulson & Nowakowski 2007; HYPERLINK \l "_ENREF_32" \o "Pywell, 2012 #971" Pywell, Heard, Bradbury, Hinsley, Nowakowski et al. 2012; HYPERLINK \l "_ENREF_33" \o "Pywell, 2011 #972" Pywell, Meek, Loxton, Nowakowski, Carvell et al. 2011). However, there has been much debate as to whether these schemes are effective in halting declines in farmland biodiversity ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_6" \o "Carvalheiro, 2013 #973" Carvalheiro, Kunin, Keil, Aguirre-Gutirrez, Ellis et al. 2013; HYPERLINK \l "_ENREF_22" \o "Kleijn, 2003 #407" Kleijn & Sutherland 2003). In particular, there is little evidence for positive effects of AES on reproduction and population persistence of key taxa.
Bumblebees are a group of conservation concern globally, having undergone widespread declines in range and diversity over recent decades ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_5" \o "Cameron, 2011 #974" Cameron, Lozier, Strange, Koch, Cordes et al. 2011; HYPERLINK \l "_ENREF_40" \o "Williams, 2009 #788" Williams & Osborne 2009). They are key pollinators of native plant species and a variety of crops and, together with other wild bees, may provide insurance against honey bee declines ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_16" \o "Garratt, 2014 #906" Garratt, Coston, Truslove, Lappage, Polce et al. 2014; HYPERLINK \l "_ENREF_42" \o "Winfree, 2007 #807" Winfree, Williams, Dushoff & Kremen 2007). Bumblebees are eusocial insects with (in temperate regions) an annual colony cycle. Queens establish colonies in spring and their ability to produce new sexuals (males and queens) at the end of the cycle is dependent on the availability of floral resources to their worker force within foraging distance of the nest ADDIN EN.CITE Williams2012975(Williams, Regetz & Kremen 2012)97597517Williams, Neal M. Regetz, James Kremen, Claire Landscape-scale resources promote colony growth but not reproductive performance of bumble beesEcology Ecology1049 1058
932012( HYPERLINK \l "_ENREF_39" \o "Williams, 2012 #975" Williams, Regetz & Kremen 2012). They therefore require an extensive habitat matrix providing undisturbed nesting sites, accessible foraging sites with a temporal succession of nectar and pollen-rich plants, and mating and hibernation sites ADDIN EN.CITE Benton2006603(Benton 2006)6036036Benton, T.BumblebeesThe New Naturalist Series5802006LondonCollins( HYPERLINK \l "_ENREF_2" \o "Benton, 2006 #603" Benton 2006).
The importance of food availability for bumblebee reproduction has been inferred from the earlier appearance of queens at flower-rich sites ADDIN EN.CITE Bowers1985325(Bowers 1985)32532517Bowers, M.A.Bumblebee colonization, extinction and reproduction in subalpine meadows in northeastern Utah. EcologyEcology914-9276631985CC#( HYPERLINK \l "_ENREF_4" \o "Bowers, 1985 #325" Bowers 1985). Studies using laboratory-reared colonies placed in the field have shown positive effects of supplementary food ADDIN EN.CITE Pelletier200384(Pelletier & McNeil 2003)848417Pelletier, L.McNeil, J. N.208 Canotiers, Aylmer, PQ J9J 1W4, Canada Univ Laval, Dept Biol, Quebec City, PQ G1K 7P4, CanadaThe effect of food supplementation on reproductive success in bumblebee field coloniesOikosOikos688-6941033Queen-worker conflictbombus-terrestrisbee coloniessex-ratiosresource availabilityapidaehymenopteraparasitessizeallocation2003DecISI:000186985900023( HYPERLINK \l "_ENREF_30" \o "Pelletier, 2003 #84" Pelletier & McNeil 2003) or increased floral resources in the landscape on colony growth and numbers of males produced, but mixed effects on queen production, despite positive correlations between worker number and reproductive success ADDIN EN.CITE Westphal2009847(Westphal, Steffan-Dewenter & Tscharntke 2009; Williams et al. 2012)84784717C. WestphalI. Steffan-DewenterT. TscharntkeInstitute of Animal Ecology I, Department of Population Ecology, University of Bayreuth, 95440 Bayreuth, Germany; Department of Crop Sciences, Agroecology, University of Gttingen, Waldweg 26, 37073 Gttingen, GermanyMass flowering oilseed rape improves early colony growth but not sexual reproduction of bumblebeesJournal of Applied EcologyJournal of Applied Ecology187-19346120091365-2664http://dx.doi.org/10.1111/j.1365-2664.2008.01580.x Williams201297597597517Williams, Neal M. Regetz, James Kremen, Claire Landscape-scale resources promote colony growth but not reproductive performance of bumble beesEcology Ecology1049 1058
932012( HYPERLINK \l "_ENREF_38" \o "Westphal, 2009 #847" Westphal, Steffan-Dewenter & Tscharntke 2009; HYPERLINK \l "_ENREF_39" \o "Williams, 2012 #975" Williams et al. 2012). These studies suggested that spatiotemporal variation in floral resources was a key determinant of reproductive success, and availability of later-season resources could be critical for queen production. Furthermore, bumblebee declines across Europe, particularly in late-emerging species, have been linked to the loss of preferred forage resources such as late-season red clover (Trifolium pratense), as a result of agricultural intensification ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_3" \o "Bommarco, 2012 #976" Bommarco, Lundin, Smith & Rundlf 2012; HYPERLINK \l "_ENREF_10" \o "Carvell, 2006 #810" Carvell, Roy, Smart, Pywell, Preston et al. 2006; HYPERLINK \l "_ENREF_15" \o "Fitzpatrick, 2007 #763" Fitzpatrick, Murray, Paxton, Breen, Cotton et al. 2007; HYPERLINK \l "_ENREF_21" \o "Kleijn, 2008 #798" Kleijn & Raemakers 2008).
Production of sexuals may therefore be increased in many wild bee species by an increase in food resources available to the provisioning adults. However, since the work of Bowers (1985), few field studies of wild bumblebees have reported counts of sexuals, as opposed to workers. Lye et al. ADDIN EN.CITE Lye2009817(Lye, Park, Osborne, Holland & Goulson 2009)81781717Lye, GillianPark, KirstyOsborne, JulietHolland, JohnGoulson, DaveAssessing the value of Rural Stewardship schemes for providing foraging resources and nesting habitat for bumblebee queens (Hymenoptera: Apidae)Biological ConservationBiological Conservation2023-203214210BombusPollinatorAgri-environmentLand managementFarmAgriculture2009http://www.sciencedirect.com/science/article/B6V5X-4W99NRJ-2/2/fd692c2147f0537232abbb0a17cb77c6 ( HYPERLINK \l "_ENREF_28" \o "Lye, 2009 #817" Lye, Park, Osborne, Holland & Goulson 2009) investigated the effects of habitat management under the Scottish agri-environment scheme on nest-site searching queens during the period of emergence and colony foundation. Rundlf et al. ADDIN EN.CITE Rundlf2014977(Rundlf, Persson, Smith & Bommarco 2014)97797717Rundlf, MajPersson, Anna S.Smith, Henrik G.Bommarco, RiccardoLate-season mass-flowering red clover increases bumble bee queen and male densitiesBiological ConservationBiological Conservation138-1451720BombusFlower resourcesMitigation measurePollinatorReproductive successTrifolium pratense20144//0006-3207http://www.sciencedirect.com/science/article/pii/S0006320714000883http://dx.doi.org/10.1016/j.biocon.2014.02.027( HYPERLINK \l "_ENREF_35" \o "Rundlf, 2014 #977" Rundlf, Persson, Smith & Bommarco 2014) found higher queen densities in established late-season red clover fields ranging from 4-16 ha than in linear field borders in surrounding landscapes during a single year. Densities of sexuals in were also higher in landscapes with, compared to landscapes without, clover fields. However, we know of no studies that have assessed the effects of newly-sown flower mixtures, and the scale of their establishment, on bumblebee reproduction across multiple years, as measured by the abundance of males and queens from wild nests throughout the season.
We previously described the response of foraging worker bumblebees to a mixture of nectar and pollen-rich plants sown in experimental patches of different sizes across a gradient of agricultural landscapes ADDIN EN.CITE Heard2007775(Carvell, Osborne, Bourke, Freeman, Pywell et al. 2011; Heard, Carvell, Carreck, Rothery, Osborne et al. 2007)77577517Heard, M. S.Carvell, C.Carreck, N. L.Rothery, P.Osborne, J. L.Bourke, A. F. G.Landscape context not patch size determines bumble-bee density on flower mixtures sown for agri-environment schemesBiology LettersBiology Letters638-641362007December 22, 2007http://rsbl.royalsocietypublishing.org/content/3/6/638.abstract 10.1098/rsbl.2007.0425Carvell201188388388317Carvell, C. Osborne, J.L.Bourke, A.F.G.Freeman, S.N. Pywell, R.F.Heard, M.S.Bumble bee species responses to a targeted conservation measure depend on landscape context and habitat qualityEcological Applications1760 - 17712152011( HYPERLINK \l "_ENREF_9" \o "Carvell, 2011 #883" Carvell, Osborne, Bourke, Freeman, Pywell et al. 2011; HYPERLINK \l "_ENREF_19" \o "Heard, 2007 #775" Heard, Carvell, Carreck, Rothery, Osborne et al. 2007). The mixture was targeted at bees and other pollinators under the Entry Level Stewardship scheme in England ADDIN EN.CITE Natural England2010804(Natural England 2010)8048046Natural England,Entry Level Stewardship: Environmental Stewardship Handbook2010PeterboroughNatural England( HYPERLINK \l "_ENREF_29" \o "Natural England, 2010 #804" Natural England 2010), aiming to provide floral resources from May to late August, essentially to provision populations during and beyond the main periods of flowering crop bloom. Furthermore, estimates of the number of colonies represented by these foraging workers suggested that, in two species, population growth rates were positive on sown flower patches relative to control habitats in intensively farmed landscapes (Heard et al. unpublished).
Here we present data derived from counts of males and queens from across 28 of the sown and control experimental patches in Carvell et al. (2011) and from conventionally managed field margins in surrounding landscapes. This approach allows us to test whether sown flower patches lead to detectable increases in counts of sexuals in semi-natural habitats in landscapes surrounding the patches, often referred to as a 'spill-over' effect ADDIN EN.CITE Hanley2011887(Hanley, Franco, Dean, Franklin, Harris et al. 2011)88788717Hanley, M. E.Franco, M.Dean, C. E.Franklin, E. L.Harris, H. R.Haynes, A. G.Rapson, S. R.Rowse, G.Thomas, K. C.Waterhouse, B. R.Knight, M. E.Increased bumblebee abundance along the margins of a mass flowering crop: evidence for pollinator spill-overOikos1618-1624120112011Blackwell Publishing Ltd1600-0706http://dx.doi.org/10.1111/j.1600-0706.2011.19233.x10.1111/j.1600-0706.2011.19233.x( HYPERLINK \l "_ENREF_18" \o "Hanley, 2011 #886" Hanley, Franco, Dean, Franklin, Harris et al. 2011). Our counts are expressed as an index of the total biomass of bumblebee sexuals, which reflects levels of reproduction or productivity across the different study landscapes, under the assumption that the sexuals observed were most likely to be foraging about a kilometre from their natal nests rather than responding to forage from many kilometres away as part of a dispersal process.
We tested the following hypotheses: 1) sown flower patches will enhance total sexual biomass of bumblebees at local and landscape scales; 2) the size of sown flower patches will influence sexual biomass, such that higher densities of males and queens will be recorded on, and in the landscapes surrounding, larger patches; and 3) the effect of sown flower patches on total sexual biomass will vary depending on landscape context, with the strongest positive responses being detected in more intensively farmed areas.
Methods
Experimental design
We selected seven sites across central and eastern England, located between 140W and 102E longitude and between 5110 and 5256N latitude, that represented typical land use for their locations but varied widely in landscape characteristics (Table A.1). At each site, three patches of different sizes (0.25 ha, 0.5 ha and 1.0 ha) were sown with a mixture of 20% legumes (Trifolium pratense of early- and late-flowering varieties, Trifolium hybridum and Lotus corniculatus) and 80% fine-leaved grasses (Festuca rubra, Poa pratensis and Cynosurus cristatus) (henceforth sown patches) as recommended under the AES 'nectar flower mixture' option at the time ADDIN EN.CITE Natural England2010804(Natural England 2010)8048046Natural England,Entry Level Stewardship: Environmental Stewardship Handbook2010PeterboroughNatural England( HYPERLINK \l "_ENREF_29" \o "Natural England, 2010 #804" Natural England 2010). We also selected a 0.25 ha control patch at each site within conventionally managed non-crop vegetation. Each patch was randomly allocated to a position along a field edge or corner and the four patches at a site were separated by an average of 3 km to minimize the influence of bumblebees flying between them ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_7" \o "Carvell, 2012 #885" Carvell, Jordan, Bourke, Pickles, Redhead et al. 2012; HYPERLINK \l "_ENREF_23" \o "Knight, 2005 #552" Knight, Martin, Bishop, Osborne, Hale et al. 2005). Sown patches were established in September 2003 and were subsequently cut and/or resown to achieve consistent flowering by summer 2005 and to maintain this throughout the experiment.
To assess densities of males and queens on patches, two 2 m x 100 m transects were established in the centre of each sown and control patch (hereafter 'local' transects). To assess the effect of sown flower patches on male and queen densities in the landscapes surrounding each patch (i.e. to quantify 'spill-over' effects), four 2 m x 100 m transects were established at random in conventionally managed field margins within 1000 m of the centre of each patch (hereafter 'landscape' transects). Of these, two were located along the margins of arable fields, one along the margin of a grass ley or semi-natural grassland depending on the landscape, and one along the edge of a woodland in order to fully represent typical vegetation for each site. This gave a total of 24 sampling transects (8 local and 16 landscape transects) per site.
Bumblebee and flower surveys
Males and queens of all social Bombus species were recorded in monthly surveys from June to September over the three years 2005 2007. Queen activity during earlier months was not recorded as we considered that these were most likely to be foundress queens rather than newly-emerged queens produced by colonies located within each landscape. On each survey, individuals visiting flowers were counted along all transects and the visited plant species was noted. The order in which the six transects on or surrounding each patch were visited was varied between surveys. Our surveys were conducted within a larger study that included counts of workers ADDIN EN.CITE Carvell2011883(Carvell et al. 2011)88388317Carvell, C. Osborne, J.L.Bourke, A.F.G.Freeman, S.N. Pywell, R.F.Heard, M.S.Bumble bee species responses to a targeted conservation measure depend on landscape context and habitat qualityEcological Applications1760 - 17712152011( HYPERLINK \l "_ENREF_9" \o "Carvell, 2011 #883" Carvell et al. 2011) for which the ecologically similar species Bombus terrestris and B. lucorum were recorded as a group, denoted B. terrestris agg., as their workers cannot be distinguished reliably in the field. For consistency, we recorded males or queens of these two species as B. terrestris agg. For B. ruderatus, only melanic individuals were recorded separately to species level, due to the difficulty of separating banded individuals from B. hortorum in the field ADDIN EN.CITE Ellis2005856(Ellis, Knight & Goulson 2005)85685617Ellis, J.S.Knight, M. E.Goulson, D.Journal of Insect Conservation75-8392Bombus,conservation, cryptic species, mtDNA, restriction enzyme2005( HYPERLINK \l "_ENREF_14" \o "Ellis, 2005 #856" Ellis, Knight & Goulson 2005). Transect visits were carried out between 10.00 and 17.30 during dry weather when ambient temperature was above 13C with at least 60% clear sky, or above 17C under any sky conditions.
To measure floral density on each survey, we identified all flowering dicotyledonous species and scored their flower abundance within ten 2 m ( 10 m sections of each transect, within the following ranges: 15; 625; 26200; 2011000; 10014999 and 5000+ flower units (defined as a single flower or an umbel, spike or capitulum on multi-flowered stems). Flower abundance was expressed as the mid-point value for each range (with a value of 12000 for the 5000+ category), and summed across all ten sections, giving a monthly estimate of the density of flowering units per transect. Subsequently we selected only plant species visited by male or queen bumblebees during the study. The summed flower abundance of these species was used as a measure of floral density.
Landscape context
Habitat surveys were undertaken to characterise the landscape surrounding each patch. In July 2004 all land parcels (defined areas of continuous land-use) within 1000 m of the patch centre were visited and categorised according to their broad land-use type and habitat composition. This radius took account of estimates of worker foraging distance for the most frequent Bombus species in our study ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_23" \o "Knight, 2005 #552" Knight et al. 2005; HYPERLINK \l "_ENREF_24" \o "Knight, 2009 #814" Knight, Osborne, Sanderson, Hale, Martin et al. 2009). These data were digitised onto a UK Ordnance Survey base map using Arc GIS software (ESRI), allowing for edits in parcel location, shape, and size. Parcel attributes were then extracted to allow calculation of the total area of each broad land-use type (hereafter 'landscape context') within 1000 m of each patch (Table A.1). We used the proportion of arable land (cropped fields) as our key measure of landscape context for analyses (as in Carvell et al. 2011), as this variable was significantly negatively correlated with proportions of improved grassland (r = -0.84, P < 0.001), built-up areas (r = -0.37, P = 0.03) and semi-natural habitats (r = -0.66, P < 0.001).
Statistical analysis
All analyses were carried out in R (version 2.8.1). Of a potential total of 672 bee surveys over three years, 8 were missed on the experimental patches due to cutting or re-sowing in early September before the sampling visit and were identified as missing values in all analyses.
Calculating an index of total sexual biomass combining male and queen counts (MQ)
We used an index of sexual biomass (MQ) that combines counts of males and queens as follows: 'MQ' = M + 3Q, where M = number of males and Q = number of queens ADDIN EN.CITE Pelletier200384(Pelletier et al. 2003)848417Pelletier, L.McNeil, J. N.208 Canotiers, Aylmer, PQ J9J 1W4, Canada Univ Laval, Dept Biol, Quebec City, PQ G1K 7P4, CanadaThe effect of food supplementation on reproductive success in bumblebee field coloniesOikosOikos688-6941033Queen-worker conflictbombus-terrestrisbee coloniessex-ratiosresource availabilityapidaehymenopteraparasitessizeallocation2003DecISI:000186985900023( HYPERLINK \l "_ENREF_30" \o "Pelletier, 2003 #84" Pelletier et al. 2003). This reflects the greater investment of time and resources required to rear queens, on a per capita basis, than males ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_1" \o "Beekman, 1998 #209" Beekman & van Stratum 1998; HYPERLINK \l "_ENREF_27" \o "Lopez-Vaamonde, 2009 #796" Lopez-Vaamonde, Raine, Koning, Brown, Pereboom et al. 2009). Values of MQ and floral density were calculated for each survey for: i) local transects (total counts per control or sown patch) and ii) landscape transects (total counts across four conventionally managed field margin transects in landscapes surrounding each patch). The three most abundant Bombus species were analysed separately, with counts of the less abundant species included in the summed MQ for all species, designated total Bombus.
Effects of sown flower patches at local and landscape scales
We used Generalized Linear Models to assess the effect of sown flower patches on MQ, with separate analyses of the data from local and landscape transects in order to compare equivalent enhanced or conventionally-managed habitats both within and between study sites. Analysis began with a maximal model that included patch type (sown vs. control), site and year as fixed effects, and a two-way interaction of patch type with year to account for possible temporal variation. Floral density of visited plants was added as a covariate to account for variation due to differences in flower abundance over time and between patches. Models were fitted assuming a Poisson distribution with a log-link function, and an offset for the number of transects per survey. An adjustment for overdispersion was added in cases where the Pearson Chi-squared statistic exceeded its associated degrees of freedom by more than two-fold ADDIN EN.CITE Crawley2005844(Crawley 2005)8448446Crawley, M.J. Statistics: An Introduction using R 2005Chichester, UKWiley( HYPERLINK \l "_ENREF_11" \o "Crawley, 2005 #844" Crawley 2005). Thereafter, terms were removed sequentially until only significant interactions and main effects (P < 0.05) remained.
Effects of patch size
To test whether the size of the three sown flower patches had an effect on MQ, we fitted additional models in which patch size (0.25 ha, 0.5 ha, 1.0 ha) replaced the binary patch type classification. Each patch size model was tested against the equivalent model with identical effects at all sown patches. A statistically significant deterioration in fit therefore implies a difference between the effects of patches of different sizes.
Effects of landscape context
Effects of landscape context on the response of MQ to sown flower patches were tested using linear models with normally-distributed errors and a log-link function. Means of predicted values from the minimal adequate models with patch type were used in cases where patch size was not significant, and means from the models with patch size were used where this term was significant. As there were no significant interactions between year and patch type in the models described (aside from one case for B. terrestris), predicted values of MQ were averaged across years, before the fitting of separate regressions of mean MQ per 100 m transect from control and sown flower patches against the proportion of arable land in the surrounding landscape.
Results
Across all transect counts, we recorded a total of 1306 males and 203 queens, representing nine social bumblebee species (Table A.2). The most abundant were Bombus lapidarius, B. pascuorum and B. terrestris agg., accounting for 53%, 15% and 20% of all observations, respectively. Males and queens were observed visiting 53 different flowering plant species. The legume species T. pratense, T. hybridum and L. corniculatus sown on the experimental patches together accounted for 21% of all flower visits by males and 53% of all visits by queens. Species receiving a high proportion of visits on transects in the surrounding landscapes were, in descending order, for males, Cirsium vulgare, Picris echioides, Senecio jacobaea, Cirsium arvense and Centaurea nigra (together accounting for 57% of visits) and, for queens, Cirsium vulgare, Ballota nigra and Lamium album (together accounting for 26% of visits).
Effects of sown flower patches at local and landscape scales
Floral density was a significant predictor of MQ at both local and landscape scales for all species except B. pascuorum (Table 1). We therefore present the means of fitted values from the minimal adequate models for each species or group in order to demonstrate differences between sown and control patches over and above the influence of floral density. Study site was a significant factor in the models for total Bombus, B. lapidarius and B. pascuorum on both local and landscape transects, and this effect is explored further in the regression analysis of MQ against landscape context.
On the local transects, MQ for total Bombus, B. lapidarius and B. pascuorum was significantly higher on sown flower patches than on conventionally managed control patches in all three years of the study (Table 1A; Fig. 1). For B. terrestris agg. on local transects, the effect of patch type was non-significant. Significant differences between years were detected for all species (Table 1A), with a tendency for lower counts in 2006 than in 2005 or 2007, but with B. pascuorum showing a significant increase in mean MQ per transect per year from 0.11 to 0.56 over the three years.
On the landscape transects surrounding sown flower patches, MQ was nearly five times lower than on local transects on the sown patches (ratio of mean MQ per transect for total Bombus on local: landscape transects = 2.4:0.5). On landscape transects surrounding control patches, MQ was roughly equal to MQ on local transects on the control patches (ratio of mean MQ per transect for total Bombus on local: landscape transects = 0.6:0.5). Hence, although total sexual biomass was highest overall in landscape sectors containing a sown patch (considering both local and landscape transects together), we did not find higher MQ on landscape transects surrounding sown patches compared with unsown controls (Fig. 2). Effects of patch type on MQ on the landscape transects were non-significant for total Bombus and B. pascuorum. For B. lapidarius, MQ was significantly lower on landscape transects surrounding sown flower patches than on landscape transects surrounding control patches (Table 1B). Significant differences between years were detected for each species (but not the total Bombus group), and for B. terrestris the effect of patch type depended on year (significant year x patch type interaction, Table 1B), with lower MQ on landscape transects surrounding sown patches (relative to control patches) in 2005 and 2007. Our first hypothesis (that sown flower patches will enhance total sexual biomass of bumblebees at local and landscape scales) is therefore supported at local scales but not at landscape scales when looking in isolation at MQ on landscape transects surrounding the focal patches.
Effects of patch size
At the local scale, the size of sown flower patches did not have a significant effect on MQ per 100m transect for any species (Table 1A). However, significant effects of patch size were found at the landscape scale (Table 1B, Fig. 2). MQ was highest on transects in landscapes surrounding the largest sown flower patches (covering 1 ha) for the total Bombus group and B. lapidarius. The effect of patch size was also significant for B. pascuorum, with higher MQ on landscape transects surrounding sown 0.5 ha patches than on those surrounding 0.25 ha or 1 ha patches (Fig. 2). Our second hypothesis (that the size of sown flower patches will influence sexual biomass, such that higher densities of males and queens will be recorded on, and in the landscapes surrounding, larger patches) is therefore supported at the landscape scale for some species but not at local scales.
Effects of landscape context
For the control patches, there were no significant relationships between MQ and the proportion of arable land at either local or landscape scales (Table 2). For sown flower patches, there was a significant positive relationship between the proportion of arable land and MQ for total Bombus and B. terrestris agg. and a marginally significant positive relationship for B. lapidarius (P = 0.07) at the local scale. In other words, there was higher sexual biomass on sown patches than on control patches in the most intensively farmed landscapes, but sexual biomasses on sown and control patches were similar in less intensively farmed landscapes (Figure 3A - D). On the landscape transects surrounding sown patches, where effects of patch size were significant, there were significant positive relationships between MQ and proportion of arable land for total Bombus and B. lapidarius (Table 2). Higher numbers of sexuals were recorded in the more intensively farmed landscapes, but only on landscape transects associated with the largest sown patches (1 ha) was MQ higher than on transects associated with control patches (Fig. 4). Effects on MQ of the proportion of arable land for B. pascuorum were non-significant, though numbers of B. pascuorum sexuals were low (Table A.2), and, in contrast to the other species, showed a trend for a negative relationship (Fig. 4C). Our third hypothesis (that the effect of sown flower patches on total sexual biomass will vary depending on landscape context) is therefore supported for some species.
Discussion
We compared standardised counts of bumblebee sexuals visiting either transects on sown patches of flowers or transects in the landscapes surrounding sown patches, relative to counts of sexuals visiting transects on or surrounding unsown, control patches, expressing these counts as an index of total sexual biomass (MQ). Sown patches providing high density forage resources throughout the season significantly enhanced sexual biomass of bumblebees at local (patch) scales. This effect was consistent over three years. At landscape scales, overall effects of sown flower patches were not detected when comparing MQ on transects surrounding them with that on transects surrounding unsown patches. However, the size of sown patches did influence sexual biomass at landscape scales, with higher densities of males and queens being recorded in landscapes surrounding larger sown patches of 1 ha or 0.5 ha depending on species. Finally, effects of sown patches on total sexual biomass were moderated by landscape context, with significant positive responses being detected at sites with high proportions of arable land (as found for worker bumblebees ADDIN EN.CITE Carvell2011883(Carvell et al. 2011)88388317Carvell, C. Osborne, J.L.Bourke, A.F.G.Freeman, S.N. Pywell, R.F.Heard, M.S.Bumble bee species responses to a targeted conservation measure depend on landscape context and habitat qualityEcological Applications1760 - 17712152011( HYPERLINK \l "_ENREF_9" \o "Carvell, 2011 #883" Carvell et al. 2011)).
The question of whether the sown flower patches enhanced reproduction within local bumblebee populations or attracted sexuals in from many kilometres away is central to the interpretation of our results. Here we consider flower preferences, flight distances and colony dynamics to offer possible explanations. The legume (Fabaceae) species sown in our study represent highly rewarding nectar and pollen resources for worker bumblebees from May to late August ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_9" \o "Carvell, 2011 #883" Carvell et al. 2011; HYPERLINK \l "_ENREF_34" \o "Pywell, 2006 #599" Pywell, Warman, Hulmes, Hulmes, Nuttall et al. 2006). The flower preferences of males and queens differ from those of workers and from each other ADDIN EN.CITE Benton2006603(Benton 2006)6036036Benton, T.BumblebeesThe New Naturalist Series5802006LondonCollins( HYPERLINK \l "_ENREF_2" \o "Benton, 2006 #603" Benton 2006). For example, B. lapidarius males favour Cirsium vulgare and other open flowers for nectar collection but have no requirement for pollen, whereas newly-emerged queens favour Trifolium pratense and other long-corolla flowers from which they consume large amounts of pollen ADDIN EN.CITE Carvell2007745(Carvell et al. 2007)74574517Carvell, C.Meek, W. R.Pywell, R. F.Goulson, D.Nowakowski, M.NERC, Ctr Ecol & Hydrol, Huntingdon PE28 2LS, England. Univ Stirling, Sch Biol & Environm Sci, Stirling FK9 4LA, Scotland. Wildlife Farming Co, Bicester OX26 1UN, Oxon, England.
Carvell, C, NERC, Ctr Ecol & Hydrol, Huntingdon PE28 2LS, England.
ccar@ceh.ac.ukComparing the efficacy of agri-environment schemes to enhance bumble bee abundance and diversity on arable field marginsJournal of Applied EcologyJournal of Applied Ecology29-40441agri-environmentarable farmlandBombusbumblebeesforage plantsINTENSIVELY FARMED LANDSCAPESPROVIDING FORAGING RESOURCESPROMOTINGBIODIVERSITYBOMBUSMANAGEMENTCONSERVATIONGRASSLANDENGLANDFLOWERSSCALE2007Feb0021-8901ISI:000243023600005<Go to ISI>://000243023600005 ( HYPERLINK \l "_ENREF_8" \o "Carvell, 2007 #745" Carvell et al. 2007). Both types of flower were available to sexuals in our study, and, as expected, floral density on transects was a significant predictor of sexual biomass for B. lapidarius and B. terrestris. The sown patches contained weedy species and legumes (e.g. Lotus corniculatus) that are attractive to males. In addition most were grassy and linear in shape, offering males good opportunities for patrolling for mates. This may explain why we found higher sexual biomass (dominated by male densities) on sown patches than on controls or surrounding landscape transects, in contrast to a previous study that found higher male densities on landscape transects than on pure clover fields ADDIN EN.CITE Rundlf2014977(Rundlf et al. 2014)97797717Rundlf, MajPersson, Anna S.Smith, Henrik G.Bommarco, RiccardoLate-season mass-flowering red clover increases bumble bee queen and male densitiesBiological ConservationBiological Conservation138-1451720BombusFlower resourcesMitigation measurePollinatorReproductive successTrifolium pratense20144//0006-3207http://www.sciencedirect.com/science/article/pii/S0006320714000883http://dx.doi.org/10.1016/j.biocon.2014.02.027( HYPERLINK \l "_ENREF_35" \o "Rundlf, 2014 #977" Rundlf et al. 2014). That floral density did not relate to sexual biomass of B. pascuorum may have been due to the more specialised flower choices of this species. Nevertheless, total sexual biomass was consistently greater on sown flower patches than on control patches at the local scale, over and above the influence of floral density, suggesting that sown patches enhanced reproduction in local populations of the focal species.
With regard to flight distances and the scale at which sown flower patches affect the distribution of males and queens, our data suggest that sown patches may attract sexuals over a short range from the surrounding landscape, if those sexuals travel over distances similar to the foraging distance of workers (estimated in the region of 200 1000 m in UK landscapes similar to those surveyed here ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_7" \o "Carvell, 2012 #885" Carvell et al. 2012; HYPERLINK \l "_ENREF_23" \o "Knight, 2005 #552" Knight et al. 2005)). For patches of 0.25 ha or 0.5 ha, we found lower sexual biomass on the landscape transects surrounding (within 1 km of) sown patches than on the landscape transects surrounding control patches (for B. lapidarius in all years, and B. terrestris in 2007). This could have occurred if the majority of sexuals in landscapes with sown patches were being drawn into them to forage, and if, in landscapes with no sown patch, sexuals were more evenly distributed. Where larger patches of 1 ha were sown, local densities did not differ from those on smaller patches suggesting that overall numbers of sexuals were higher on larger patches. Furthermore, sexual biomass on the landscape transects surrounding larger patches was equal to or higher than that on those surrounding control patches, suggesting a spill-over effect from sown patches into surrounding semi-natural habitats ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_18" \o "Hanley, 2011 #886" Hanley et al. 2011). We cannot rule out longer-range attraction to sown resources since flight distances of newly-emerged males and queens may exceed those of workers. While evidence is limited, male and queen dispersal have been estimated at several kilometres ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_13" \o "Dreier, 2014 #988" Dreier, Redhead, Warren, Bourke, Heard et al. 2014; HYPERLINK \l "_ENREF_25" \o "Kraus, 2009 #987" Kraus, Wolf & Moritz 2009; HYPERLINK \l "_ENREF_26" \o "Lepais, 2010 #876" Lepais, Darvill, OConnor, Osborne, Sanderson et al. 2010), though newly-emerged queens are known to return to their natal colonies to shelter and build reserves for the winter. Attraction of sexuals at large spatial scales could still constitute a beneficial effect on local populations if sown flower patches enhanced male and queen fitness, mating or hibernation opportunities through the provision of non-cropped habitats.
We found the strongest effects in the most arable landscapes with a lack of alternative forage resources (Figs. 3 and 4), consistent with similar analyses on abundances of worker bumblebees and other pollinators ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_9" \o "Carvell, 2011 #883" Carvell et al. 2011; HYPERLINK \l "_ENREF_36" \o "Scheper, 2013 #986" Scheper, Holzschuh, Kuussaari, Potts, Rundlf et al. 2013). It is likely that the detection probability for males and queens on semi-natural habitats is greater in more arable landscapes due to a concentration effect where overall cover of foraging habitats is low (Scheper et al. 2013). In addition, we would expect the spill-over effect from sown flower patches to increase in landscapes where a higher proportion of colonies were foraging on them, as seems plausible in the intensive arable landscapes here. These patterns were not shown by B. pascuorum for which a non-significant relationship between sexual biomass and proportion of arable land was found at the landscape scale. This may reflect the close association of B. pascuorum with grassland habitats for nesting and foraging, and highlights the value of existing habitats in more complex landscapes ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_17" \o "Goulson, 2010 #874" Goulson, Lepais, OConnor, Osborne, Sanderson et al. 2010; HYPERLINK \l "_ENREF_20" \o "Kennedy, 2013 #890" Kennedy, Lonsdorf, Neel, Williams, Ricketts et al. 2013).
Considering colony dynamics, reproductive success in bumblebees can be highly variable between colonies. In studies using captive-reared B. terrestris colonies, most or all produced males but only between 15-50% produced queens ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_27" \o "Lopez-Vaamonde, 2009 #796" Lopez-Vaamonde et al. 2009; HYPERLINK \l "_ENREF_38" \o "Westphal, 2009 #847" Westphal et al. 2009). Wild colonies may experience even lower rates of queen production ADDIN EN.CITE Cumber1953985(Cumber 1953)98598517Cumber, R.A. Some aspects of the biology and ecology of bumble-bees bearing upon the
yields of red-clover seed in New Zealand.New Zealand Journal of Science and
Technology227-240111953( HYPERLINK \l "_ENREF_12" \o "Cumber, 1953 #985" Cumber 1953). Furthermore, consistent with our data, numerical sex ratios in bumblebees tend to be highly male-biased (in B. terrestris reared in semi-natural conditions, the numerical sex ratio was c. 50 males: 1 queen ADDIN EN.CITE Lopez-Vaamonde2009796(Lopez-Vaamonde et al. 2009)79679617Lopez-Vaamonde, C.Raine, N.E.Koning, J.W.Brown, R.M.Pereboom, J.J.M.Ings, T.C.Ramos-Rodriguez, O.Jordan, W.C.Bourke, A.F.G.Institute of Zoology, Zoological Society of London, London, UK; Queen Mary University of London, Research Centre for Psychology, School of Biological and Chemical Sciences, London, UKLifetime reproductive success and longevity of queens in an annual social insectJournal of Evolutionary Biology983-99622520091420-9101http://dx.doi.org/10.1111/j.1420-9101.2009.01706.x ( HYPERLINK \l "_ENREF_27" \o "Lopez-Vaamonde, 2009 #796" Lopez-Vaamonde et al. 2009)). Thus higher densities of males in a particular landscape act an as indicator of the potential for population growth, but only indirectly. Our study also provides evidence of population persistence as effects of sown patches were sustained over the three years. Numbers of sexuals were not reduced during 2006 and 2007 to the same extent as numbers of workers of the same species ADDIN EN.CITE Carvell2011883(Carvell et al. 2011)88388317Carvell, C. Osborne, J.L.Bourke, A.F.G.Freeman, S.N. Pywell, R.F.Heard, M.S.Bumble bee species responses to a targeted conservation measure depend on landscape context and habitat qualityEcological Applications1760 - 17712152011( HYPERLINK \l "_ENREF_9" \o "Carvell, 2011 #883" Carvell et al. 2011), suggesting that colonies may be able to respond to effects of poor weather by investing in sexual production rather than increased worker production. Furthermore, B. pascuorum showed a trend for increasing total sexual biomass over time, as would be predicted from our finding of positive population growth rates on sown patches (Heard et al. unpublished). Studies on the effects of landscape-level resources at the colony level are emerging from the application of molecular genetic methods ADDIN EN.CITE Carvell2012885(Carvell et al. 2012)88588517Carvell, ClaireJordan, William C.Bourke, Andrew F. G.Pickles, RobertRedhead, John W.Heard, Matthew S.Molecular and spatial analyses reveal links between colony-specific foraging distance and landscape-level resource availability in two bumblebee speciesOikos734-74212152012Blackwell Publishing Ltd1600-0706http://dx.doi.org/10.1111/j.1600-0706.2011.19832.x10.1111/j.1600-0706.2011.19832.x( HYPERLINK \l "_ENREF_7" \o "Carvell, 2012 #885" Carvell et al. 2012), but there is still a need for better understanding of the dynamics of different castes in wild bumblebee populations.
Conclusions
Our study provides important evidence for effects of landscape-level enhancements via a targeted agri-environment scheme on bumblebee reproduction as measured by the abundance of males and queens from wild nests. It suggests that sown flower mixtures providing season-long resources can enhance reproduction via an increase in the production of sexuals from nests within foraging distance. If sown patches are established at large enough scales (of at least 1 ha), this response can lead to spill-over effects into surrounding semi-natural habitats, particularly in intensively farmed landscapes. This is consistent with two recent meta-analyses at European ADDIN EN.CITE Scheper2013986(Scheper et al. 2013)98698617Scheper, JeroenHolzschuh, AndreaKuussaari, MikkoPotts, Simon G.Rundlf, MajSmith, Henrik G.Kleijn, DavidEnvironmental factors driving the effectiveness of European agri-environmental measures in mitigating pollinator loss a meta-analysisEcology LettersEcology Letters912-920167Agri-environmental schemesecological contrastecosystem serviceslandscape contextland-use intensitypollinators20131461-0248http://dx.doi.org/10.1111/ele.1212810.1111/ele.12128( HYPERLINK \l "_ENREF_36" \o "Scheper, 2013 #986" Scheper et al. 2013) and global ADDIN EN.CITE ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_20" \o "Kennedy, 2013 #890" Kennedy et al. 2013) scales, suggesting that farms within highly intensified agricultural landscapes receive substantial benefits for pollinators from on-farm diversification. The effectiveness of the nectar flower mixture option under the Entry Level Stewardship scheme in England is currently limited by low uptake and variable establishment quality ADDIN EN.CITE POSTNOTE2013963(POSTNOTE 2013)96396327POSTNOTE,Reversing Insect Pollinator Decline. Parliamentary Office of Science and Technology briefing for the House of Commons no. 4422013( HYPERLINK \l "_ENREF_31" \o "POSTNOTE, 2013 #963" POSTNOTE 2013). Our study adds to the evidence base for enhancing forage resources in arable landscapes, but this should not detract from the use of flower mixtures where appropriate in more heterogeneous landscapes to benefit species of conservation concern. The mechanistic relationships between bumblebee distributions, population dynamics and landscape quality are still poorly understood ADDIN EN.CITE Williams2012975(Williams et al. 2012)97597517Williams, Neal M. Regetz, James Kremen, Claire Landscape-scale resources promote colony growth but not reproductive performance of bumble beesEcology Ecology1049 1058
932012( HYPERLINK \l "_ENREF_39" \o "Williams, 2012 #975" Williams et al. 2012). Such information is central to understanding population responses to landscape change and mitigation measures, and to predicting the resulting impacts on pollination services.
Acknowledgements
We thank Sarah Hulmes, Lucy Hulmes, Pete Nuttall, Bill Meek, James Peat, Amanda Borrows, Norman Carreck, Andrew Martin, Chris Shortall, Jenny Swain and the late Bill Jordan for fieldwork assistance, GIS mapping and/or advice. We also thank Marek Novakowski (Wildlife Farming Company Ltd) for guidance on sowing and maintenance of flower patches, and all farmers who participated in the study. This research was funded by the UK Department for Environment, Food and Rural Affairs (research grant BD1625), and Natural England, Peterborough, UK.
Appendix A. Supplementary material
Table A.1. Locations and surveyed measures of landscape context (percent cover) for each study landscape in England.
Table A.2. Total counts of males and queens on local and landscape transects across seven UK study landscapes over three years.
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Figure Legends
Fig. 1. Index of bumblebee sexual biomass (MQ, see text), at the local scale on sown flower patches (filled bars) vs control patches (open bars). Results shown are means of predicted values from minimal adequate models in Table 1A with standard errors calculated from data aggregated at the level used in statistical analyses. The effect of patch type was non-significant for B. terrestris agg.
Fig. 2. Index of bumblebee sexual biomass (MQ, see text), at the landscape scale on conventionally managed margins of fields surrounding sown flower patches of different sizes (0.25 ha, 0.5 ha, 1 ha) and unsown controls (0 ha). Results shown are means of predicted values from minimal adequate models in Table 1B with standard errors calculated from data aggregated at the level used in statistical analyses.
Fig. 3. Relationships between bumblebee sexual biomass (MQ) per 100 m on local transects on sown flower (filled circles) and control (open circles) patches and the proportion of arable land within 1000 m, for (A) total Bombus, (B) Bombus lapidarius, (C) Bombus pascuorum and (D) Bombus terrestris agg.. Curves representing sown (solid line) and control (dashed line) patches were fitted using the slope and intercept values from each model (Table 2).
Fig. 4. Relationships between bumblebee sexual biomass (MQ) per 100 m on landscape transects surrounding sown flower patches of different sizes and the proportion of arable land, for (A) total Bombus, (B) Bombus lapidarius, (C) Bombus pascuorum and (D) Bombus terrestris agg.. Curves representing different patch sizes were fitted using the slope and intercept values from each model (Table 2).
Table 1. Model results showing the effects of sown flower patches on total biomass of bumblebee sexuals (MQ) at A) local and B) landscape scales. P values of deletion tests from the maximal model are shown, with terms retained in the minimal adequate model for each species shown in bold. Main effects included in significant interactions are not given separate test statistics.
A)
Model termsTotal BombusB. lapidariusB. pascuorumB. terrestris agg.dfFPFPFPFPpatch type111.4740.00111.4320.0016.9710.0093.0610.081site64.3560.0004.7480.0003.7330.0011.9770.069year25.7180.0044.0540.01813.5650.0004.9620.008MQ forage19.1690.0037.1790.0080.6000.43918.3750.000year:p type20.1010.9040.3640.6950.6850.5051.5640.211patch size20.6880.5031.8280.1620.0840.9200.1160.890
B)
Model termsTotal BombusB. lapidariusB. pascuorumB. terrestris agg.dfFPFPFPFPpatch type13.7340.0544.0230.0463.3730.066site63.1440.0054.1220.00120.5570.0021.8790.084year22.2350.1094.0690.0188.4450.015floral density115.0870.0005.3030.0221.8360.1756.8360.009year:p type22.1280.1211.1050.3333.0860.2143.2030.042patch size25.6490.0048.1580.00021.2240.0000.5540.767Table 2. Regression statistics for linear models relating total biomass of bumblebee sexuals (MQ) to the proportion of arable land within 1000 m of each patch.
Transect typeTotal BombusB. lapidariusB. pascuorumB. terrestris agg.LocalSownR sq0.6100.5110.0370.651(on patches)(mean all sizes)slope0.0310.0370.0060.009P0.0380.0710.6780.028ControlR sq0.5640.4790.0370.034slope0.0260.0320.0060.000P0.0520.0850.6780.694LandscapeSown (1ha)R sq0.5750.7150.0330.138(conventional margins)slope0.0330.0440.0050.008P0.0480.0170.6980.412Sown (0.5ha)R sq0.5080.7860.4950.337slope0.0270.053-0.022-0.001P0.0720.0080.0780.172Sown (0.25ha)R sq0.6420.5380.1540.016slope0.0170.023-0.0090.000P0.0300.0610.3840.787ControlR sq0.2970.4300.2210.103slope0.0130.026-0.0110.000P0.2060.1100.2870.483
Fig. 1
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