the value of sown grass margins for enhancing soil macrofaunal biodiversity in arable systems
TRANSCRIPT
Agriculture, Ecosystems and Environment 127 (2008) 119–125
Contents l is ts ava i lab le at ScienceDirec t
Agriculture, Ecosystems and Environment
journal homepage: www.e lsev ier .com/ locate /agee
The value of sown grass margins for enhancing soil macrofaunal biodiversityin arable systems
Jo Smith a,b,*, Simon Potts a, Paul Eggleton b
a Centre for Agri-Environmental Research, The University of Reading, Earley Gate, PO Box 237, Reading RG6 6AR, United Kingdomb Soil Biodiversity Programme, Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom
A R T I C L E I N F O
Article history:
Received 9 September 2007
Received in revised form 6 March 2008
Accepted 18 March 2008
Available online 5 May 2008
Keywords:
Agri-environment schemes
Functional diversity
Grass margins
Soil macrofauna
A B S T R A C T
The presence of a grass strip was found to be beneficial to soil macrofauna, increasing the species
densities and abundances of earthworms, woodlice and staphylinid beetles. The biodiversity of the three
main feeding groups – predators, soil ingesters and litter consumers – was also significantly higher in the
grass strips than in the field edges without strips, indicating that establishment of grassy margins in
arable fields may enhance ecosystem services such as soil fertility and pest control. The grass strip habitat
contained a large number of species of soil macrofauna, being second only to hedgerow habitat, with 10%
of the total species list for the farm found only within the margins. Of the rare species recorded on the
farm, five of the nine were from the grass strips, four of which were found only there. This study shows
that establishing grassy strips in the margins of arable fields increases the biodiversity of the soil
macrofauna, both within fields (alpha diversity) and across the farm (beta diversity).
� 2008 Elsevier B.V. All rights reserved.
1. Introduction
The establishment of grassy strips at the edges of arable fields is apopular option in many agri-environment schemes across WesternEurope (Marshall and Moonen, 2002). In England, around 33,000 haof grass strips were in place by 2004 under the CountrysideStewardship Scheme (CSS) (Defra, 2005a) and this remains a popularoption under the new Environmental Stewardship Scheme (Defra,2005b). The value of such semi-natural habitats for a variety offarmland taxa such as birds, bees, butterflies, arable weeds, smallmammals and beetles, has been well documented (Woodcock et al.,2005; Carvell et al., 2007). However, little research has assessed theimpacts of sown grass strips on soil biodiversity, despite the role ofsoil fauna communities in many ecosystem services (Brown, 1999;Lagerlof et al., 2002).
De Snoo and Chaney (1999) recognised two approaches in thedevelopment of field margin management to increase farmlandbiodiversity: (i) targeting rare or endangered species (a traditionalconservation approach) and (ii) enhancing the abundance ofcommon species forming the basis of the food chains essential toecosystem functioning (an ecological approach). The first approachoften requires careful, tailored management specific to the targettaxa in question, e.g. the provision of certain forage plants for long-
* Corresponding author at: Soil Biodiversity Programme, Department of
Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD,
United Kingdom. Tel.: +44 207 9426982; fax: +44 207 9425229.
E-mail addresses: [email protected], [email protected] (J. Smith).
0167-8809/$ – see front matter � 2008 Elsevier B.V. All rights reserved.
doi:10.1016/j.agee.2008.03.008
tongued bumblebees (Carvell et al., 2007). Current agri-environ-ment schemes adopt the second approach, and aim to enhancefarmland biodiversity by providing general prescriptions applic-able to a wide range of taxa, rather than seeking to increase thebiodiversity of a narrow group of taxa through specifically tailoredoptions (Potts et al., 2006).
This study considers the value of grass strips in arable fieldmargins for increasing the diversity of both common and rare soilmacrofauna in a UK agroecosystem. First, we compare theabundance, species density and assemblages of the macrofauna inbean fields with and without 6-m wide sown grass strips to test thehypothesis that grass strips increase soil invertebrate biodiversitywithin arable fields (alpha diversity) (H1). We then classify themacrofauna functionally according to their feeding type (soilingester, litter consumer, predator) to test the hypothesis that grassstrips can potentially enhance ecosystem services in arable fields byincreasing the abundance and species densities within functionalguilds (H2). Next we compare the soil macrofauna community of thegrass strips with those in a number of cultivated and semi-naturalhabitats across the farm to test whether sown grass marginscontribute to within-farm biodiversity (beta diversity) (H3). Finallywe test the hypothesis that sown grass margins can be importanthabitats for rare species or those with restricted distributions (H4).
2. Materials and methods
The Benham Estate (51:25:00N, 1:23:53W) is located inBerkshire, England, and is a 2630 ha mixed arable farm with
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J. Smith et al. / Agriculture, Ecosystems and Environment 127 (2008) 119–125120
sheep and cattle, and 485 ha of forestry, on loamy soils over eitherchalk or clay. Wheat is cultivated in an annual rotation with eitheroil seed rape or beans. Six-metre wide grass strips in arable fieldmargins were established in 2000/2001 under the CSS, and weresited according to advice from the Lambourn Valley Project(Farming and Wildlife Advisory Group) to link up existing semi-natural habitats, or alongside woodland or well-developed hedge-rows. The 4 m adjacent to the field boundary were sown with atussocky grass mix as recommended by the CSS, while the outer2 m were left to regenerate naturally. Following CSS/Environ-mental Stewardship guidelines, the outer 2-m strip were cut andbaled in August or September, depending on the field crop, whilethe remaining 4 m were cut when necessary to control woodygrowth. Hedges were cut no more than three times in 5 years, inline with CSS/Environmental Stewardship requirements, exceptalongside roads where they were cut more frequently for roadsafety.
To test the hypotheses H1 and H2, that grass strips increase thebiodiversity of the soil macrofauna within arable fields, soil coreswere taken along transects running from the field boundary(hedgerow) into the crop (field beans), in paired boundaries withand without 6 m grass strips in April and May 2006. The hedgerow/grass margin combination was chosen as the study system as thisrepresents the most common configuration in this region. Inaddition, the Environmental Stewardship recommends that farmerssite the grass strips adjacent to existing environmental features suchas hedgerows and boundary tree lines (Defra, 2005b). Pesticideapplications on the field bean crop include herbicides in November(Simazine1 and Centium1 (clomazone) at 1.8 and 0.2 l/ha,respectively), and fungicide (Amistar 51 (strobilurin) at 0.5 l/ha)and insecticide (Minuet1 (cypermethrin) at 0.15 l/ha) in June.
Three pairs of boundaries were sampled, each pair comprisingone boundary with and one boundary without a 6-m grass strip.Three transects were sampled across each boundary, giving a total of18 transects. Transects were located perpendicular to east- or west-facing hedgerows, on south-facing fields (slope < 3.58). Transectsalong the same boundary were at least 50 m apart. Each sampleconsisted of three cores measuring 25 cm� 25 cm and 10 cm deep,taken 3 m apart and parallel to the boundary. Soil cores wereextracted at 0 m (under the hedge), 3 m (within grass strip or crop),and at 9 m and 27 m into crop from the boundary, giving a total of 72samples (i.e. 216 soil cores). Each soil core was sorted by hand for40 min, and all macrofauna extracted into 80% alcohol.
To test the hypotheses H3 and H4, that grass strips increase thebiodiversity of soil macrofauna within farms, a number of otherhabitats, both cultivated and semi-natural, were sampled in May2006 in addition to the soil cores taken from the hedgerows, grassstrips and bean fields described above (Table 1). The additionalhabitats were typical of mixed farms in the region and includedwinter wheat fields; pasture (inorganic fertiliser applied at75 kg N/ha�1, variable P and K/ha�1 depending upon soil analysesand a June silage cut); set-aside (established in 2000/2001 bynatural regeneration and cut annually in August/September);coniferous plantation (Pinus sylvestris) and broadleaf woodland.Three separate areas of each habitat type were sampled, and thesewere spread across the farm (minimum separation = 900 m).Within each habitat patch, three samples were collected at pointsat least 50 m apart and 27 m from any boundary with an adjacenthabitat. As before, each sample consisted of three soil cores taken3 m apart, i.e. three samples, consisting of nine soil cores, perhabitat patch � three patches = nine samples (27 cores) perhabitat, with eight habitats in total. Macrofauna were extractedfrom the soil cores in the same way as described previously.
A number of environmental variables were recorded for eachsoil core (Table 1). Before core extraction, the percentage cover of
J. Smith et al. / Agriculture, Ecosystems and Environment 127 (2008) 119–125 121
grasses, forbs, bare soil and litter in a 1-m2 quadrat centred on thesoil core were estimated visually. Percentage canopy cover wascalculated using a spherical densiometer (Forest Densiometers,Bartlesville, US). Within the 25 cm � 25 cm soil core, soiltemperature was recorded using a push-in soil thermometer toa depth of 10 cm. After extraction of the soil core, samples weretaken from the adjacent soil walls at a depth of 5 cm to determinesoil moisture, bulk density, pH (H2O), texture, and C and Nconcentrations. Soil texture was determined by hand texturingfollowing the method of Dubbin (2001). Soil texturing and CNanalyses were performed on a composite sample of the three soilcores taken from each point.
The Lumbricidae, Isopoda, Diplopoda, Chilopoda, Carabidae andStaphylinidae were identified to species and checked againstreference collections at the Natural History Museum (NHM),London. The Aleocharinae (Staphylinidae) were sorted initially intomorphospecies before identification to species by P. Hammond(NHM). To test hypothesis H4, species of conservation value wereidentified from conservation reviews, distribution atlases and fieldguides (Barber and Keay, 1988; Hopkin, 1991; Hyman and Keay,1992; Hyman and Parsons, 1994; Sims and Gerard, 1999; Lee,2006). Nomenclature follows Blakemore (2005), Barber (2006),Duff (2005, 2006), Gregory (2006) and Lee (2006). Invertebrateabundances were summed for each sample (consisting of three soilcores) and species densities calculated per sample.
In order to test the hypothesis that grass strips can potentiallyenhance ecosystem services in arable fields (H2), the soilmacrofauna were divided into groups based on their feedingecology, on the assumption that species of the same trophic groupwill have a similar effect on certain ecosystem services. In thisstudy, epigeic and anecic earthworms, woodlice and millipedeswere classified as litter consumers, endogeic earthworms as soilingesters, and centipedes as predators. The Carabidae andStaphylinidae were assigned to feeding groups based on theirspecies or genus description (Luff, 1998; Clough et al., 2007).
General linear analyses with mixed models were used toidentify differences between transects with and without grassstrips for the abundances and species densities of each of the sixmacrofauna taxa (Lumbricidae, Isopoda, Diplopoda, Chilopoda,Carabidae and Staphylinidae) (H1) and the three dominant feedinggroups (litter consumers, soil ingesters and predators) (H2).Abundances were log-transformed (log(N + 1)) to meet theassumptions of the model, and analyses were carried out usingSAS 9.1 (2002). Grass strip (presence/absence), distance fromboundary, and their interaction were included as fixed factors, andboundary pair as a random effect. When a significant effect of theinteraction between grass strip and distance was found, post hoc
pairwise comparisons using a Tukey test were performed.To investigate the influence of grassy strips on the structure and
composition of the soil invertebrate assemblages (H1), the samemodel structure was applied to the species abundance data usingcanonical ordination techniques in Canoco 4.5.1 (Ter Braak andSmilauer, 2003). Species represented by a single individual wereremoved prior to analysis to reduce bias towards rare species. Apreliminary DCCA produced short gradient lengths (2.08), indicat-ing that linear ordination methods were most appropriate for thisdata (Leps and Smilauer, 2003). A partial redundancy analysis(pRDA) was carried out on the log-transformed species data, withpresence of grass strip (coded as a nominal variable), distance fromthe boundary, and the interaction between the two, included asexplanatory variables, and boundary pair as a covariable. Manualselection using Monte Carlo permutation tests (999 permutations,restricted within boundary pairs) was used to determine thesignificance of the explanatory variables in explaining variation inspecies composition. The other measured environmental para-
meters (soil and vegetation) were plotted onto the resultingordination diagram passively to identify the main factorscorrelated with the species assemblages.
To ensure equal sample sizes across all habitats, and remove thepossible bias of having a grass strip, only those samples taken fromthe hedgerow and bean fields that had no grass strip were includedin the analyses of within-farm biodiversity (H3 and H4). Thecontribution of grass strips to within-farm biodiversity (H3) wasevaluated in three ways. Firstly, the number of species unique tothe grassy strip habitat (therefore adding to the overall speciesdiversity of the farm). Secondly, the amount of species turnover (orbeta diversity) between the grass strips and the other habitats, andfinally, the distinctiveness of species assemblages in the grass striphabitat. Species turnover was measured using the Bray–Curtisabundance-based similarity index calculated with EstimateS(Colwell, 2005). This index takes into account the relativeabundance of species in addition to the simple presence/absenceof species, and was transformed into an index of species turnover(beta diversity) by subtraction from 1 (Magurran, 2004). The valuewill be 1 when habitats have no species in common and 0 whentwo habitats are identical.
Differences in the species assemblages of the different habitats(H3) were compared using principal components analysis (PCA) ofthe log-transformed species data, after removal of singletons. Toaccount for the effect of spatial autocorrelation on speciesassemblages in the different habitats, a preliminary RDA wascarried out on the species data with the spatial co-ordinates andtheir quadratic and cubic terms as environmental variables(Borcard et al., 1992). This allows identification of any spatialpatterns (linear, patches or gaps) in the data that can then bepartialled out of the main analysis as covariables. Forwardselection of the nine spatial terms was performed in Canoco4.5.1 to identify those which had a statistically significantinfluence on the species data (Borcard et al., 1992). However,none of the nine terms were found to be significant and it wasconcluded that spatial variation in the species assemblages wasminimal and therefore it was unnecessary to include spatialcovariables in the PCA analysis. As before, the abiotic and bioticenvironmental factors were superimposed on the ordinationdiagram passively to examine their relationships with the speciesdata.
3. Results
Sampling within the bean fields and associated grass strips andhedgerows to test hypotheses H1 and H2 collected just over 6000individuals, consisting of 128 species. General linear analyses withmixed models showed that there was a significant decline(P < 0.05) in all species densities and abundances of the macro-fauna taxa, except Carabidae species richness, with increasingdistance from the boundary hedge (Table 2). The abundances andspecies densities of the Lumbricidae, Isopoda and Staphylinidaeresponded significantly to the presence of a grass strip (H1), withhigher numbers present at 3 m in the boundaries with grass stripsthan without (Table 2). The species densities and abundances ofthe three main feeding groups showed a similar response to thegrass strips (H2, Table 2, Fig. 1a–f). However, the presence of a grassstrip did not increase invertebrate abundances and speciesdensities in samples taken from outside the strip (Fig. 1a–f), andsignificantly lower isopod abundances were recorded in thehedgerows with adjacent grassy strips (mean abundance (S.E.M)59.6 (11.8) with grass strip, 115.2 (24.6) without).
The RDA model explained 27% of the variation in the speciesdata, with the first axis accounting for the majority of this(eigenvalues: Ax I = 23.5%, Ax II = 3.0% and Ax III = 0.4%). Distance
Fig. 1. Species densities and abundances of the three main feeding groups in bean fields with and without grassy strips (�1 S.E.M). Differences between means based on Tukey’s
post hoc tests: NS = not significant, *P < 0.05, **P < 0.01, ***P < 0.001. Shaded bars = boundary without grassy strip, open bars = boundary with 6 m grassy strip.
Table 2Results of general linear analysis with mixed models on species density and abundance of the soil macrofauna in grassy strips and crop
Grass strip (F1,62) Distance from boundary (F3,62) Interaction (F3,62)
Abundance Species density Abundance Species density Abundance Species density
Taxa
Lumbricidae 9.15** 17.11*** 20.82*** 33.63*** 7.67*** 13.41***
Isopoda 58.27*** 13.19*** 482.31*** 274.94*** 85.21*** 9.59***
Diplopoda 1.87 NS 1.04 NS 6.28*** 5.96** 0.35 NS 0.25 NS
Chilopoda 0.01 NS 0.06 NS 61.43*** 40.72*** 2.05 NS 1.06 NS
Carabidae 2.37 NS 4.06* 5.98** 2.24 NS 0.7 NS 1.78 NS
Staphylinidae 27.97*** 19.15*** 126.21*** 98.54*** 27.96*** 24.13***
Feeding groups
Litter consumers 28.66*** 5.35* 154.92*** 88.57*** 28.39*** 4.92**
Soil ingesters 6.2* 14.17*** 10.94*** 21.64*** 5.52** 16.53***
Predators 0.91 NS 0.54 NS 78.72*** 70.17*** 6.75*** 11.42***
NS = not significant; *P < 0.05; **P < 0.01; **P < 0.001.
J. Smith et al. / Agriculture, Ecosystems and Environment 127 (2008) 119–125122
Fig. 2. RDA triplot of soil macrofaunal assemblages in bean fields with and without
grassy strips. Only species with a fit greater than 15% are shown. Environmental
variables included in the RDA are shown in black: DISTANCE = distance from
boundary, MARGIN = presence of grassy strip in field margin, INTERACTION =
interaction between distance and grassy strip. Supplementary environmental
variables are shown in grey. Samples are plotted using ‘‘Samp’’ scores (i.e.
observed values) rather than ‘‘SamE’’ scores (fitted values). Open symbols =
boundaries without grassy strips, filled symbols = boundaries with grassy strips,
(&) = 0 m from boundary, (*) = 3 m, ( ) = 9m, (b) = 27 m. Lumbricidae:
lAPOcal = Aporrectodea caliginosa, lAPOros = Aporrectodea rosea, lLUMcas =
Lumbricus castaneus, lMURmul = Murchieona muldaii. Isopoda: iARMvul =
Armadillidium vulgare, iONIase = Oniscus asellus, iPHImus = Philoscia muscorum,
iPOLsca = Porcellio scaber. Diplopoda: dTACnig = Tachypodoiulus niger. Chilopoda:
cLITmic = Lithobius microps, cNECfla = Necrophloeophagus flavus. Carabidae:
DEMatr = Demetrias atricapillus. Staphylinidae: METcly = Metopsia clypeata,
STEoss = Stenus ossium, TACnit = Tachyporus nitidulus, TACsol = Tachyporus solutus.
J. Smith et al. / Agriculture, Ecosystems and Environment 127 (2008) 119–125 123
from the boundary and the interaction between distance and grassstrip were found to be significantly correlated with speciescomposition (H1, F = 20.54, P < 0.001 and F = 5.23, P < 0.001,respectively). The ordination diagram shows a division betweensamples from the hedgerows and grass strip and those from thebean fields along axis I, while axis II differentiates between thegrass strip and hedgerow without grass strip (Fig. 2). Differenthabitats were characterised by particular sets of environmentalvariables: bean field samples had high soil temperatures andpercentage bare soil; grass strip samples had high grass cover, soilbulk density and pH; and hedgerow samples had high litter, forband canopy cover, and soil moisture (Fig. 2).
Sampling within the eight cultivated and semi-natural habitatsacross the farm, to test hypotheses H3 and H4, collected just under7000 individuals, consisting of 132 species, of which 32 wererepresented by a single individual. The most speciose groups werethe Staphylinidae with 55 species and the Carabidae with 34species. The least diverse were the Isopoda with only 5 species,while the Lumbricidae had 14, Diplopoda 11 and Chilopoda 13species each. The two most diverse habitats were hedgerows (69species) and grass strips (59 species). Of the 59 species found in thegrass strips, 13 were found solely there, of which 9 were singletons(H3). Of the 132 species collected across all habitats, nine wereclassified as rare, five of which were recorded in grass strips, andfour of these found only there (H4, Table 3).
Table 4 shows the species turnover between the grass strips andthe seven other habitats sampled (H3). The beta diversity of thewhole assemblage was quite high (0.49–0.85) with lowestturnover (0.49) between the grass strip and the hedgerow. Inparticular, there was a high species turnover of the carabids,diplopods, isopods and staphylinids between the grass strip andother habitats, while the chilopod and lumbricid communitiesshowed greater similarities with two or more other habitats.
The first four axes of the PCA model for soil macrofaunalassemblages and environmental variables, explained just under60% of the variation in the species data (eigenvalues: Ax I = 0.317,Ax II = 0.108, Ax III = 0.100 and Ax IV = 0.067). The first axis
Table 3Species classified as rare or of conservation value
Species Conservation status
Polydesmus coriaceous (Diplopoda) UK BAP long lista
Geophilus electricus (Chilopoda) 3/4b
Henia brevis (Chilopoda) 4/5b
Lithobius muticus (Chilopoda) 4/4b
Ophonus ardosiacus (Carabidae) Notable Bc
Ophonus azureus (Carabidae) Notable Bc
Panageus bipustulatus (Carabidae) Notable Bc
Aleochara brevipennis (Staphylinidae) Notablec
Lamprinodes saginatus (Staphylinidae) Notable Ac
a Classification based on a number of criteria including 25% of the world’s populatio
declined by more than 25% in the last 25 years.b Rarity index employed by Barber and Keay (1988) based on the number of 10 km2 a
1 = very common, 5/5 = rare species with a limited distribution.c Species that do not fall within Red Data Book criteria but are uncommon in Britain
Table 4Species turnover (beta-diversity) between grassy strips and other farmland habitats, se
b-Diversity All species Carabidae Chilopoda
Beans 0.85 0.92 0.57
Broadleaf 0.57 0.91 0.56
Coniferous 0.67 0.71 0.36
Hedgerow 0.49 0.69 0.74
Pasture 0.64 0.88 0.21
Set-aside 0.65 0.80 0.45
Wheat 0.71 0.60 0.62
separates hedgerow assemblages from those of the cultivatedhabitats (wheat, beans, pasture) (Fig. 3a). Abundances of speciesalong Axis I are positively correlated with the higher canopy andforb cover of the hedgerow, and negatively correlated with percent
Reference Habitat
Lee (2006) Margin, broadleaf, wheat, set-aside
Barber and Keay (1988) Hedgerow
Barber and Keay (1988) Wheat
Barber and Keay (1988) Margin
Hyman and Keay (1992) Hedgerow, set-aside
Hyman and Keay (1992) Hedgerow
Hyman and Keay (1992) Margin
Hyman and Parsons (1994) Margin
Hyman and Parsons (1994) Margin
n of a species occurring within the UK, and species where numbers or range have
species has been recorded from and the total number of records for that species: 1/
.
e text for details
Diplopoda Isopoda Lumbricidae Staphylinidae
0.76 1.00 0.66 0.92
0.58 0.66 0.36 0.89
0.83 0.75 0.53 0.98
0.86 0.46 0.24 0.64
0.69 0.94 0.37 0.69
0.89 0.75 0.45 0.70
0.56 0.95 0.42 0.70
Fig. 3. PCA triplot of soil macrofaunal assemblages in Berkshire farmland habitats,
with supplementary environmental variables plotted post hoc in grey. Grey
triangles = soil texture: L = loam, SL = silt loam, SCL = silty clay loam, CL = clay
loam, SC = silty clay. Habitats: (&) = hedgerow, (*) = grassy strips, ( ) = broadleaf
woodland, ( ) = coniferous woodland, ( ) = set-aside, (b) = pasture, (^) = wheat,
( ) = beans. (a) Axes I and II, showing only species with a fit greater than 30%. Species as
Fig. 2 plus Lumbricidae: lALOchl = Alollobophora chlorotica. Chilopoda:
cHAPsub = Haplophilus subterraneus. Carabidae: OPHlat = Ophonus azureus,
PARlin = Paradromius linearis. Staphylinidae: DRUcan = Drusilla canaliculata,
STEace = Stenus aceris. (b) Axes III and IV, showing only species with a fit greater
than 10%. Species as before plus Lumbricidae: lEIStet = Eiseniella tetraedra,
lLUMrub = Lumbricus rubellus, lLUMter = Lumbricus terrestris, lSATmam = Satchellius
mammalis. Diplopoda: dBLAgut = Blaniulus guttulatus, dBRApus = Brachyiulus pusillus,
dBRAsup = Brachydesmus superus. Chilopoda: cGEOeas = Geophilus easoni,
cLITvar = Lithobius variegatus. Carabidae: ACUmer = Acupalpis meridianis,
AMAple = Amara plebeja, ANCdor = Anchomenus dorsale, BEMobt = Bembidion
obtusum, HARaff = Harpalus affinis, PHImel = Philorhizus melanocephalus,
TREqua = Trechus quadristriatus. Staphylinidae: AMIana = Amischa analis,
MOCfun = Mocyta fungi, STEbru = Stenus brunnipes, STEcla = Stenus clavicornis,
TACsig = Tachinus signatus, TAChyp = Tachyporus hypnorum.
J. Smith et al. / Agriculture, Ecosystems and Environment 127 (2008) 119–125124
of bare soil. Samples from the grass strips are located adjacent tothe hedgerow samples along Axis I, indicating a high degree ofspecies similarity, but with lower abundances in the grass strips.Axis II divides the woodland samples into two groups, reflectingdifferences in soil pH, bulk density and soil moisture. Axes III and IVisolate the grass strip samples from the other habitats based onhigher abundances of three staphylinid species and the woodlouseArmadillidium vulgare (H3, Fig. 3b).
4. Discussion
This study shows that grass strips are also of benefit to the soilmacrofauna, increasing the species densities and abundances ofearthworms, woodlice and staphylinid beetles (H1). The abun-dance and species densities of the three main feeding groups –predators, soil ingesters and litter consumers – were alsosignificantly higher in the grass strips than in the field edgeswithout strips (H2). More diverse assemblages of litter consumersare likely to include species that differ in their preferences for littertype and mode of litter fragmentation, and in a soil microcosmexperiment, Heemsbergen et al. (2004) showed that this functionaldissimilarity among detritivores facilitated decomposition pro-cesses.
Observed benefits to biodiversity were limited to within thegrass strips and the presence of a grass strip did not increasepopulations within the adjacent crop or hedgerow (Fig. 1).However, during this study the bean crop was in its early stagesof development when sampling took place, with little vegetationcover, making it a hostile environment for most soil invertebratesother than those adapted to exposed habitats such as carabids likeBembidion lampros and Poecilus cupreus (Luff, 1998).
There were significantly fewer woodlice recorded in thehedgerows with adjacent grass strips. Although this may suggestthat the establishment of a grass strip alongside a hedgerowreduces its value for isopods, it was apparent that this result wasdue to very high densities recorded from just one of the hedgerowswithout adjacent grass strips (1098 m�2 compared to 426 and318 m�2). This hedge had a thick layer of ivy along its base thatappeared to provide a particularly good resource for populations ofwoodlice.
The grass strip habitat contained a large number of species ofsoil macrofauna, being second only to hedgerow habitat. Tenpercent (13 species) of the total species list for the farm was foundonly within the grass strips, which suggests that these habitatssupport an important component of within-farm biodiversity (H3).High values of beta diversity (species turnover), particularly for thewoodlice, millipedes, carabid and staphylinid beetles, support thisconclusion (Table 4), as does the PCA analysis which clearlyisolates the grass strip samples on Axes 3 and 4 (Fig. 3b). Speciesrecorded in the grass strips include both grassland species likeLumbricus castaneus and L. terrestris and woodland species such asGlomeris marginata and Lithobius muticus, as well as generalistarable species like Alollobophora chlorotica and Cylindroiulus
caeruleocinctus.The high abundances and species densities recorded in the
hedgerow habitat reflect the high floral diversity, low disturbanceand heterogeneity of micro-habitats found there. The PCA alsoshows the strong similarity in species composition between thegrass strips and hedgerow (Fig. 3a), but with lower speciesabundances in the grass strips. A PCA of the abiotic and bioticenvironmental data (results not shown), groups the grass stripsamples with the other cultivated habitats (beans, wheat, set-aside, pasture) with similar soil pH, bulk density and soiltemperatures. Therefore, despite the environmental conditionsin the grass strips being similar to those in cultivated habitats,
J. Smith et al. / Agriculture, Ecosystems and Environment 127 (2008) 119–125 125
species assemblages in the grass strips resemble more closelyhedgerow assemblages, which again indicates the dispersal ofspecies from the hedgerows into adjacent grass strips.
The PCA also emphasises the unique character of the hedgerowassemblage (Fig. 3a). Hedgerow flora and fauna are usuallyconsidered a subset of woodland communities (Petit and Usher,1998; McCollin et al., 2000), but the ordination diagram shows thatthe soil macrofauna assemblages of the hedgerow and woodlandare not closely related (Fig. 3a). High species densities andabundances recorded in the hedgerow make this a valuable sourceof biodiversity, and therefore an important habitat in agroecosys-tems.
Of the 59 species found in the grass strips, 26 were representedby a single individual. Singletons represent species that are eithernaturally occurring at low abundances in the assemblage, or areinvaders from other habitats. Grassy margin strips therefore maybe benefiting rare species, or alternatively, enhancing speciesdispersal by acting as corridors (Fry, 1994) by increasing thepermeability of the agricultural matrix for species in isolatednatural habitat patches, as suggested by Donald and Evans (2006).Of the rare species recorded on the farm, five of the nine were fromthe grass strips, four of which were found only there (Table 3),which suggests that, in addition to increasing the abundances ofcommon species, establishing grass strips is of conservation valuealso (H4). This contrasts with the conclusions of Kleijn et al. (2006)that agri-environment schemes may be of little benefit to rarespecies.
Acknowledgements
We are grateful to Eric Mew and Sir Richard Sutton’s SettledEstates, Newbury, Berkshire, for permission to sample on HomeFarm Benham Estate. Thanks also to Peter Hammond and RogerBooth (NHM) for assistance with beetle identification, and SarahJames (EMMA lab, NHM) for help with soil analysis. We thank twoanonymous reviewers for valuable and constructive commentsand suggestions. Jo Smith was funded by an RETF grant from theUniversity of Reading, and a grant from the Natural HistoryMuseum.
References
Barber, A.D., 2006. A working checklist of British Centipedes. http://www.bmig.or-g.uk/ (accessed April 23, 2007).
Barber, A.D., Keay, A.N., 1988. Provisional Atlas of the Centipedes of the British Isles.Biological Records Centre, Huntingdon.
Blakemore, 2005. British and Irish earthworms—a checklist of species updated fromSims and Gerard (1999). http://bio-eco.eis.ynu.ac.jp/eng/database/earthworm/(accessed April 23, 2007).
Borcard, D., Legendre, P., Drapeau, P., 1992. Partialling out the spatial component ofecological variation. Ecology 73, 1045–1055.
Brown, R.W., 1999. Grass margins and earthworm activity in organic and integratedsystems. Aspects Appl. Biol. 43, 207–210.
Carvell, C., Meek, W.R., Pywell, R.F., Goulson, D., Nowakowski, M., 2007. Comparingthe efficacy of agri-environment schemes to enhance bumble-bee abundanceand diversity on arable field margins. J. Appl. Ecol. 44, 29–40.
Clough, Y., Kruess, A., Tscharntke, T., 2007. Organic versus conventional arablefarming systems: functional grouping helps understand staphylinid response.Agric. Ecosyst. Environ. 118, 285–290.
Colwell, R.K., 2005. EstimateS: statistical estimation of species richness and sharedspecies from samples, Version 7.5. http://purl.oclc.org/estimates.
De Snoo, G.R., Chaney, K., 1999. Unsprayed field margins—what are we trying toachieve? Aspects Appl. Biol. 54, 1–12.
Defra, 2005a. Countryside Stewardship Uptake. http://www.defra.gov.uk/erdp/schemes/css/cssuptake.htm (accessed November 8, 2006).
Defra, 2005b. Entry Level Stewardship Handbook. Department for Environment,Food and Rural Affairs, UK.
Donald, P.F., Evans, A.D., 2006. Habitat connectivity and matrix restoration: thewider implications of agri-environment schemes. J. Appl. Ecol. 43, 209–218.
Dubbin, W., 2001. Soils. The Natural History Museum, London.Duff, A., 2005. Checklist of the Carabidae of the British Isles. http://www.coleopter-
ist.org.uk (accessed April 23, 2007).Duff, A., 2006. Checklist of the Staphylinidae of the British Isles. http://www.co-
leopterist.org.uk (accessed April 23, 2007).Fry, G.L.A., 1994. The role of field margins in the landscape. In: Boatman, N. (Ed.),Field
Margins: Integrating Agriculture and Conservation. British Crop ProtectionCouncil, University of Warwick.
Gregory, S., 2006. Checklist of the Woodlice of Britain and Ireland. http://www.bmi-g.org.uk/ (accessed April 23, 2007).
Heemsbergen, D.A., Berg, M.P., Loreau, M., van Hal, J.R., Faber, J.H., Verhoef, H.A.,2004. Biodiversity effects on soil processes explained by interspecific functionaldissimilarity. Science 306, 1019–1020.
Hopkin, S., 1991. A Key to the Woodlice of Britain and Ireland. Field Studies Council,Shrewsbury, UK.
Hyman, P.S., Keay, A.N., 1992. A Review of the Scarce and Threatened Coleoptera ofGreat Britain. Part 1. JNCC, Peterborough.
Hyman, P.S., Parsons, M.S., 1994. A Review of the Scarce and Threatened Coleopteraof Great Britain. Part 2. JNCC, Peterborough.
Kleijn, D., Baquero, R.A., Clough, Y., Diaz, M., De Esteban, J., Fernandez, F., Gabriel, D.,Herzog, F., Holzschuh, A., Johl, R., Knop, E., Kruess, A., Marshall, E.J.P., Steffan-Dewenter, I., Tscharntke, T., Verhulst, J., West, T.M., Yela, J.L., 2006. Mixedbiodiversity benefits of agri-environment schemes in five European countries.Ecol. Lett. 9, 243–254.
Lagerlof, J., Goffre, B., Vincent, C., 2002. The importance of field boundaries forearthworms (Lumbricidae) in the Swedish agricultural landscape. Agric. Eco-syst. Environ. 89, 91–103.
Lee, P., 2006. Atlas of the Millipedes (Diplopoda) of Britain and Ireland. Pensoft,Sofia.
Leps, J., Smilauer, P., 2003. Multivariate Analysis of Ecological Data using CANOCO.Cambridge University Press, Cambridge.
Luff, M.L., 1998. Provisional Atlas of the Ground Beetles (Coleoptera: Carabidae) ofBritain. Biological Records Centre, Huntingdon.
Magurran, A.E., 2004. Measuring Biological Diversity. Blackwell Publishing, Malden,MA.
Marshall, E.J.P., Moonen, A.C., 2002. Field margins in northern Europe: their func-tions and interactions with agriculture. Agric. Ecosyst. Environ. 89, 5–21.
McCollin, D., Jackson, J.I., Bunce, R.G.H., Barr, C.J., Stuart, R., 2000. Hedgerows ashabitat for woodland plants. J. Environ. Manage. 60, 77–90.
Petit, S., Usher, M.B., 1998. Biodiversity in agricultural landscapes, the ground beetlecommunities of woody uncultivated habitats. Biodivers. Conserv. 7, 1549–1561.
Potts, S.G., Bradbury, R.B., Mortimer, S.R., Woodcock, B.A., 2006. Commentary onKleijn et al. 2006. Ecol. Lett. 9, 245–256.
SAS, 2002. SAS Release 9. 1 For Windows. SAS Institute Inc., Cary, USA.Sims, R., Gerard, B., 1999. Earthworms. The Field Studies Council, Shrewsbury.Ter Braak, C.J.F., Smilauer, P., 2003. CANOCO for Windows. Centre for Biometry,
Wageningen.Woodcock, B.A., Westbury, D.B., Potts, S.G., Harris, S.J., Brown, V.K., 2005. Establish-
ing field margins to promote beetle conservation in arable farms. Agric. Ecosyst.Environ. 107, 255–266.