Linking soil properties and nematode community composition
13
Nematology, 2006, Vol. 8(5), 703-715 Linking soil properties and nematode community composition: effects of soil management on soil food webs Sara S ÁNCHEZ-MORENO 1,∗ , Hideomi MINOSHIMA 2 , Howard F ERRIS 1 and Louise E. JACKSON 2 1 Department of Nematology, One Shields Avenue, University of California, Davis, CA 95616, USA 2 Department of Land, Air, and Water Resources, One Shields Avenue, University of California, Davis, CA 95616, USA Received: 20 June 2006; revised: 14 July 2006 Accepted for publication: 14 July 2006 Summary – The purported benefits of conservation tillage and continuous cropping in agricultural systems include enhancement of soil ecosystem functions to improve nutrient availability to crops and soil C storage. Studies relating soil management to community structure allow the development of bioindicators and the assessment of the consequences of management practices on the soil food web. During one year (December 2003-December 2004), we studied the influence of continuous cropping (CC), intermittent fallow (F), standard tillage (ST) and no tillage (NT) on the nematode assemblage and the soil food web in a legume-vegetable rotation system in California. The most intensive systems included four crops during the study period. Tillage practices and cropping pattern strongly influenced nematode faunal composition, and the soil food web, at different soil depths. Management effects on nematode taxa depended on their position along the coloniser-persister (cp) scale and on their trophic roles. At the last sampling date (December 2004), Mesorhabditis and Acrobeloides were positively associated with NH + 4 , while Panagrolaimus and Plectus were negatively correlated with certain phospholipid fatty acids (PLFA). Microbial-feeders were in general associated with both bacterial and fungal PLFA, microbial biomass C (MBC) by chloroform fumigation-extraction, total C and N, NH + 4 and NO − 3 , and were most abundant in the surface soil of the NTCC treatment. Fungal-feeders were more closely related to PLFA markers of fungi than to ergosterol, a purported fungal sterol. Discolaimus, Prionchulus, Mylonchulus and Aporcelaimidae, in contrast, were associated with intermittent fallow and deeper soil layers. The organisms in the higher levels of the soil food web did not respond to the continuous input of C in the soil and a long recovery period may be required for appropriate taxa to be reintroduced and to increase. At the end of the experiment, each treatment supported quite different nematode assemblages and soil food webs. Keywords – cover crops, fallow, nematode sensitivity, soil food web, tillage. Composition and abundance of the nematode fauna have been used as soil health indicators in many different environments (Neher, 2001). Nematodes are functionally diverse and ubiquitous, and respond readily to environ- mental changes. The tight relationships between soil char- acteristics and abundance of nematode in different func- tional guilds (Fiscus & Neher, 2002) have been used to de- velop soil assessment criteria. In agricultural fields, nema- tode abundance and diversity are used to infer soil process rates (Ettema, 1998; Porazinska et al., 1999), soil func- tions (Ekschmitt et al., 2003; Yeates, 2003) and effects of disturbance on soil fauna (Wardle et al., 1995). Both in natural areas and under experimental conditions, nema- tode assemblages are used to assess the effects of pollu- tion (Korthals et al., 1996; Gyedu-Ababio et al., 1999), as indicators of enrichment and disturbance (Bongers, 1990; ∗ Corresponding author, e-mail: [email protected] Ferris et al., 2001; Berkelmans et al., 2003) and to study food webs dynamics (Mikola & Setälä, 1998b; Wardle et al., 2005). Reduced tillage practices are used to minimise soil disturbance, with benefits that include improved soil structure, positive effects on soil fauna, increase in water storage and reductions of fuel cost, soil erosion and air- borne dust. Under some established no-tillage systems, crop production can reach similar levels to those achieved in conventional tillage systems (Thiagalingam et al., 1996). Tillage and cropping patterns cause profound changes in populations of soil organisms (Kladivko, 2001). Studies of the effects of tillage and cropping patterns on nematode assemblages have been focused mainly on plant-parasitic nematodes (Yamada, 2001; Bulluck et al., 2002; Smiley © Koninklijke Brill NV, Leiden, 2006 703 Also available online - www.brill.nl/nemy
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Transcript of Linking soil properties and nematode community composition
Nematology 2006 Vol 8(5) 703-715
Linking soil properties and nematode community compositioneffects of soil management on soil food webs
Sara SAacuteNCHEZ-MORENO 1lowast Hideomi MINOSHIMA 2 Howard FERRIS 1 and Louise E JACKSON 2
1 Department of Nematology One Shields Avenue University of California Davis CA 95616 USA2 Department of Land Air and Water Resources One Shields Avenue University of California Davis CA 95616 USA
Received 20 June 2006 revised 14 July 2006Accepted for publication 14 July 2006
Summary ndash The purported benefits of conservation tillage and continuous cropping in agricultural systems include enhancement ofsoil ecosystem functions to improve nutrient availability to crops and soil C storage Studies relating soil management to communitystructure allow the development of bioindicators and the assessment of the consequences of management practices on the soil foodweb During one year (December 2003-December 2004) we studied the influence of continuous cropping (CC) intermittent fallow (F)standard tillage (ST) and no tillage (NT) on the nematode assemblage and the soil food web in a legume-vegetable rotation system inCalifornia The most intensive systems included four crops during the study period Tillage practices and cropping pattern stronglyinfluenced nematode faunal composition and the soil food web at different soil depths Management effects on nematode taxadepended on their position along the coloniser-persister (cp) scale and on their trophic roles At the last sampling date (December 2004)Mesorhabditis and Acrobeloides were positively associated with NH+
4 while Panagrolaimus and Plectus were negatively correlatedwith certain phospholipid fatty acids (PLFA) Microbial-feeders were in general associated with both bacterial and fungal PLFAmicrobial biomass C (MBC) by chloroform fumigation-extraction total C and N NH+
4 and NOminus3 and were most abundant in the
surface soil of the NTCC treatment Fungal-feeders were more closely related to PLFA markers of fungi than to ergosterol a purportedfungal sterol Discolaimus Prionchulus Mylonchulus and Aporcelaimidae in contrast were associated with intermittent fallow anddeeper soil layers The organisms in the higher levels of the soil food web did not respond to the continuous input of C in the soil anda long recovery period may be required for appropriate taxa to be reintroduced and to increase At the end of the experiment eachtreatment supported quite different nematode assemblages and soil food webs
Keywords ndash cover crops fallow nematode sensitivity soil food web tillage
Composition and abundance of the nematode faunahave been used as soil health indicators in many differentenvironments (Neher 2001) Nematodes are functionallydiverse and ubiquitous and respond readily to environ-mental changes The tight relationships between soil char-acteristics and abundance of nematode in different func-tional guilds (Fiscus amp Neher 2002) have been used to de-velop soil assessment criteria In agricultural fields nema-tode abundance and diversity are used to infer soil processrates (Ettema 1998 Porazinska et al 1999) soil func-tions (Ekschmitt et al 2003 Yeates 2003) and effectsof disturbance on soil fauna (Wardle et al 1995) Bothin natural areas and under experimental conditions nema-tode assemblages are used to assess the effects of pollu-tion (Korthals et al 1996 Gyedu-Ababio et al 1999) asindicators of enrichment and disturbance (Bongers 1990
lowast Corresponding author e-mail ssanchezmorenoucdavisedu
Ferris et al 2001 Berkelmans et al 2003) and to studyfood webs dynamics (Mikola amp Setaumllauml 1998b Wardle etal 2005)
Reduced tillage practices are used to minimise soildisturbance with benefits that include improved soilstructure positive effects on soil fauna increase in waterstorage and reductions of fuel cost soil erosion and air-borne dust Under some established no-tillage systemscrop production can reach similar levels to those achievedin conventional tillage systems (Thiagalingam et al1996)
Tillage and cropping patterns cause profound changesin populations of soil organisms (Kladivko 2001) Studiesof the effects of tillage and cropping patterns on nematodeassemblages have been focused mainly on plant-parasiticnematodes (Yamada 2001 Bulluck et al 2002 Smiley
copy Koninklijke Brill NV Leiden 2006 703Also available online - wwwbrillnlnemy
S Saacutenchez-Moreno et al
et al 2004 Adediran et al 2005 Roberts et al 2005)but important information on soil health and quality canbe derived from the entire nematode fauna (Urzelai et al2000 Neher 2001)
The positive effects of limiting physical disturbancemay include increases in abundance of the nematodefauna (Nakamoto et al 2006) Most organisms are moreabundant in no tillage than in conventional tillage systemsand larger-bodied organisms are especially sensitive tosoil disruption (Kladivko 2001) Thus earthworms areusually more abundant in non-tilled than in tilled soilsalthough some species react positively to tillage due to therapid incorporation of organic matter into the soil (Chan2001)
In a review of tillage effects on soil organisms Wardle(1995) reported that bacterial-feeding nematodes wereat least slightly stimulated by tillage in 65 of thestudies However in some studies total nematode densitywas reduced after the first tillage with bacterial feedersdominating in tilled plots and herbivores more abundant inno-tilled plots (Lenz amp Eisenbeis 2000) In other studiesthe density of herbivore nematodes was independent ofthe tillage system (Bulluck et al 2002) Where nematodedensities are greater in conventional than in no tillagesoils it is mainly due to greater abundances of bacterialand fungal feeders (Liphadzi et al 2005)
Fiscus and Neher (2002) developed a methodology fordistinguishing distinctive responses of nematode genera toagricultural management practices They concluded thatthe nematode taxa most sensitive to tillage were Aphelen-choides Discolaimus Eucephalobus Eudorylaimus He-terocephalobus and Wilsonema whilst Achromadora My-lonchulus Plectus and Prismatolaimus were among themost resistant to tillage effects
The maintenance of agricultural fields under bare fal-low conditions leads usually to a reduction in abundanceof plant-parasitic nematodes (Cadet et al 2003) Theeffects of bare fallow on free-living nematodes are notwell studied but they include reductions in abundance ofsome taxa (Pankhurst et al 2005) and greater nematodeabundance in the higher volumes of run-off water (Vil-lenave et al 2003) Compared with natural areas croppedfields support lower nematode diversity When croppingis abandoned and fields are allowed to revert to naturalconditions nematode diversity can increase significantly(Haacutenel 2003)
In a previous study (Minoshima et al 2006) we foundsignificant effects of tillage and continuous croppingsystems on C storage and other soil properties C storage
was higher in no-tillage than in standard tillage and withcontinuous cropping than in plots which had intermittentfallow periods Above ground plant biomass includingcrop yields was lower under no tillage than standardtillage
Our working hypotheses were based on the followingideas i) higher trophic levels of soil organisms includingnematodes are susceptible to disturbance ii) conventionalcropping systems that include periods of bare fallow donot supply sufficient C to the soil to sustain omnivores andpredators since C is respired by metabolically-active bac-terivore opportunists iii) omnivores and predators may in-crease with continuous cropping since C will be availableto support higher trophic levels iv) omnivores and preda-tors which are susceptible to disturbance should be moreabundant under no-tillage and v) soil food web structurewill be up-regulated by C inputs and slower degradationof soil C will occur in the no tillage continuous croppingtreatments
Some of these questions have been addressed in a previ-ous paper (Minoshima et al 2006) Therefore the objec-tives of the present study were to i) determine the sensi-tivity of nematode taxa to tillage and intermittent fallowtreatments at different soil depths in agricultural fieldsii) relate soil properties and nematode assemblage com-position to soil management and iii) determine whetherdifferent agricultural practices establish and maintain dif-ferent nematode assemblages and soil food webs
Materials and methods
STUDY SITE
The experiment was performed in the companion plotarea of the Long Term Research in Agricultural Systems(LTRAS) site at the University of California Davis Theexperimental plots were conventionally farmed for manydecades eg for oat hay The soil is classified as Rinconsilty clay loam (fine montmorillonitic thermic MollicHaploxeralfs) The four treatments were combinations ofintermittent fallow (F) or continuous cropping (CC) withstandard tillage (ST) and no-tillage (NT) In the NT plotsthere were no tillage operations during the study and cropresidues were spread on the top of the beds In the STplots crop residues were disked and incorporated to adepth of 20 cm between crops The cropping sequence inCC was a tomato (Lycopersicon esculentum) crop (plantedin spring 2003) sudan-sorghum (Sorghum bicolor) covercrop (planted in late summer) and a garbanzo (Cicer
704 Nematology
Effects of soil management on soil food webs
arietinum) crop (planted in late autumn) In 2004 thesummer crop was cowpeas (Vigna unguiculata) In theF treatments only tomato and garbanzo were plantedand the plots were fallow in autumn 2003 and summer2004 Four treatments were established as combinationsof both cropping pattern and tillage system NTCC (no-tillage + continuous cropping) STCC (standard tillage+ continuous cropping) NTF (no-tillage + intermittentfallow) and STF (standard tillage + intermittent fallow)
SOIL SAMPLING AND NEMATODE IDENTIFICATION
Soil was sampled in December 2003 June 2004September 2004 (only two treatments) and December2004 Soil samples were taken at three depths 0-5 cm5-15 cm and 15-30 cm Nematodes were extracted froma subsample of 350 g using a combination of decantingand sieving and Baermann funnel methods All nematodesin each sample were counted at low magnification andthen 100 nematodes (200 at the last sampling date) fromeach sample were identified to genus or family at highermagnification
Nematodes were classified by trophic habit (Yeates etal 1993) and by coloniser-persister (cp) groups (Bongers1990) The cp scale classifies nematode families in fivegroups from microbial feeders with short life cycles (cp1 and 2) to predators and omnivores with long life cyclesand greater sensitivity to environmental perturbations (cpgroups 4 and 5) Soil food web indices were calculatedafter Ferris et al (2001) based on the abundance of func-tional guilds (Bongers amp Bongers 1998) The StructureIndex (SI) is based on the relative abundance of highertrophic level nematodes and indicates soil food web lengthand soil resilience The Channel Index (CI) is calculatedas the proportion of fungal-feeding nematodes comparedto enrichment-opportunistic bacterial feeders and is anindicator of activity in the predominant decompositionchannels in the soil fungal mediated (higher values) orbacterial mediated (lower values) The Basal Index (BI) isan indicator of the prevalence of the general opportunisticnematodes that are tolerant of soil perturbation Finallythe Enrichment Index (EI) is an indicator of enrichmentopportunistic nematodes both fungal and bacterial feed-ers which respond rapidly to increases in food resourcesThe resilience of nematode trophic groups to tillage wascalculated according to Wardle (1995)
SOIL PROPERTIES
Microbial organic carbon (MBC) NH+4 NOminus
3 and er-gosterol were measured at all sampling dates Phospho-lipid fatty acids (PLFA) were used as indicators of bac-terial and fungal biomass in the soil Bacterial PLFAmarkers were iso 150 anteiso 150 150 iso 160161ω5c iso 170 anteiso 170 170cy 170 and 190cyFungal PLFA markers were 182ω 6 and 9c (Bossio etal 1998 Mikola amp Setaumllauml 1998a) Bulk density wasmeasured once in samples collected in February 2005For details of measurements of soil properties see Mi-noshima et al (2006) Soil physicochemical analyses (to-tal N total C soil pH K and plant available (Olsen)P) were performed by the University of CaliforniarsquosAgriculture and Natural Resources Analytical Laboratory(httpdanranlabucanrorg)
STATISTICAL ANALYSES
The influence of treatments on the nematode assem-blage across the four sampling dates was determined byCorrespondence Canonical Analysis (CCA) and by themethodology of Fiscus and Neher (2002) Nematode iden-tification at higher resolution was used to relate nematodetaxa with soil chemistry at the last sampling date (Decem-ber 2004) All variables were transformed as ln(x + 1)
to normalise data before the analyses ANOVA was usedto check the influence of categorical variables on nema-tode abundances and soil food web indices Correlationanalysis was used to check relationships between vari-ables Analyses were performed using STATISTICA soft-ware (StatSoft 1996)
Direct effects of tillage system cropping pattern anddepth
Differences in abundances of nematode taxa and foodweb indices were tested using General Linear Models Allthe nematological variables (nematode taxa abundancesand soil food web indices) and three categorical factors(tillage system cropping pattern and soil depth) weresubjected to CCA using data from the four samplingperiods (December 2003 June 2004 September 2004December 2004 n = 126)
In CCA bi-plots environmental axes are represented byarrows The length of the arrow indicates the importanceof the environmental variable for the ordination rootsIts direction indicates the correlation of the variable withother variables arrows in the same direction are positivelycorrelated while arrows pointing in opposite directions
Vol 8(5) 2006 705
S Saacutenchez-Moreno et al
are negatively related Dependent variables (nematodetaxa and food web indices) located near an environmental(independent) variable suggest a positive effect of thelatter on the former
Indirect effects of tillage system cropping pattern anddepth
Data from the last sampling date were subjected toANOVA to test differences in the soil properties amongtreatments Nematode abundances and soil propertieswere used to perform multivariate analyses (CCA) ofthe state of the nematode assemblage at the end ofthe cropping cycle (December 2004 n = 36) In theseanalyses nematode data were expressed at the highestlevel of taxonomic resolution available
Results
DIRECT EFFECTS OF TILLAGE SYSTEM CROPPING
PATTERN AND DEPTH
Cropping pattern tillage system and depth affected thecomposition of the nematode fauna and food web indicesacross the four sampling dates Tylenchidae Rhabditi-dae Acrobeloides and Pratylenchus were more abundantin continuously cropped plots while Dorylaimidae weremore abundant in the intermittent fallow treatments (Ta-ble 1) Consequently number of nematodes was lower andthe SI was higher under intermittent fallow (Table 2)
Tillage directly affected Aphelenchus and Rhabditidaewhich were more abundant in ST plots and Tylenchidaemore abundant in the NT treatments Depth affected Aphe-lenchus Tylenchidae Panagrolaimus and Dorylaimidaewhich were more abundant in the upper soil layers (0-15 cm) The CI was higher in NT plots Both BI and CIwere lower in the upper soil where EI was higher (Ta-ble 2)
Following Wardlersquos methodology to infer the resilienceof soil organisms to tillage (Wardle 1995) nematodes as awhole were mildly stimulated by tillage (V index = 014)In fact the response of nematodes varied depending ontheir trophic group bacterial-feeders and fungal-feederswere mildly stimulated by tillage (V = 029 and 003respectively) and herbivores and predators and omnivoreswere mildly inhibited by tillage (V = minus006 and minus0004respectively) By the same logic bacterial fungal andplant feeders were inhibited and predators and omnivoresstimulated by intermittent fallow (Fig 1)
Direct effects of cropping intensity tillage system anddepth on the nematode faunal data across the four sam-
Fig 1 V index values for nematode trophic groups (Ba =bacterial-feeders Fu = fungal-feeders Pp = plant parasitesPO = predators and omnivores) sensitivity to tillage (T) andfallow (F) Positive values indicate stimulation negative valuesindicate inhibition (after Wardle 1995)
pling dates were analysed and expressed in a CCA bi-plotTylenchidae were associated with CC and negatively af-fected by the F treatments while Aphelenchus Acrobeloi-des Rhabditidae and Panagrolaimus were positively asso-ciated with ST and negatively affected by soil depth theywere most abundant in the upper soil layers
For the four sampling dates the CI and the SI werehigher in the 15-30 cm depth and were associated withNT and F The EI was associated positively with uppersoil and the BI with medium depths and F (Fig 2)
Following Fiscus and Neher (2002) the analysis ofthe direct effects of tillage cropping pattern and depthon the nematode assemblage along the four samplingdates allowed classification of nematode taxa and foodweb descriptors as functions of their associations witheach variable Nematodes were classified as tolerant totillage if positioned in the bi-plot area defined by STand sensitive if positioned in the opposite half indicatingassociation with NT The same logic was used to scoreeach nematode taxon as sensitive or resistant to fallow andto infer associations with different soil depths (Table 3)
INDIRECT EFFECT OF TILLAGE AND COVER CROPS
Relationship between environmental variables andmanagement
On the last sampling date (December 2004) soil pHNOminus
3 and bulk density varied among the treatments pHand bulk density were higher in the NT treatments NOminus
3was significantly higher in STCC Total C total N pHergosterol and bulk density were all significantly affectedby tillage system and were higher in NT (Table 4)
Soil properties were in general strongly correlatedSoil pH and C N P and K concentrations were positively
706 Nematology
Effects of soil management on soil food websTa
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Tabl
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food
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CI=
Cha
nnel
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otal
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(N)
and
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rich
ness
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ifica
nce
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cate
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=12
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Con
tinuo
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geSt
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35
599
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362
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194
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355
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291
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364
297
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283
422
7plusmn
332
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Plt
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297
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172
264
1plusmn
149
291
4plusmn
137
270
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186
229
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161
335
0plusmn
202
285
6plusmn
191
nsns
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CI
408
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371
432
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320
471
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328
369
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239
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533
4plusmn
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483
7plusmn
428
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Vol 8(5) 2006 707
S Saacutenchez-Moreno et al
Table 3 Direct effects of tillage (ST = standard tillage NT = no-till) cropping pattern (F = fallow CC = continuous cropping)and soil depth (0-5 5-15 and 15-30 cm) on abundance ofnematode taxa and on soil food web indices (S = taxa richnessN = total number of nematodes EI = Enrichment index SI =Structure index BI = Basal index CI = Channel index) Trophicgroup (Ba = bacterial feeders Fu = fungal feeders Pp = plantparasites P = predators O = omnivores) of nematode taxa areindicated
Trophic Cp Tillage Cropping Depthgroup pattern (cm)
Aphelenchus Fu 2 ST CC 0-5Tylenchidae PpFu 2 NT CC 5-15Acrobeloides Ba 2 ST CC 0-5Panagrolaimus Ba 1 ST CC 0-5Rhabditidae Ba 1 ST CC 0-5Tylenchorhynchus Pp 3 NT F 5-15Dorylaimidae O 4 ST F 5-15Small Dorylaimidae O 4 NT CC 5-15Plectus Ba 2 NT CC 5-15Pratylenchus Pp 3 NT CC 5-15Tylencholaimus Fu 4 NT CC 5-15N ST CC 0-5S NT F 5-15EI ST CC 0-5SI ST F 15-30BI NT CC 5-15CI NT F 15-30
related (r between 049 and 083 P lt 005) NH+4
was associated with intermittent fallow and correlatedwith ergosterol and MBC (r between 049 and 052P lt 005) PLFA of fungal markers were correlated withergosterol (r = 035 P lt 005) and with PLFA ofbacterial markers (r = 095 P lt 005)
Influence of environmental variables on nematode taxaand soil food web descriptors
In December 2004 at the end of the experiment inthe ordination of the nematode taxa in the multivariatespace defined by the environmental variables positivevalues for most of the soil properties grouped togetherindicating soil enrichment and high biological activity(Fig 3a b) The PLFA biomarkers of both bacteria andfungi were related with the abundance of AcrobeloidesMesorhabditis and Tylenchorhynchus Panagrolaimus andAcrobeles both bacterial feeders were not correlated witheither group of PLFAs and ordered in the opposite part ofthe graph Tylenchidae was associated with pH (r = 047P lt 005) Aphelenchoides was associated with NOminus
3
The abundance of all the omnivores and predators(Discolaimus Aporcelaimidae Qudsianematidae and My-lonchulus) except Prionchulus were inversely correlatedwith almost all soil properties The EI was negativelycorrelated with the CI (r = minus093 P lt 005) BI(r = minus095 P lt 005) taxa richness (r = minus056P lt 005) bulk density (r = minus040 P lt 005) andPLFA of bacterial markers (r = minus035 P lt 005) It waspositioned in the opposite part of the graph than BI andCI (Fig 3) CI was positively correlated with bulk densityand PLFA of fungal markers (r = 037 and 034 respec-tively P lt 005) SI was negatively correlated with NOminus
3 pH and K (r = minus037 minus033 and minus034 P lt 005)Taxa richness and number of nematodes were negativelycorrelated (r = minus036 P lt 005) Number of nematodeswas associated with total C and taxa richness with bulkdensity CI and BI were positively correlated (r = 086P lt 005)
Discussion
The aim of this study was to evaluate the relationshipsbetween nematode faunal composition and soil propertiesas determined by agricultural management It is generallyaccepted that nematodes are strongly influenced by theirmicroenvironment and provide a useful reflection ofsoil health status and several soil functions (Mulder etal 2005) The use of multivariate statistics especiallyCanonical Analysis has improved the understanding ofthe complex relationships between different groups of soilfauna and between organisms and soil physical-chemicalproperties (Popovici amp Ciobanu 2000 Wardle et al2001 Fiscus amp Neher 2002)
As expected from previous studies (eg Wardle 1995)total nematode abundance was not strongly influenced bytillage due to the varied responses of different taxa Ne-matode responses to tillage and cropping intensity var-ied with their trophic group bacterial feeders and fun-gal feeders were stimulated by tillage and reduced un-der intermittent fallow plant-feeders were generally in-hibited by both tillage and intermittent fallow and preda-tors and omnivores were stimulated by intermittent fallowand did not respond clearly to tillage practices In factthe few omnivores and predators in this and most agri-cultural fields probably represent the more tolerant taxawithin these trophic levels Taxa intolerant to disturbancemay no longer be present in arable soils These observa-tions agree with Lenz and Eisenbeis (2000) who found nochanges in total nematode abundance and an increase of
708 Nematology
Effects of soil management on soil food webs
Table 4 Average values (plusmn SE) of soil properties in the four different treatments across three depths Significant effects of treatments(NTCC STCC STF NTF) crop pattern (CC and F) and tillage (ST and NT) are indicated by level of significance Data are from thelast sampling date (December 2004 n = 36) Data from Minoshima et al (2006)
NTF STF NTCC STCC Treatment Crop Tillage
Total C () 106 plusmn 003 099 plusmn 001 107 plusmn 004 103 plusmn 002 P lt 005Total N () 012 plusmn 000 011 plusmn 000 012 plusmn 000 012 plusmn 000 P lt 005pH 707 plusmn 003 686 plusmn 003 708 plusmn 006 690 plusmn 004 P lt 001 P lt 0001K (mg lminus1) 700 plusmn 049 591 plusmn 013 786 plusmn 132 734 plusmn 080P (microg gminus1) 1738 plusmn 088 1578 plusmn 031 1908 plusmn 217 1598 plusmn 083NO3 454 plusmn 106 550 plusmn 148 646 plusmn 092 1203 plusmn 253 P lt 005 P lt 005
(microg N gminus1)
NH4 236 plusmn 131 127 plusmn 054 116 plusmn 027 106 plusmn 016(microg N gminus1)
MBC 17123 plusmn 2623 14816 plusmn 1905 26275 plusmn 6398 17158 plusmn 1823(microg C gminus1)
Ergosterol 99932 plusmn 16846 57594 plusmn 3631 224691 plusmn 82975 121820 plusmn 25685 P lt 005(ng gminus1)
Bulk density 134 plusmn 002 125 plusmn 003 132 plusmn 002 125 plusmn 002 P lt 005 P lt 001(gcm3)
PLFAba 190753 plusmn 50529 144540 plusmn 35185 230127 plusmn 55833 208676 plusmn 31240(mgm2)
PLFAfu 24662 plusmn 12047 14295 plusmn 4381 55785 plusmn 26261 27208 plusmn 7651(mgm2)
bacterial-feeder nematodes after the first tillage treatmentOur results indicate that the response of total nematodeabundance to management depends on the assemblagecomposition so no general patterns can be discerned with-out analysing separately the taxa and functional group re-sponses For example Liphadzi et al (2005) found gen-eral increase in nematode abundance in tilled plots due tothe predominance of fungal feeders and bacterial feeders(up to 90) in the assemblages they studied
Throughout the four sampling dates of this study mostof the microbial feeders (Panagrolaimus RhabditidaeAphelenchus and Acrobeloides) were positively associ-ated with standard tillage indicating the stimulatory effecton microbes of incorporating organic matter into the soilThe nematodes less responsive to incorporated organicmatter were the higher cp taxa (Tylenchorhynchus Tylen-cholaimus Pratylenchus and some Dorylaimidae) whichwere associated with no-tillage Even though a greaternumber of taxa (especially of upper trophic levels) andhigher resolution identification would be desirable to in-fer relationships more reliably (Yeates 2003 Mulder etal 2005) we observed significant relationships betweensensitivity to tillage and trophic or cp groups as similarlyreported by Fiscus and Neher (2002)
Plectus was the only bacterivore associated with thesoil properties of the NT treatments suggesting a highersensitivity to tillage practices While Fiscus and Neher(2002) suggested that Plectus is an indicator of distur-bance due to the concordance between its cp value (2)and its tolerance to chemical and mechanical perturba-tions we found it to be more sensitive to tillage than ex-pected from its cp value Different responses among ge-nera in the same trophic group are common (Porazinska etal 1999) and nematode genera within the same trophicgroup can exhibit asymmetric competition negatively in-fluencing the abundance of other genera (Postma-Blaaw etal 2005) so responses to perturbation may be influencedby the presence of other nematode taxa Greater taxo-nomic resolution may be necessary to resolve differencesin response to environmental variables among nematodeswithin higher taxonomic groupings (Yeates 2003) espe-cially for taxa that have numerous species and a broad sizerange (eg Plectus)
Bacterial feeders are usually abundant in cultivatedsoils while predators and omnivores often disappear withcultivation (Wardle et al 1995) Microbivorous nema-todes belonging to the cp 1 group (eg Panagrolaimusor Rhabditidae enrichment-opportunistic nematodes) andthose with longer life cycles in the cp 2 group (eg Aphe-
Vol 8(5) 2006 709
S Saacutenchez-Moreno et al
Fig 2 Canonical correspondence analysis bi-plot of effects of tillage system crop pattern and depth on nematode abundances andsoil food web indices Environmental variables are marked by arrows Aphel Aphelenchus Tyl Tylenchidae Acro Acrobeloides PanPanagrolaimus Rhab Rhabditidae Tylen Tylenchorhynchus Dor Dorylaimidae SDor Small Dorylaimidae Plec Plectus PratPratylenchus Tylo Tylencholaimus N Total number of nematodes S Taxa richness EI Enrichment index SI Structure index BIBasal index CI Channel index Eigenvalues were 0568 and 0362 for the first and the second root respectively Percentage of varianceexplained was 330 for both root 1 and root 2
lenchus and Acrobeloides) were also associated with con-tinuous cropping The combined effect of standard tillageand continuous cropping significantly enhanced the abun-dance of nematodes at the entry level of the soil foodweb Bacterial-feeding nematodes influence C- and N-
mineralisation by feeding on bacteria excreting NH+4 and
by spreading bacteria through the soil (Bouwman et al1994 Fu et al 2005) Mesorhabditis and Acrobeloidestwo of the most abundant bacterial-feeders in our plotswere positively associated with NH+
4 a reasonable expec-
Fig 3 Scatter plot of CCA ordination showing relationships between soil properties and nematode taxa abundance (a) and soil foodweb indices taxa richness and total number of nematodes (b) Acro Acrobeles Acrob Acrobeloides Aphel Aphelenchus AphoAphelenchoides Aporce Aporcelaimidae Diph Diphtherophora Disco Discolaimus Dity Ditylenchus Meso Mesorhabditis MylMylonchulus Pan Panagrolaimus Plec Plectus Prat Pratylenchus Prion Prionchulus Qudsi Qusianematidae Tyl TylenchidaeTylen Tylenchorhynchus Eigenvalues were 097 and 096 (a) and 080 and 058 (b) for roots 1 and 2 respectively Percentages ofexplained variance for roots 1 and 2 were 107 and 110 (a) and 114 and 64 (b) respectively
710 Nematology
Effects of soil management on soil food webs
Vol 8(5) 2006 711
S Saacutenchez-Moreno et al
tation for the group associated with increased N mineral-isation (Ferris et al 1997 2004) By contrast Panagro-laimus and Plectus ordered in an opposite position due totheir negative relationship with PLFA biomarkers of fungiand bacteria and with bulk density Panagrolaimus has ahigh metabolic rate and a broad non-selective microbialfeeding habit (De Mesel et al 2004) It may decreasebacterial populations (as indicated by lower PFLA frombacterial markers) to a greater extent than other bacter-ial feeders in our plots When microbivorous nematodespredominate in soils they enhance N mineralisation andthus the availability of N for plants (Ferris et al 2004)Total soil N may be correlated with abundance of certainnematodes (Nakamoto et al 2006) but potentially min-eralisable N is a better indicator of N availability Thatmight explain why total soil N was associated only withabundance of Tylenchidae in this study Total C on thecontrary was more strongly associated with total nema-tode abundance
Surprisingly the abundance of fungal-feeding nema-todes such as Aphelenchus and some Tylenchidae was notrelated as strongly with ergosterol as expected suggest-ing that fungal biomass may not determining the size offungal feeder populations Villenave et al (2004) founddiffering responses of fungal feeders to ergosterol contentfungal feeders in cp groups 2 and 4 were positively relatedwith ergosterol but fungal feeders in the cp 5 group werenot
The discrimination between responses of nematodesin the higher and the lower levels of the soil food webwas evident in the CCA ordination revealing a link be-tween lower trophic levels and MBC NH+
4 ergosteroltotal N total C and certain PLFA Bacterial- fungal-and plant-feeding taxa with low cp values ordered op-posite to predatory and omnivore nematodes such asPrionchulus Qudsianematidae Aporcelaimidae Disco-laimus and Mylonchulus With the only exceptions ofthe plant-feeder Tylenchorhynchus (cp 3) which orderedclose to Mesorhabditis (cp 1) and Acrobeles (cp 2) whichscored close to the predators (cp 4 5) nematodes belong-ing to cp groups 1 and 2 showed an opposite response toenvironmental variables than those in cp groups 3 4 and 5
Predatory and omnivore nematodes are in higher co-loniser-persistent groups (3) and are more sensitive tosoil perturbation Intermittent fallow and standard tillagesupported higher abundances of most of the predators andomnivores Mylonchulus Qudsianematidae Prionchulusand Aporcelaimidae It is generally accepted that nema-tode functional diversity decreases with increasing man-
Table 5 Summarized effects of treatments on nematode trophicgroups (Ba = bacterial-feeders Fu = fungal-feeders Pp =plant-feeders PO = predators and omnivores)
Standard tillage No-tillage
Fallow Small increase of Ba Decrease of BaSmall decrease of Fu Decrease of FuDecrease of Pp Small decrease of PpIncrease of PO Increase of POIncrease of SI values Increase of CI values
Continuous Increase of Ba Small decrease of Bacropping Small increase of Fu Increase of Fu
Increase of Pp Increase of PpDecrease of PO Decrease of POIncrease of EI values Increase of BI values
agement intensity (Mulder et al 2003) predatory nema-todes were in our case much more affected by the crop-ping pattern (being enhanced in the intermittent fallowtreatment) than by standard tillage Our results thus sug-gest that even though predatory nematodes are sensitive tosoil physical perturbation other soil forces can drive theirabundance In some studies 25 years of tillage did notstrongly affect predators but reduced fungal-feeder nema-todes (Wang et al 2004)
An increase in predator and omnivore nematodes wasexpected in CC treatments as a result of the continuousincorporation of C into the soil but was not found (Ta-ble 5) Minoshima et al (2006) found that nematodesin the higher trophic levels were not significantly asso-ciated with the C pools in the soil Previous studies foundomnivore and predatory nematodes much more abundantin recently abandoned fallow fields than in cultivated orseminatural meadow lands (Haacutenel 2003) Polis et al(2000) suggest that trophic cascades produced by com-plex trophic interactions are abundant in soil systemsbut bottom-up regulation is difficult to demonstrate insoil trophic levels due to the high complexity of the soilbiota interactions In forest soils Salomon et al (2006)found more abundant microbial grazers when abundantresources were added to the soil but the effects did notextend into higher trophic levels of the soil food webleading to the conclusion that the availability of resourcesplays a minor role structuring soil food webs
Responses of plant-parasites and root feeders to tillageare usually difficult to interpret and are more closely re-lated to plant status and phenology than to soil propertiesThe association between Pratylenchus (endoparasite) andstandard tillage might be explained by the release of the
712 Nematology
Effects of soil management on soil food webs
nematodes from the roots as a result of tillage (Lenz ampEisenbeis 2000)
Ammonium MBC C K P and ergosterol were pos-itively related with total number of nematodes and theEI The EI is based on the weighted abundance of bacte-rial feeding nematodes enrichment-opportunistic relativeto longer life cycle bacterial-feeders indicating highlyactive bacterial-mediated decomposition channels Whenthe field is organically enriched these nematodes exploitthe abundant resources (fungi and bacteria) and increaserapidly in abundance due to their short life cycles and highfecundity (Bongers 1990) On the contrary high valuesof the CI indicate slower fungal-mediated decompositionpathways so a significant relationship between CI and er-gosterol was expected but not found CI was positivelycorrelated with PLFA of fungal biomarkers and EI wasnegatively correlated with PLFA of bacterial markers butnot correlated with MBC Thus the relationship betweenPLFA and microbial grazers may reflect the strength of thegrazing pressure at the sampling time The prevalence ofopportunistic bacterial feeders over other microbial feed-ers (as expressed by the EI) may decrease bacterial bio-mass (indicated by PLFA of bacterial markers) more obvi-ously than the effect of fungal feeders on fungal biomassas indicated by the positive association between the CIindicator of the prevalence of fungal-feeding nematodesover bacterial feeders with fungal biomass (inferred fromPLFA of fungal markers) The absence of correlation be-tween MBC and nematode populations may thus indicatethat the grazing pressure affects only certain microbes andnot the total microbial community
CI and BI were strongly correlated and associatedwith deeper soil layers and no tillage across all samplingdates High BI values indicate a nematode assemblagecomposed of perturbation-resistant nematodes mainly oflower trophic levels The community structure was in thiscase associated with fungal-dominated organic matterdecomposition pathways The SI was associated withdeeper soil layers and intermittent fallow suggesting anegative relationship between predator abundance and thehigh physical disturbance and biological activity presentat the soil surface and in the continuous cropping plots
Conclusions
Different tillage practices and cropping systems deter-mine soil properties and thus nematode abundance Theseeffects vary with nematode trophic and functional group
By the end of the experiment each treatment supporteddifferent nematode assemblages and soil food webs
Each soil food web index describes a model nema-tode assemblage (Ferris et al 2001) Our four treat-ments structured four different nematode assemblagesThe combination of standard tillage and continuous crop-ping (STCC) was associated with high EI values reflect-ing an assemblage predominantly composed of bacterial-feeding nematodes with short life cycles This enrichedassemblage was especially characteristic of the upper soillayer Perhaps not surprisingly for a long-disturbed agri-cultural system we did not find the relationships we ex-pected between continuous cropping and the abundanceof predator and omnivore nematodes The organisms inthe higher levels of the soil food web did not respond tothe continuous input of C in the soil and a long recoveryperiod may be required for appropriate taxa to be rein-troduced and to increase Intermittent fallow (especiallySTF) supported a longer more structured soil food web(high SI values) especially in the deeper soil layers Thecombination of no tillage and intermittent fallow (NTF)supported a fungal-based community with slower organicmatter decomposition rates especially below the upper 5cm of soil The accumulation of plant residues on the soilsurface may result in slower incorporation of C into thefood web and exploitation by fungi Indeed the absenceof tillage and thus of physical perturbation would not dis-rupt fungal hyphae Finally the combination of no tillageand continuous cropping (NTCC) supported a less well-defined assemblage dominated by basal perturbation-resistant nematodes
Acknowledgements
This research was supported by California Bay DeltaAuthority (CBDA)-Ecosystem Restoration Program grant ERP-02-P36 by the California Department of Food andAgricultureKearney Foundation of Soil Science Projects2003011 and by the Kearney Foundation of Soil ScienceProject 2005210 We thank the LTRAS staff for fieldmanagement Many thanks to members of the Jackson andTemple lab groups for help with sampling and Dr S Goyalfor guidance with the HPLC
References
ADEDIRAN JA ADEGBITE AA AKINLOSOTU TAAGBAJE GO TAIWO LB OWOLADE OF amp
Vol 8(5) 2006 713
S Saacutenchez-Moreno et al
OLUWATOSIN GA (2005) Evaluation of fallow and covercrops for nematode suppression in three agroecologies ofsouth western Nigeria African Journal of Biotechnology 41034-1039
BERKELMANS R FERRIS H TENUTA M amp VAN
BRUGGEN AHC (2003) Effects of long-term crop man-agement on nematode trophic levels other than plant feedersdisappear after 1 year of disruptive soil management AppliedSoil Ecology 23 223-235
BONGERS T (1990) The maturity index an ecological mea-sure of environmental disturbance based on nematode speciescomposition Oecologia 83 14-19
BONGERS T amp BONGERS M (1998) Functional diversity ofnematodes Applied Soil Ecology 10 239-251
BOSSIO DA SCOW KM GUNAPALA N amp GRAHAMKJ (1998) Determinants soil microbial communities ef-fects of agricultural management season and soil type onphospholipids fatty acid profiles Microbial Ecology 36 1-12
BOUWMAN LA BLOEM J VAN DEN BOOGERT PHJFBREMER F HOENDERBOOM GHJ amp DE RUITER PC(1994) Short-term and long-term effects of bacterivorousnematodes and nematophagous fungi on carbon and nitrogenmineralization in microcosms Biology and Fertility of Soils17 249-256
BULLUCK III LR BARKER KR amp RISTAINO JB (2002)Influences of organic and synthetic soil fertility amendmentson nematode trophic groups and community dynamics undertomatoes Applied Soil Ecology 21 233-250
CADET P PATEacute E amp NrsquoDIAYE-FAYE N (2003) Nematodecommunity changes and survival rates under natural fallow inthe sudano sahelian area of Senegal Pedobiologia 47 149-160
CHAN KY (2001) An overview of some tillage impacts onearthworm population abundance and diversity ndash implicationsfor functioning in soils Soil and Tillage Research 57 179-191
DE MESEL I DERYCKE S MOENS T VAN DER GUCHTK VINCX M amp SWINGS J (2004) Top-down impactof bacteriovorous nematodes on the bacterial communitystructure a microcosm study Environmental Microbiology 6733-744
EKSCHMITT E STIERHOF T DAUBER J KREIMES Kamp WOLTERS V (2003) On the quality of soil biodiversityindicators abiotic parameters as predictor of soil faunalrichness at different spatial scales Agriculture Ecosystemsand Environment 98 273-283
ETTEMA CH (1998) Soil nematode diversity species coex-istence and ecosystem function Journal of Nematology 30159-169
FERRIS H VENETTE RC amp LAU SS (1997) Populationenergetics of bacterial-feeding nematodes Carbon and nitro-gen budgets Soil Biology and Biochemistry 29 1183-1194
FERRIS H BONGERS T amp DE GOEDE RGM (2001) Aframework for soil food web diagnostics extension of the
nematode faunal analysis concept Applied Soil Ecology 1813-29
FERRIS H VENETTE RC amp SCOW KM (2004) Soil man-agement to enhance bacteriovore and fungivore nematodepopulations and their nitrogen mineralization function Ap-plied Soil Ecology 25 19-35
FISCUS DA amp NEHER DA (2002) Distinguishing sensi-tivity of free-leaving soil nematode genera to physical andchemical disturbances Ecological Applications 12 565-575
FU S FERRIS H BROWN D amp PLANT R (2005) Doespositive feedback effect of nematodes on the biomass andactivity of their bacteria prey vary with nematode speciesand population size Soil Biology and Biochemistry 37 1979-1987
GYEDU-ABABIO TK FURTENBERG JP BAIRD D ampVANREUSEL A (1999) Nematodes as indicators of pollu-tion a case study from the Swartkops river system SouthAfrica Hydrobiologia 397 155-169
HAacuteNEL L (2003) Recovery of soil nematode populations fromcropping stress by natural secondary succession to meadowland Applied Soil Ecology 22 255-270
KLADIVCO EJ (2001) Tillage systems and soil ecology Soiland Tillage Research 61 61-76
KORTHALS GW VAN DE ENDE A VAN MEGEN HLEXMOND THM KAMMENGA JE amp BONGERS T(1996) Short-term effects of cadmium copper nickel andzinc on soil nematodes from different feeding and life-historystrategy groups Applied Soil Ecology 4 107-117
LENZ R amp EISENBEIS G (2000) Short-term effects ofdifferent tillage in a sustainable farming system on nematodecommunity structure Biology and Fertility of Soils 31 237-244
LIPHADZI KB AL-KHATIB K BENSCH C STAHLMANPW DILLE JA TODD T RICE CW HORAK MJamp HEAD G (2005) Soil microbial and nematode commu-nities as affected by glyphosate and tillage practices in aglyphosate-resistant cropping system Weed Science 53 536-545
MIKOLA J amp SETAumlLAuml H (1998a) No evidence of trophiccascades in an experimental microbial-based soil food webEcology 79 153-164
MIKOLA J amp SETAumlLAuml H (1998b) Relating species diversityto ecosystem functioning mechanistic backgrounds and ex-perimental approach with a decomposer food web Oikos 83180-194
MINOSHIMA H JACKSON LE CAVAGNARO TRSAacuteNCHEZ-MORENO S FERRIS H TEMPLE S ampMITCHELL J (2006) Soil food webs and carbon dynam-ics in response to conservation tillage in legume rotations inCalifornia Soil Science Society of America in press
MULDER C DE ZWART D VAN WIJNEN HJSCHOUTEN AJ amp BREURE AM (2003) Observa-tional and simulated evidence of ecological shifts withinthe soil nematode community of agroecosystems under
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NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
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ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
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SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
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THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
YAMADA M (2001) Methods of control injury associatedwith continuous vegetable cropping in Japan ndash Crop rotationand several cultural practices Japan Agricultural ResearchQuarterly 35 39-45
YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
YEATES GW BONGERS T DE GOEDE RGM FRECK-MAN DW amp GEORGIEVA SS (1993) Feeding-habits insoil nematode families and genera ndash an outline for soil ecolo-gists Journal of Nematology 25 315-331
Vol 8(5) 2006 715
S Saacutenchez-Moreno et al
et al 2004 Adediran et al 2005 Roberts et al 2005)but important information on soil health and quality canbe derived from the entire nematode fauna (Urzelai et al2000 Neher 2001)
The positive effects of limiting physical disturbancemay include increases in abundance of the nematodefauna (Nakamoto et al 2006) Most organisms are moreabundant in no tillage than in conventional tillage systemsand larger-bodied organisms are especially sensitive tosoil disruption (Kladivko 2001) Thus earthworms areusually more abundant in non-tilled than in tilled soilsalthough some species react positively to tillage due to therapid incorporation of organic matter into the soil (Chan2001)
In a review of tillage effects on soil organisms Wardle(1995) reported that bacterial-feeding nematodes wereat least slightly stimulated by tillage in 65 of thestudies However in some studies total nematode densitywas reduced after the first tillage with bacterial feedersdominating in tilled plots and herbivores more abundant inno-tilled plots (Lenz amp Eisenbeis 2000) In other studiesthe density of herbivore nematodes was independent ofthe tillage system (Bulluck et al 2002) Where nematodedensities are greater in conventional than in no tillagesoils it is mainly due to greater abundances of bacterialand fungal feeders (Liphadzi et al 2005)
Fiscus and Neher (2002) developed a methodology fordistinguishing distinctive responses of nematode genera toagricultural management practices They concluded thatthe nematode taxa most sensitive to tillage were Aphelen-choides Discolaimus Eucephalobus Eudorylaimus He-terocephalobus and Wilsonema whilst Achromadora My-lonchulus Plectus and Prismatolaimus were among themost resistant to tillage effects
The maintenance of agricultural fields under bare fal-low conditions leads usually to a reduction in abundanceof plant-parasitic nematodes (Cadet et al 2003) Theeffects of bare fallow on free-living nematodes are notwell studied but they include reductions in abundance ofsome taxa (Pankhurst et al 2005) and greater nematodeabundance in the higher volumes of run-off water (Vil-lenave et al 2003) Compared with natural areas croppedfields support lower nematode diversity When croppingis abandoned and fields are allowed to revert to naturalconditions nematode diversity can increase significantly(Haacutenel 2003)
In a previous study (Minoshima et al 2006) we foundsignificant effects of tillage and continuous croppingsystems on C storage and other soil properties C storage
was higher in no-tillage than in standard tillage and withcontinuous cropping than in plots which had intermittentfallow periods Above ground plant biomass includingcrop yields was lower under no tillage than standardtillage
Our working hypotheses were based on the followingideas i) higher trophic levels of soil organisms includingnematodes are susceptible to disturbance ii) conventionalcropping systems that include periods of bare fallow donot supply sufficient C to the soil to sustain omnivores andpredators since C is respired by metabolically-active bac-terivore opportunists iii) omnivores and predators may in-crease with continuous cropping since C will be availableto support higher trophic levels iv) omnivores and preda-tors which are susceptible to disturbance should be moreabundant under no-tillage and v) soil food web structurewill be up-regulated by C inputs and slower degradationof soil C will occur in the no tillage continuous croppingtreatments
Some of these questions have been addressed in a previ-ous paper (Minoshima et al 2006) Therefore the objec-tives of the present study were to i) determine the sensi-tivity of nematode taxa to tillage and intermittent fallowtreatments at different soil depths in agricultural fieldsii) relate soil properties and nematode assemblage com-position to soil management and iii) determine whetherdifferent agricultural practices establish and maintain dif-ferent nematode assemblages and soil food webs
Materials and methods
STUDY SITE
The experiment was performed in the companion plotarea of the Long Term Research in Agricultural Systems(LTRAS) site at the University of California Davis Theexperimental plots were conventionally farmed for manydecades eg for oat hay The soil is classified as Rinconsilty clay loam (fine montmorillonitic thermic MollicHaploxeralfs) The four treatments were combinations ofintermittent fallow (F) or continuous cropping (CC) withstandard tillage (ST) and no-tillage (NT) In the NT plotsthere were no tillage operations during the study and cropresidues were spread on the top of the beds In the STplots crop residues were disked and incorporated to adepth of 20 cm between crops The cropping sequence inCC was a tomato (Lycopersicon esculentum) crop (plantedin spring 2003) sudan-sorghum (Sorghum bicolor) covercrop (planted in late summer) and a garbanzo (Cicer
704 Nematology
Effects of soil management on soil food webs
arietinum) crop (planted in late autumn) In 2004 thesummer crop was cowpeas (Vigna unguiculata) In theF treatments only tomato and garbanzo were plantedand the plots were fallow in autumn 2003 and summer2004 Four treatments were established as combinationsof both cropping pattern and tillage system NTCC (no-tillage + continuous cropping) STCC (standard tillage+ continuous cropping) NTF (no-tillage + intermittentfallow) and STF (standard tillage + intermittent fallow)
SOIL SAMPLING AND NEMATODE IDENTIFICATION
Soil was sampled in December 2003 June 2004September 2004 (only two treatments) and December2004 Soil samples were taken at three depths 0-5 cm5-15 cm and 15-30 cm Nematodes were extracted froma subsample of 350 g using a combination of decantingand sieving and Baermann funnel methods All nematodesin each sample were counted at low magnification andthen 100 nematodes (200 at the last sampling date) fromeach sample were identified to genus or family at highermagnification
Nematodes were classified by trophic habit (Yeates etal 1993) and by coloniser-persister (cp) groups (Bongers1990) The cp scale classifies nematode families in fivegroups from microbial feeders with short life cycles (cp1 and 2) to predators and omnivores with long life cyclesand greater sensitivity to environmental perturbations (cpgroups 4 and 5) Soil food web indices were calculatedafter Ferris et al (2001) based on the abundance of func-tional guilds (Bongers amp Bongers 1998) The StructureIndex (SI) is based on the relative abundance of highertrophic level nematodes and indicates soil food web lengthand soil resilience The Channel Index (CI) is calculatedas the proportion of fungal-feeding nematodes comparedto enrichment-opportunistic bacterial feeders and is anindicator of activity in the predominant decompositionchannels in the soil fungal mediated (higher values) orbacterial mediated (lower values) The Basal Index (BI) isan indicator of the prevalence of the general opportunisticnematodes that are tolerant of soil perturbation Finallythe Enrichment Index (EI) is an indicator of enrichmentopportunistic nematodes both fungal and bacterial feed-ers which respond rapidly to increases in food resourcesThe resilience of nematode trophic groups to tillage wascalculated according to Wardle (1995)
SOIL PROPERTIES
Microbial organic carbon (MBC) NH+4 NOminus
3 and er-gosterol were measured at all sampling dates Phospho-lipid fatty acids (PLFA) were used as indicators of bac-terial and fungal biomass in the soil Bacterial PLFAmarkers were iso 150 anteiso 150 150 iso 160161ω5c iso 170 anteiso 170 170cy 170 and 190cyFungal PLFA markers were 182ω 6 and 9c (Bossio etal 1998 Mikola amp Setaumllauml 1998a) Bulk density wasmeasured once in samples collected in February 2005For details of measurements of soil properties see Mi-noshima et al (2006) Soil physicochemical analyses (to-tal N total C soil pH K and plant available (Olsen)P) were performed by the University of CaliforniarsquosAgriculture and Natural Resources Analytical Laboratory(httpdanranlabucanrorg)
STATISTICAL ANALYSES
The influence of treatments on the nematode assem-blage across the four sampling dates was determined byCorrespondence Canonical Analysis (CCA) and by themethodology of Fiscus and Neher (2002) Nematode iden-tification at higher resolution was used to relate nematodetaxa with soil chemistry at the last sampling date (Decem-ber 2004) All variables were transformed as ln(x + 1)
to normalise data before the analyses ANOVA was usedto check the influence of categorical variables on nema-tode abundances and soil food web indices Correlationanalysis was used to check relationships between vari-ables Analyses were performed using STATISTICA soft-ware (StatSoft 1996)
Direct effects of tillage system cropping pattern anddepth
Differences in abundances of nematode taxa and foodweb indices were tested using General Linear Models Allthe nematological variables (nematode taxa abundancesand soil food web indices) and three categorical factors(tillage system cropping pattern and soil depth) weresubjected to CCA using data from the four samplingperiods (December 2003 June 2004 September 2004December 2004 n = 126)
In CCA bi-plots environmental axes are represented byarrows The length of the arrow indicates the importanceof the environmental variable for the ordination rootsIts direction indicates the correlation of the variable withother variables arrows in the same direction are positivelycorrelated while arrows pointing in opposite directions
Vol 8(5) 2006 705
S Saacutenchez-Moreno et al
are negatively related Dependent variables (nematodetaxa and food web indices) located near an environmental(independent) variable suggest a positive effect of thelatter on the former
Indirect effects of tillage system cropping pattern anddepth
Data from the last sampling date were subjected toANOVA to test differences in the soil properties amongtreatments Nematode abundances and soil propertieswere used to perform multivariate analyses (CCA) ofthe state of the nematode assemblage at the end ofthe cropping cycle (December 2004 n = 36) In theseanalyses nematode data were expressed at the highestlevel of taxonomic resolution available
Results
DIRECT EFFECTS OF TILLAGE SYSTEM CROPPING
PATTERN AND DEPTH
Cropping pattern tillage system and depth affected thecomposition of the nematode fauna and food web indicesacross the four sampling dates Tylenchidae Rhabditi-dae Acrobeloides and Pratylenchus were more abundantin continuously cropped plots while Dorylaimidae weremore abundant in the intermittent fallow treatments (Ta-ble 1) Consequently number of nematodes was lower andthe SI was higher under intermittent fallow (Table 2)
Tillage directly affected Aphelenchus and Rhabditidaewhich were more abundant in ST plots and Tylenchidaemore abundant in the NT treatments Depth affected Aphe-lenchus Tylenchidae Panagrolaimus and Dorylaimidaewhich were more abundant in the upper soil layers (0-15 cm) The CI was higher in NT plots Both BI and CIwere lower in the upper soil where EI was higher (Ta-ble 2)
Following Wardlersquos methodology to infer the resilienceof soil organisms to tillage (Wardle 1995) nematodes as awhole were mildly stimulated by tillage (V index = 014)In fact the response of nematodes varied depending ontheir trophic group bacterial-feeders and fungal-feederswere mildly stimulated by tillage (V = 029 and 003respectively) and herbivores and predators and omnivoreswere mildly inhibited by tillage (V = minus006 and minus0004respectively) By the same logic bacterial fungal andplant feeders were inhibited and predators and omnivoresstimulated by intermittent fallow (Fig 1)
Direct effects of cropping intensity tillage system anddepth on the nematode faunal data across the four sam-
Fig 1 V index values for nematode trophic groups (Ba =bacterial-feeders Fu = fungal-feeders Pp = plant parasitesPO = predators and omnivores) sensitivity to tillage (T) andfallow (F) Positive values indicate stimulation negative valuesindicate inhibition (after Wardle 1995)
pling dates were analysed and expressed in a CCA bi-plotTylenchidae were associated with CC and negatively af-fected by the F treatments while Aphelenchus Acrobeloi-des Rhabditidae and Panagrolaimus were positively asso-ciated with ST and negatively affected by soil depth theywere most abundant in the upper soil layers
For the four sampling dates the CI and the SI werehigher in the 15-30 cm depth and were associated withNT and F The EI was associated positively with uppersoil and the BI with medium depths and F (Fig 2)
Following Fiscus and Neher (2002) the analysis ofthe direct effects of tillage cropping pattern and depthon the nematode assemblage along the four samplingdates allowed classification of nematode taxa and foodweb descriptors as functions of their associations witheach variable Nematodes were classified as tolerant totillage if positioned in the bi-plot area defined by STand sensitive if positioned in the opposite half indicatingassociation with NT The same logic was used to scoreeach nematode taxon as sensitive or resistant to fallow andto infer associations with different soil depths (Table 3)
INDIRECT EFFECT OF TILLAGE AND COVER CROPS
Relationship between environmental variables andmanagement
On the last sampling date (December 2004) soil pHNOminus
3 and bulk density varied among the treatments pHand bulk density were higher in the NT treatments NOminus
3was significantly higher in STCC Total C total N pHergosterol and bulk density were all significantly affectedby tillage system and were higher in NT (Table 4)
Soil properties were in general strongly correlatedSoil pH and C N P and K concentrations were positively
706 Nematology
Effects of soil management on soil food websTa
ble
1E
ffect
sof
crop
ping
patt
ern
till
age
syst
eman
dso
ilde
pth
onab
unda
nce
ofne
mat
ode
taxa
(num
ber
ofne
mat
odes
100
gso
il)
Fva
lues
and
leve
lofs
igni
fican
cear
ein
dica
ted
(ns=
nots
igni
fican
t)D
ata
are
from
the
four
sam
plin
gda
tes
(n=
126)
Cro
ppin
gT
illag
eD
epth
Uni
vari
ate
effe
cts
F=
529
P
lt0
0001
F=
575
P
lt0
0001
F=
198
P
lt0
01
Con
tinuo
usFa
llow
No-
till
Stan
dard
0-5
cm5-
15cm
15-3
0cm
Cro
ppin
gT
illag
eD
epth
crop
ping
Aph
elen
chus
127
84plusmn
104
911
688
plusmn12
11
100
07plusmn
921
144
65plusmn
133
312
651
plusmn15
47
167
63plusmn
154
175
29
plusmn6
72ns
Plt
001
Plt
005
Tyle
nchi
dae
233
71plusmn
153
913
210
plusmn17
77
209
73plusmn
188
515
608
plusmn16
60
180
23plusmn
211
823
802
plusmn26
52
152
25plusmn
163
9P
lt0
001
Plt
005
Plt
001
Acr
obel
oide
s13
355
plusmn16
22
739
5plusmn
187
363
29
plusmn11
54
144
20plusmn
234
711
288
plusmn17
60
131
10plusmn
268
880
03
plusmn21
74
Plt
005
nsns
Pana
grol
aim
us14
108
plusmn34
50
123
28plusmn
398
411
335
plusmn33
48
151
01plusmn
403
231
343
plusmn67
07
580
0plusmn
182
728
92
plusmn7
55ns
nsP
lt0
001
Rha
bditi
dae
135
08plusmn
203
057
76
plusmn23
44
499
3plusmn
124
314
291
plusmn32
24
126
05plusmn
269
412
482
plusmn39
03
549
5plusmn
160
0P
lt0
05P
lt0
01Ty
lenc
horh
ynch
us19
29
plusmn4
9828
47
plusmn5
7526
15
plusmn4
1721
61
plusmn6
5316
89
plusmn6
5834
46
plusmn8
4718
32
plusmn2
93ns
nsns
Dor
ylai
mid
ae27
57
plusmn5
7648
78
plusmn6
6537
40
plusmn6
5838
94
plusmn5
6448
10
plusmn11
67
374
9plusmn
470
243
8plusmn
299
Plt
005
nsP
lt0
05Sm
all
197
plusmn0
671
08plusmn
078
251
plusmn0
900
54plusmn
024
164
plusmn0
962
59plusmn
110
054
plusmn0
30ns
nsns
Dor
ylai
mid
aeP
lect
us8
13plusmn
175
440
plusmn2
027
41plusmn
226
512
plusmn1
1010
24
plusmn3
334
93plusmn
155
443
plusmn1
30P
raty
lenc
hus
305
0plusmn
585
124
8plusmn
675
157
6plusmn
348
272
2plusmn
883
436
plusmn1
2421
58
plusmn5
6642
38
plusmn11
62
Plt
005
nsP
lt0
05Ty
lenc
hola
imus
101
plusmn0
430
36plusmn
050
070
plusmn0
260
66plusmn
064
042
plusmn0
250
93plusmn
087
084
plusmn0
38ns
nsns
Tabl
e2
Effe
cts
ofcr
oppi
ngpa
tter
nti
llag
esy
stem
and
soil
dept
hon
soil
food
web
indi
ces
(EI=
Enr
ichm
ent
inde
xSI
=St
ruct
ure
inde
xB
I=
Bas
alin
dex
CI=
Cha
nnel
inde
x)t
otal
num
ber
ofne
mat
odes
(N)
and
taxa
rich
ness
(S)
Fva
lues
and
leve
lof
sign
ifica
nce
are
indi
cate
d(n
s=
not
sign
ifica
nt)
Dat
aar
efr
omth
efo
ursa
mpl
ing
date
s(n
=12
6)
Cro
ppin
gT
illag
eD
epth
Uni
vari
ate
F=
452
P
lt0
0001
F=
269
P
lt0
05F
=5
34
Plt
000
01
Con
tinuo
usFa
llow
No-
tilla
geSt
anda
rd0-
5cm
5-15
cm15
-30
cmC
ropp
ing
Till
age
Dep
thcr
oppi
ng
N85
972
plusmn64
35
599
53plusmn
800
362
631
plusmn66
25
832
94plusmn
878
194
076
plusmn10
665
821
56plusmn
960
448
232
plusmn61
25
Plt
005
nsP
lt0
01S
761
plusmn0
157
85plusmn
012
781
plusmn0
127
65plusmn
015
745
plusmn0
157
74plusmn
017
795
plusmn0
17ns
nsP
lt0
05E
I65
66
plusmn2
0166
64
plusmn1
7264
77
plusmn1
5267
53
plusmn2
2073
58
plusmn1
7960
63
plusmn2
2064
03
plusmn2
30ns
nsP
lt0
01SI
262
9plusmn
315
436
2plusmn
209
343
3plusmn
259
355
7plusmn
300
291
1plusmn
364
297
7plusmn
283
422
7plusmn
332
Plt
000
1ns
Plt
001
BI
297
6plusmn
172
264
1plusmn
149
291
4plusmn
137
270
2plusmn
186
229
0plusmn
161
335
0plusmn
202
285
6plusmn
191
nsns
Plt
005
CI
408
5plusmn
371
432
6plusmn
320
471
7plusmn
328
369
3plusmn
348
239
3plusmn
233
533
4plusmn
417
483
7plusmn
428
nsP
lt0
001
Plt
001
Vol 8(5) 2006 707
S Saacutenchez-Moreno et al
Table 3 Direct effects of tillage (ST = standard tillage NT = no-till) cropping pattern (F = fallow CC = continuous cropping)and soil depth (0-5 5-15 and 15-30 cm) on abundance ofnematode taxa and on soil food web indices (S = taxa richnessN = total number of nematodes EI = Enrichment index SI =Structure index BI = Basal index CI = Channel index) Trophicgroup (Ba = bacterial feeders Fu = fungal feeders Pp = plantparasites P = predators O = omnivores) of nematode taxa areindicated
Trophic Cp Tillage Cropping Depthgroup pattern (cm)
Aphelenchus Fu 2 ST CC 0-5Tylenchidae PpFu 2 NT CC 5-15Acrobeloides Ba 2 ST CC 0-5Panagrolaimus Ba 1 ST CC 0-5Rhabditidae Ba 1 ST CC 0-5Tylenchorhynchus Pp 3 NT F 5-15Dorylaimidae O 4 ST F 5-15Small Dorylaimidae O 4 NT CC 5-15Plectus Ba 2 NT CC 5-15Pratylenchus Pp 3 NT CC 5-15Tylencholaimus Fu 4 NT CC 5-15N ST CC 0-5S NT F 5-15EI ST CC 0-5SI ST F 15-30BI NT CC 5-15CI NT F 15-30
related (r between 049 and 083 P lt 005) NH+4
was associated with intermittent fallow and correlatedwith ergosterol and MBC (r between 049 and 052P lt 005) PLFA of fungal markers were correlated withergosterol (r = 035 P lt 005) and with PLFA ofbacterial markers (r = 095 P lt 005)
Influence of environmental variables on nematode taxaand soil food web descriptors
In December 2004 at the end of the experiment inthe ordination of the nematode taxa in the multivariatespace defined by the environmental variables positivevalues for most of the soil properties grouped togetherindicating soil enrichment and high biological activity(Fig 3a b) The PLFA biomarkers of both bacteria andfungi were related with the abundance of AcrobeloidesMesorhabditis and Tylenchorhynchus Panagrolaimus andAcrobeles both bacterial feeders were not correlated witheither group of PLFAs and ordered in the opposite part ofthe graph Tylenchidae was associated with pH (r = 047P lt 005) Aphelenchoides was associated with NOminus
3
The abundance of all the omnivores and predators(Discolaimus Aporcelaimidae Qudsianematidae and My-lonchulus) except Prionchulus were inversely correlatedwith almost all soil properties The EI was negativelycorrelated with the CI (r = minus093 P lt 005) BI(r = minus095 P lt 005) taxa richness (r = minus056P lt 005) bulk density (r = minus040 P lt 005) andPLFA of bacterial markers (r = minus035 P lt 005) It waspositioned in the opposite part of the graph than BI andCI (Fig 3) CI was positively correlated with bulk densityand PLFA of fungal markers (r = 037 and 034 respec-tively P lt 005) SI was negatively correlated with NOminus
3 pH and K (r = minus037 minus033 and minus034 P lt 005)Taxa richness and number of nematodes were negativelycorrelated (r = minus036 P lt 005) Number of nematodeswas associated with total C and taxa richness with bulkdensity CI and BI were positively correlated (r = 086P lt 005)
Discussion
The aim of this study was to evaluate the relationshipsbetween nematode faunal composition and soil propertiesas determined by agricultural management It is generallyaccepted that nematodes are strongly influenced by theirmicroenvironment and provide a useful reflection ofsoil health status and several soil functions (Mulder etal 2005) The use of multivariate statistics especiallyCanonical Analysis has improved the understanding ofthe complex relationships between different groups of soilfauna and between organisms and soil physical-chemicalproperties (Popovici amp Ciobanu 2000 Wardle et al2001 Fiscus amp Neher 2002)
As expected from previous studies (eg Wardle 1995)total nematode abundance was not strongly influenced bytillage due to the varied responses of different taxa Ne-matode responses to tillage and cropping intensity var-ied with their trophic group bacterial feeders and fun-gal feeders were stimulated by tillage and reduced un-der intermittent fallow plant-feeders were generally in-hibited by both tillage and intermittent fallow and preda-tors and omnivores were stimulated by intermittent fallowand did not respond clearly to tillage practices In factthe few omnivores and predators in this and most agri-cultural fields probably represent the more tolerant taxawithin these trophic levels Taxa intolerant to disturbancemay no longer be present in arable soils These observa-tions agree with Lenz and Eisenbeis (2000) who found nochanges in total nematode abundance and an increase of
708 Nematology
Effects of soil management on soil food webs
Table 4 Average values (plusmn SE) of soil properties in the four different treatments across three depths Significant effects of treatments(NTCC STCC STF NTF) crop pattern (CC and F) and tillage (ST and NT) are indicated by level of significance Data are from thelast sampling date (December 2004 n = 36) Data from Minoshima et al (2006)
NTF STF NTCC STCC Treatment Crop Tillage
Total C () 106 plusmn 003 099 plusmn 001 107 plusmn 004 103 plusmn 002 P lt 005Total N () 012 plusmn 000 011 plusmn 000 012 plusmn 000 012 plusmn 000 P lt 005pH 707 plusmn 003 686 plusmn 003 708 plusmn 006 690 plusmn 004 P lt 001 P lt 0001K (mg lminus1) 700 plusmn 049 591 plusmn 013 786 plusmn 132 734 plusmn 080P (microg gminus1) 1738 plusmn 088 1578 plusmn 031 1908 plusmn 217 1598 plusmn 083NO3 454 plusmn 106 550 plusmn 148 646 plusmn 092 1203 plusmn 253 P lt 005 P lt 005
(microg N gminus1)
NH4 236 plusmn 131 127 plusmn 054 116 plusmn 027 106 plusmn 016(microg N gminus1)
MBC 17123 plusmn 2623 14816 plusmn 1905 26275 plusmn 6398 17158 plusmn 1823(microg C gminus1)
Ergosterol 99932 plusmn 16846 57594 plusmn 3631 224691 plusmn 82975 121820 plusmn 25685 P lt 005(ng gminus1)
Bulk density 134 plusmn 002 125 plusmn 003 132 plusmn 002 125 plusmn 002 P lt 005 P lt 001(gcm3)
PLFAba 190753 plusmn 50529 144540 plusmn 35185 230127 plusmn 55833 208676 plusmn 31240(mgm2)
PLFAfu 24662 plusmn 12047 14295 plusmn 4381 55785 plusmn 26261 27208 plusmn 7651(mgm2)
bacterial-feeder nematodes after the first tillage treatmentOur results indicate that the response of total nematodeabundance to management depends on the assemblagecomposition so no general patterns can be discerned with-out analysing separately the taxa and functional group re-sponses For example Liphadzi et al (2005) found gen-eral increase in nematode abundance in tilled plots due tothe predominance of fungal feeders and bacterial feeders(up to 90) in the assemblages they studied
Throughout the four sampling dates of this study mostof the microbial feeders (Panagrolaimus RhabditidaeAphelenchus and Acrobeloides) were positively associ-ated with standard tillage indicating the stimulatory effecton microbes of incorporating organic matter into the soilThe nematodes less responsive to incorporated organicmatter were the higher cp taxa (Tylenchorhynchus Tylen-cholaimus Pratylenchus and some Dorylaimidae) whichwere associated with no-tillage Even though a greaternumber of taxa (especially of upper trophic levels) andhigher resolution identification would be desirable to in-fer relationships more reliably (Yeates 2003 Mulder etal 2005) we observed significant relationships betweensensitivity to tillage and trophic or cp groups as similarlyreported by Fiscus and Neher (2002)
Plectus was the only bacterivore associated with thesoil properties of the NT treatments suggesting a highersensitivity to tillage practices While Fiscus and Neher(2002) suggested that Plectus is an indicator of distur-bance due to the concordance between its cp value (2)and its tolerance to chemical and mechanical perturba-tions we found it to be more sensitive to tillage than ex-pected from its cp value Different responses among ge-nera in the same trophic group are common (Porazinska etal 1999) and nematode genera within the same trophicgroup can exhibit asymmetric competition negatively in-fluencing the abundance of other genera (Postma-Blaaw etal 2005) so responses to perturbation may be influencedby the presence of other nematode taxa Greater taxo-nomic resolution may be necessary to resolve differencesin response to environmental variables among nematodeswithin higher taxonomic groupings (Yeates 2003) espe-cially for taxa that have numerous species and a broad sizerange (eg Plectus)
Bacterial feeders are usually abundant in cultivatedsoils while predators and omnivores often disappear withcultivation (Wardle et al 1995) Microbivorous nema-todes belonging to the cp 1 group (eg Panagrolaimusor Rhabditidae enrichment-opportunistic nematodes) andthose with longer life cycles in the cp 2 group (eg Aphe-
Vol 8(5) 2006 709
S Saacutenchez-Moreno et al
Fig 2 Canonical correspondence analysis bi-plot of effects of tillage system crop pattern and depth on nematode abundances andsoil food web indices Environmental variables are marked by arrows Aphel Aphelenchus Tyl Tylenchidae Acro Acrobeloides PanPanagrolaimus Rhab Rhabditidae Tylen Tylenchorhynchus Dor Dorylaimidae SDor Small Dorylaimidae Plec Plectus PratPratylenchus Tylo Tylencholaimus N Total number of nematodes S Taxa richness EI Enrichment index SI Structure index BIBasal index CI Channel index Eigenvalues were 0568 and 0362 for the first and the second root respectively Percentage of varianceexplained was 330 for both root 1 and root 2
lenchus and Acrobeloides) were also associated with con-tinuous cropping The combined effect of standard tillageand continuous cropping significantly enhanced the abun-dance of nematodes at the entry level of the soil foodweb Bacterial-feeding nematodes influence C- and N-
mineralisation by feeding on bacteria excreting NH+4 and
by spreading bacteria through the soil (Bouwman et al1994 Fu et al 2005) Mesorhabditis and Acrobeloidestwo of the most abundant bacterial-feeders in our plotswere positively associated with NH+
4 a reasonable expec-
Fig 3 Scatter plot of CCA ordination showing relationships between soil properties and nematode taxa abundance (a) and soil foodweb indices taxa richness and total number of nematodes (b) Acro Acrobeles Acrob Acrobeloides Aphel Aphelenchus AphoAphelenchoides Aporce Aporcelaimidae Diph Diphtherophora Disco Discolaimus Dity Ditylenchus Meso Mesorhabditis MylMylonchulus Pan Panagrolaimus Plec Plectus Prat Pratylenchus Prion Prionchulus Qudsi Qusianematidae Tyl TylenchidaeTylen Tylenchorhynchus Eigenvalues were 097 and 096 (a) and 080 and 058 (b) for roots 1 and 2 respectively Percentages ofexplained variance for roots 1 and 2 were 107 and 110 (a) and 114 and 64 (b) respectively
710 Nematology
Effects of soil management on soil food webs
Vol 8(5) 2006 711
S Saacutenchez-Moreno et al
tation for the group associated with increased N mineral-isation (Ferris et al 1997 2004) By contrast Panagro-laimus and Plectus ordered in an opposite position due totheir negative relationship with PLFA biomarkers of fungiand bacteria and with bulk density Panagrolaimus has ahigh metabolic rate and a broad non-selective microbialfeeding habit (De Mesel et al 2004) It may decreasebacterial populations (as indicated by lower PFLA frombacterial markers) to a greater extent than other bacter-ial feeders in our plots When microbivorous nematodespredominate in soils they enhance N mineralisation andthus the availability of N for plants (Ferris et al 2004)Total soil N may be correlated with abundance of certainnematodes (Nakamoto et al 2006) but potentially min-eralisable N is a better indicator of N availability Thatmight explain why total soil N was associated only withabundance of Tylenchidae in this study Total C on thecontrary was more strongly associated with total nema-tode abundance
Surprisingly the abundance of fungal-feeding nema-todes such as Aphelenchus and some Tylenchidae was notrelated as strongly with ergosterol as expected suggest-ing that fungal biomass may not determining the size offungal feeder populations Villenave et al (2004) founddiffering responses of fungal feeders to ergosterol contentfungal feeders in cp groups 2 and 4 were positively relatedwith ergosterol but fungal feeders in the cp 5 group werenot
The discrimination between responses of nematodesin the higher and the lower levels of the soil food webwas evident in the CCA ordination revealing a link be-tween lower trophic levels and MBC NH+
4 ergosteroltotal N total C and certain PLFA Bacterial- fungal-and plant-feeding taxa with low cp values ordered op-posite to predatory and omnivore nematodes such asPrionchulus Qudsianematidae Aporcelaimidae Disco-laimus and Mylonchulus With the only exceptions ofthe plant-feeder Tylenchorhynchus (cp 3) which orderedclose to Mesorhabditis (cp 1) and Acrobeles (cp 2) whichscored close to the predators (cp 4 5) nematodes belong-ing to cp groups 1 and 2 showed an opposite response toenvironmental variables than those in cp groups 3 4 and 5
Predatory and omnivore nematodes are in higher co-loniser-persistent groups (3) and are more sensitive tosoil perturbation Intermittent fallow and standard tillagesupported higher abundances of most of the predators andomnivores Mylonchulus Qudsianematidae Prionchulusand Aporcelaimidae It is generally accepted that nema-tode functional diversity decreases with increasing man-
Table 5 Summarized effects of treatments on nematode trophicgroups (Ba = bacterial-feeders Fu = fungal-feeders Pp =plant-feeders PO = predators and omnivores)
Standard tillage No-tillage
Fallow Small increase of Ba Decrease of BaSmall decrease of Fu Decrease of FuDecrease of Pp Small decrease of PpIncrease of PO Increase of POIncrease of SI values Increase of CI values
Continuous Increase of Ba Small decrease of Bacropping Small increase of Fu Increase of Fu
Increase of Pp Increase of PpDecrease of PO Decrease of POIncrease of EI values Increase of BI values
agement intensity (Mulder et al 2003) predatory nema-todes were in our case much more affected by the crop-ping pattern (being enhanced in the intermittent fallowtreatment) than by standard tillage Our results thus sug-gest that even though predatory nematodes are sensitive tosoil physical perturbation other soil forces can drive theirabundance In some studies 25 years of tillage did notstrongly affect predators but reduced fungal-feeder nema-todes (Wang et al 2004)
An increase in predator and omnivore nematodes wasexpected in CC treatments as a result of the continuousincorporation of C into the soil but was not found (Ta-ble 5) Minoshima et al (2006) found that nematodesin the higher trophic levels were not significantly asso-ciated with the C pools in the soil Previous studies foundomnivore and predatory nematodes much more abundantin recently abandoned fallow fields than in cultivated orseminatural meadow lands (Haacutenel 2003) Polis et al(2000) suggest that trophic cascades produced by com-plex trophic interactions are abundant in soil systemsbut bottom-up regulation is difficult to demonstrate insoil trophic levels due to the high complexity of the soilbiota interactions In forest soils Salomon et al (2006)found more abundant microbial grazers when abundantresources were added to the soil but the effects did notextend into higher trophic levels of the soil food webleading to the conclusion that the availability of resourcesplays a minor role structuring soil food webs
Responses of plant-parasites and root feeders to tillageare usually difficult to interpret and are more closely re-lated to plant status and phenology than to soil propertiesThe association between Pratylenchus (endoparasite) andstandard tillage might be explained by the release of the
712 Nematology
Effects of soil management on soil food webs
nematodes from the roots as a result of tillage (Lenz ampEisenbeis 2000)
Ammonium MBC C K P and ergosterol were pos-itively related with total number of nematodes and theEI The EI is based on the weighted abundance of bacte-rial feeding nematodes enrichment-opportunistic relativeto longer life cycle bacterial-feeders indicating highlyactive bacterial-mediated decomposition channels Whenthe field is organically enriched these nematodes exploitthe abundant resources (fungi and bacteria) and increaserapidly in abundance due to their short life cycles and highfecundity (Bongers 1990) On the contrary high valuesof the CI indicate slower fungal-mediated decompositionpathways so a significant relationship between CI and er-gosterol was expected but not found CI was positivelycorrelated with PLFA of fungal biomarkers and EI wasnegatively correlated with PLFA of bacterial markers butnot correlated with MBC Thus the relationship betweenPLFA and microbial grazers may reflect the strength of thegrazing pressure at the sampling time The prevalence ofopportunistic bacterial feeders over other microbial feed-ers (as expressed by the EI) may decrease bacterial bio-mass (indicated by PLFA of bacterial markers) more obvi-ously than the effect of fungal feeders on fungal biomassas indicated by the positive association between the CIindicator of the prevalence of fungal-feeding nematodesover bacterial feeders with fungal biomass (inferred fromPLFA of fungal markers) The absence of correlation be-tween MBC and nematode populations may thus indicatethat the grazing pressure affects only certain microbes andnot the total microbial community
CI and BI were strongly correlated and associatedwith deeper soil layers and no tillage across all samplingdates High BI values indicate a nematode assemblagecomposed of perturbation-resistant nematodes mainly oflower trophic levels The community structure was in thiscase associated with fungal-dominated organic matterdecomposition pathways The SI was associated withdeeper soil layers and intermittent fallow suggesting anegative relationship between predator abundance and thehigh physical disturbance and biological activity presentat the soil surface and in the continuous cropping plots
Conclusions
Different tillage practices and cropping systems deter-mine soil properties and thus nematode abundance Theseeffects vary with nematode trophic and functional group
By the end of the experiment each treatment supporteddifferent nematode assemblages and soil food webs
Each soil food web index describes a model nema-tode assemblage (Ferris et al 2001) Our four treat-ments structured four different nematode assemblagesThe combination of standard tillage and continuous crop-ping (STCC) was associated with high EI values reflect-ing an assemblage predominantly composed of bacterial-feeding nematodes with short life cycles This enrichedassemblage was especially characteristic of the upper soillayer Perhaps not surprisingly for a long-disturbed agri-cultural system we did not find the relationships we ex-pected between continuous cropping and the abundanceof predator and omnivore nematodes The organisms inthe higher levels of the soil food web did not respond tothe continuous input of C in the soil and a long recoveryperiod may be required for appropriate taxa to be rein-troduced and to increase Intermittent fallow (especiallySTF) supported a longer more structured soil food web(high SI values) especially in the deeper soil layers Thecombination of no tillage and intermittent fallow (NTF)supported a fungal-based community with slower organicmatter decomposition rates especially below the upper 5cm of soil The accumulation of plant residues on the soilsurface may result in slower incorporation of C into thefood web and exploitation by fungi Indeed the absenceof tillage and thus of physical perturbation would not dis-rupt fungal hyphae Finally the combination of no tillageand continuous cropping (NTCC) supported a less well-defined assemblage dominated by basal perturbation-resistant nematodes
Acknowledgements
This research was supported by California Bay DeltaAuthority (CBDA)-Ecosystem Restoration Program grant ERP-02-P36 by the California Department of Food andAgricultureKearney Foundation of Soil Science Projects2003011 and by the Kearney Foundation of Soil ScienceProject 2005210 We thank the LTRAS staff for fieldmanagement Many thanks to members of the Jackson andTemple lab groups for help with sampling and Dr S Goyalfor guidance with the HPLC
References
ADEDIRAN JA ADEGBITE AA AKINLOSOTU TAAGBAJE GO TAIWO LB OWOLADE OF amp
Vol 8(5) 2006 713
S Saacutenchez-Moreno et al
OLUWATOSIN GA (2005) Evaluation of fallow and covercrops for nematode suppression in three agroecologies ofsouth western Nigeria African Journal of Biotechnology 41034-1039
BERKELMANS R FERRIS H TENUTA M amp VAN
BRUGGEN AHC (2003) Effects of long-term crop man-agement on nematode trophic levels other than plant feedersdisappear after 1 year of disruptive soil management AppliedSoil Ecology 23 223-235
BONGERS T (1990) The maturity index an ecological mea-sure of environmental disturbance based on nematode speciescomposition Oecologia 83 14-19
BONGERS T amp BONGERS M (1998) Functional diversity ofnematodes Applied Soil Ecology 10 239-251
BOSSIO DA SCOW KM GUNAPALA N amp GRAHAMKJ (1998) Determinants soil microbial communities ef-fects of agricultural management season and soil type onphospholipids fatty acid profiles Microbial Ecology 36 1-12
BOUWMAN LA BLOEM J VAN DEN BOOGERT PHJFBREMER F HOENDERBOOM GHJ amp DE RUITER PC(1994) Short-term and long-term effects of bacterivorousnematodes and nematophagous fungi on carbon and nitrogenmineralization in microcosms Biology and Fertility of Soils17 249-256
BULLUCK III LR BARKER KR amp RISTAINO JB (2002)Influences of organic and synthetic soil fertility amendmentson nematode trophic groups and community dynamics undertomatoes Applied Soil Ecology 21 233-250
CADET P PATEacute E amp NrsquoDIAYE-FAYE N (2003) Nematodecommunity changes and survival rates under natural fallow inthe sudano sahelian area of Senegal Pedobiologia 47 149-160
CHAN KY (2001) An overview of some tillage impacts onearthworm population abundance and diversity ndash implicationsfor functioning in soils Soil and Tillage Research 57 179-191
DE MESEL I DERYCKE S MOENS T VAN DER GUCHTK VINCX M amp SWINGS J (2004) Top-down impactof bacteriovorous nematodes on the bacterial communitystructure a microcosm study Environmental Microbiology 6733-744
EKSCHMITT E STIERHOF T DAUBER J KREIMES Kamp WOLTERS V (2003) On the quality of soil biodiversityindicators abiotic parameters as predictor of soil faunalrichness at different spatial scales Agriculture Ecosystemsand Environment 98 273-283
ETTEMA CH (1998) Soil nematode diversity species coex-istence and ecosystem function Journal of Nematology 30159-169
FERRIS H VENETTE RC amp LAU SS (1997) Populationenergetics of bacterial-feeding nematodes Carbon and nitro-gen budgets Soil Biology and Biochemistry 29 1183-1194
FERRIS H BONGERS T amp DE GOEDE RGM (2001) Aframework for soil food web diagnostics extension of the
nematode faunal analysis concept Applied Soil Ecology 1813-29
FERRIS H VENETTE RC amp SCOW KM (2004) Soil man-agement to enhance bacteriovore and fungivore nematodepopulations and their nitrogen mineralization function Ap-plied Soil Ecology 25 19-35
FISCUS DA amp NEHER DA (2002) Distinguishing sensi-tivity of free-leaving soil nematode genera to physical andchemical disturbances Ecological Applications 12 565-575
FU S FERRIS H BROWN D amp PLANT R (2005) Doespositive feedback effect of nematodes on the biomass andactivity of their bacteria prey vary with nematode speciesand population size Soil Biology and Biochemistry 37 1979-1987
GYEDU-ABABIO TK FURTENBERG JP BAIRD D ampVANREUSEL A (1999) Nematodes as indicators of pollu-tion a case study from the Swartkops river system SouthAfrica Hydrobiologia 397 155-169
HAacuteNEL L (2003) Recovery of soil nematode populations fromcropping stress by natural secondary succession to meadowland Applied Soil Ecology 22 255-270
KLADIVCO EJ (2001) Tillage systems and soil ecology Soiland Tillage Research 61 61-76
KORTHALS GW VAN DE ENDE A VAN MEGEN HLEXMOND THM KAMMENGA JE amp BONGERS T(1996) Short-term effects of cadmium copper nickel andzinc on soil nematodes from different feeding and life-historystrategy groups Applied Soil Ecology 4 107-117
LENZ R amp EISENBEIS G (2000) Short-term effects ofdifferent tillage in a sustainable farming system on nematodecommunity structure Biology and Fertility of Soils 31 237-244
LIPHADZI KB AL-KHATIB K BENSCH C STAHLMANPW DILLE JA TODD T RICE CW HORAK MJamp HEAD G (2005) Soil microbial and nematode commu-nities as affected by glyphosate and tillage practices in aglyphosate-resistant cropping system Weed Science 53 536-545
MIKOLA J amp SETAumlLAuml H (1998a) No evidence of trophiccascades in an experimental microbial-based soil food webEcology 79 153-164
MIKOLA J amp SETAumlLAuml H (1998b) Relating species diversityto ecosystem functioning mechanistic backgrounds and ex-perimental approach with a decomposer food web Oikos 83180-194
MINOSHIMA H JACKSON LE CAVAGNARO TRSAacuteNCHEZ-MORENO S FERRIS H TEMPLE S ampMITCHELL J (2006) Soil food webs and carbon dynam-ics in response to conservation tillage in legume rotations inCalifornia Soil Science Society of America in press
MULDER C DE ZWART D VAN WIJNEN HJSCHOUTEN AJ amp BREURE AM (2003) Observa-tional and simulated evidence of ecological shifts withinthe soil nematode community of agroecosystems under
714 Nematology
Effects of soil management on soil food webs
conventional and organic farming Functional Ecology 17516-525
MULDER C SCHOUTEN AJ HUND-RINKE K ampBREURE AM (2005) The use of nematodes in ecologi-cal soil classification and assessment concepts Ecotoxicologyand Environmental Safety 62 278-289
NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
PORAZINSKA DL DUNCAN LW MCSORLEY R ampGRAHAM JH (1999) Nematode communities as indicatorsof status and processes of a soil ecosystems influenced byagricultural management practices Applied Soil Ecology 1369-86
POSTMA-BLAAUW MB DE VRIES FT DE GOEDERGM BLOEM J FABER JH amp BRUSSAARD L(2005) Within-trophic group interactions of bacterivorousnematode species and their effects on the bacterial commu-nity and nitrogen mineralization Oecologia 142 428-439
ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
SALOMON J ALPHEI J RUF A SCHAEFER M SCHEUS SCHNEIDER K SUumlHRIG A amp MARAUN M (2006)Transitory dynamic effects in the soil invertebrate communityin a temperate deciduous forest Effects of resource qualitySoil Biology and Biochemistry 38 209-221
SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
STATSOFT INC (1996) STATISTICA for Windows (ComputerProgram Manual) Tulsa OK USA
THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
YAMADA M (2001) Methods of control injury associatedwith continuous vegetable cropping in Japan ndash Crop rotationand several cultural practices Japan Agricultural ResearchQuarterly 35 39-45
YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
YEATES GW BONGERS T DE GOEDE RGM FRECK-MAN DW amp GEORGIEVA SS (1993) Feeding-habits insoil nematode families and genera ndash an outline for soil ecolo-gists Journal of Nematology 25 315-331
Vol 8(5) 2006 715
Effects of soil management on soil food webs
arietinum) crop (planted in late autumn) In 2004 thesummer crop was cowpeas (Vigna unguiculata) In theF treatments only tomato and garbanzo were plantedand the plots were fallow in autumn 2003 and summer2004 Four treatments were established as combinationsof both cropping pattern and tillage system NTCC (no-tillage + continuous cropping) STCC (standard tillage+ continuous cropping) NTF (no-tillage + intermittentfallow) and STF (standard tillage + intermittent fallow)
SOIL SAMPLING AND NEMATODE IDENTIFICATION
Soil was sampled in December 2003 June 2004September 2004 (only two treatments) and December2004 Soil samples were taken at three depths 0-5 cm5-15 cm and 15-30 cm Nematodes were extracted froma subsample of 350 g using a combination of decantingand sieving and Baermann funnel methods All nematodesin each sample were counted at low magnification andthen 100 nematodes (200 at the last sampling date) fromeach sample were identified to genus or family at highermagnification
Nematodes were classified by trophic habit (Yeates etal 1993) and by coloniser-persister (cp) groups (Bongers1990) The cp scale classifies nematode families in fivegroups from microbial feeders with short life cycles (cp1 and 2) to predators and omnivores with long life cyclesand greater sensitivity to environmental perturbations (cpgroups 4 and 5) Soil food web indices were calculatedafter Ferris et al (2001) based on the abundance of func-tional guilds (Bongers amp Bongers 1998) The StructureIndex (SI) is based on the relative abundance of highertrophic level nematodes and indicates soil food web lengthand soil resilience The Channel Index (CI) is calculatedas the proportion of fungal-feeding nematodes comparedto enrichment-opportunistic bacterial feeders and is anindicator of activity in the predominant decompositionchannels in the soil fungal mediated (higher values) orbacterial mediated (lower values) The Basal Index (BI) isan indicator of the prevalence of the general opportunisticnematodes that are tolerant of soil perturbation Finallythe Enrichment Index (EI) is an indicator of enrichmentopportunistic nematodes both fungal and bacterial feed-ers which respond rapidly to increases in food resourcesThe resilience of nematode trophic groups to tillage wascalculated according to Wardle (1995)
SOIL PROPERTIES
Microbial organic carbon (MBC) NH+4 NOminus
3 and er-gosterol were measured at all sampling dates Phospho-lipid fatty acids (PLFA) were used as indicators of bac-terial and fungal biomass in the soil Bacterial PLFAmarkers were iso 150 anteiso 150 150 iso 160161ω5c iso 170 anteiso 170 170cy 170 and 190cyFungal PLFA markers were 182ω 6 and 9c (Bossio etal 1998 Mikola amp Setaumllauml 1998a) Bulk density wasmeasured once in samples collected in February 2005For details of measurements of soil properties see Mi-noshima et al (2006) Soil physicochemical analyses (to-tal N total C soil pH K and plant available (Olsen)P) were performed by the University of CaliforniarsquosAgriculture and Natural Resources Analytical Laboratory(httpdanranlabucanrorg)
STATISTICAL ANALYSES
The influence of treatments on the nematode assem-blage across the four sampling dates was determined byCorrespondence Canonical Analysis (CCA) and by themethodology of Fiscus and Neher (2002) Nematode iden-tification at higher resolution was used to relate nematodetaxa with soil chemistry at the last sampling date (Decem-ber 2004) All variables were transformed as ln(x + 1)
to normalise data before the analyses ANOVA was usedto check the influence of categorical variables on nema-tode abundances and soil food web indices Correlationanalysis was used to check relationships between vari-ables Analyses were performed using STATISTICA soft-ware (StatSoft 1996)
Direct effects of tillage system cropping pattern anddepth
Differences in abundances of nematode taxa and foodweb indices were tested using General Linear Models Allthe nematological variables (nematode taxa abundancesand soil food web indices) and three categorical factors(tillage system cropping pattern and soil depth) weresubjected to CCA using data from the four samplingperiods (December 2003 June 2004 September 2004December 2004 n = 126)
In CCA bi-plots environmental axes are represented byarrows The length of the arrow indicates the importanceof the environmental variable for the ordination rootsIts direction indicates the correlation of the variable withother variables arrows in the same direction are positivelycorrelated while arrows pointing in opposite directions
Vol 8(5) 2006 705
S Saacutenchez-Moreno et al
are negatively related Dependent variables (nematodetaxa and food web indices) located near an environmental(independent) variable suggest a positive effect of thelatter on the former
Indirect effects of tillage system cropping pattern anddepth
Data from the last sampling date were subjected toANOVA to test differences in the soil properties amongtreatments Nematode abundances and soil propertieswere used to perform multivariate analyses (CCA) ofthe state of the nematode assemblage at the end ofthe cropping cycle (December 2004 n = 36) In theseanalyses nematode data were expressed at the highestlevel of taxonomic resolution available
Results
DIRECT EFFECTS OF TILLAGE SYSTEM CROPPING
PATTERN AND DEPTH
Cropping pattern tillage system and depth affected thecomposition of the nematode fauna and food web indicesacross the four sampling dates Tylenchidae Rhabditi-dae Acrobeloides and Pratylenchus were more abundantin continuously cropped plots while Dorylaimidae weremore abundant in the intermittent fallow treatments (Ta-ble 1) Consequently number of nematodes was lower andthe SI was higher under intermittent fallow (Table 2)
Tillage directly affected Aphelenchus and Rhabditidaewhich were more abundant in ST plots and Tylenchidaemore abundant in the NT treatments Depth affected Aphe-lenchus Tylenchidae Panagrolaimus and Dorylaimidaewhich were more abundant in the upper soil layers (0-15 cm) The CI was higher in NT plots Both BI and CIwere lower in the upper soil where EI was higher (Ta-ble 2)
Following Wardlersquos methodology to infer the resilienceof soil organisms to tillage (Wardle 1995) nematodes as awhole were mildly stimulated by tillage (V index = 014)In fact the response of nematodes varied depending ontheir trophic group bacterial-feeders and fungal-feederswere mildly stimulated by tillage (V = 029 and 003respectively) and herbivores and predators and omnivoreswere mildly inhibited by tillage (V = minus006 and minus0004respectively) By the same logic bacterial fungal andplant feeders were inhibited and predators and omnivoresstimulated by intermittent fallow (Fig 1)
Direct effects of cropping intensity tillage system anddepth on the nematode faunal data across the four sam-
Fig 1 V index values for nematode trophic groups (Ba =bacterial-feeders Fu = fungal-feeders Pp = plant parasitesPO = predators and omnivores) sensitivity to tillage (T) andfallow (F) Positive values indicate stimulation negative valuesindicate inhibition (after Wardle 1995)
pling dates were analysed and expressed in a CCA bi-plotTylenchidae were associated with CC and negatively af-fected by the F treatments while Aphelenchus Acrobeloi-des Rhabditidae and Panagrolaimus were positively asso-ciated with ST and negatively affected by soil depth theywere most abundant in the upper soil layers
For the four sampling dates the CI and the SI werehigher in the 15-30 cm depth and were associated withNT and F The EI was associated positively with uppersoil and the BI with medium depths and F (Fig 2)
Following Fiscus and Neher (2002) the analysis ofthe direct effects of tillage cropping pattern and depthon the nematode assemblage along the four samplingdates allowed classification of nematode taxa and foodweb descriptors as functions of their associations witheach variable Nematodes were classified as tolerant totillage if positioned in the bi-plot area defined by STand sensitive if positioned in the opposite half indicatingassociation with NT The same logic was used to scoreeach nematode taxon as sensitive or resistant to fallow andto infer associations with different soil depths (Table 3)
INDIRECT EFFECT OF TILLAGE AND COVER CROPS
Relationship between environmental variables andmanagement
On the last sampling date (December 2004) soil pHNOminus
3 and bulk density varied among the treatments pHand bulk density were higher in the NT treatments NOminus
3was significantly higher in STCC Total C total N pHergosterol and bulk density were all significantly affectedby tillage system and were higher in NT (Table 4)
Soil properties were in general strongly correlatedSoil pH and C N P and K concentrations were positively
706 Nematology
Effects of soil management on soil food websTa
ble
1E
ffect
sof
crop
ping
patt
ern
till
age
syst
eman
dso
ilde
pth
onab
unda
nce
ofne
mat
ode
taxa
(num
ber
ofne
mat
odes
100
gso
il)
Fva
lues
and
leve
lofs
igni
fican
cear
ein
dica
ted
(ns=
nots
igni
fican
t)D
ata
are
from
the
four
sam
plin
gda
tes
(n=
126)
Cro
ppin
gT
illag
eD
epth
Uni
vari
ate
effe
cts
F=
529
P
lt0
0001
F=
575
P
lt0
0001
F=
198
P
lt0
01
Con
tinuo
usFa
llow
No-
till
Stan
dard
0-5
cm5-
15cm
15-3
0cm
Cro
ppin
gT
illag
eD
epth
crop
ping
Aph
elen
chus
127
84plusmn
104
911
688
plusmn12
11
100
07plusmn
921
144
65plusmn
133
312
651
plusmn15
47
167
63plusmn
154
175
29
plusmn6
72ns
Plt
001
Plt
005
Tyle
nchi
dae
233
71plusmn
153
913
210
plusmn17
77
209
73plusmn
188
515
608
plusmn16
60
180
23plusmn
211
823
802
plusmn26
52
152
25plusmn
163
9P
lt0
001
Plt
005
Plt
001
Acr
obel
oide
s13
355
plusmn16
22
739
5plusmn
187
363
29
plusmn11
54
144
20plusmn
234
711
288
plusmn17
60
131
10plusmn
268
880
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108
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28plusmn
398
411
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403
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plusmn67
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728
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001
Rha
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135
08plusmn
203
057
76
plusmn23
44
499
3plusmn
124
314
291
plusmn32
24
126
05plusmn
269
412
482
plusmn39
03
549
5plusmn
160
0P
lt0
05P
lt0
01Ty
lenc
horh
ynch
us19
29
plusmn4
9828
47
plusmn5
7526
15
plusmn4
1721
61
plusmn6
5316
89
plusmn6
5834
46
plusmn8
4718
32
plusmn2
93ns
nsns
Dor
ylai
mid
ae27
57
plusmn5
7648
78
plusmn6
6537
40
plusmn6
5838
94
plusmn5
6448
10
plusmn11
67
374
9plusmn
470
243
8plusmn
299
Plt
005
nsP
lt0
05Sm
all
197
plusmn0
671
08plusmn
078
251
plusmn0
900
54plusmn
024
164
plusmn0
962
59plusmn
110
054
plusmn0
30ns
nsns
Dor
ylai
mid
aeP
lect
us8
13plusmn
175
440
plusmn2
027
41plusmn
226
512
plusmn1
1010
24
plusmn3
334
93plusmn
155
443
plusmn1
30P
raty
lenc
hus
305
0plusmn
585
124
8plusmn
675
157
6plusmn
348
272
2plusmn
883
436
plusmn1
2421
58
plusmn5
6642
38
plusmn11
62
Plt
005
nsP
lt0
05Ty
lenc
hola
imus
101
plusmn0
430
36plusmn
050
070
plusmn0
260
66plusmn
064
042
plusmn0
250
93plusmn
087
084
plusmn0
38ns
nsns
Tabl
e2
Effe
cts
ofcr
oppi
ngpa
tter
nti
llag
esy
stem
and
soil
dept
hon
soil
food
web
indi
ces
(EI=
Enr
ichm
ent
inde
xSI
=St
ruct
ure
inde
xB
I=
Bas
alin
dex
CI=
Cha
nnel
inde
x)t
otal
num
ber
ofne
mat
odes
(N)
and
taxa
rich
ness
(S)
Fva
lues
and
leve
lof
sign
ifica
nce
are
indi
cate
d(n
s=
not
sign
ifica
nt)
Dat
aar
efr
omth
efo
ursa
mpl
ing
date
s(n
=12
6)
Cro
ppin
gT
illag
eD
epth
Uni
vari
ate
F=
452
P
lt0
0001
F=
269
P
lt0
05F
=5
34
Plt
000
01
Con
tinuo
usFa
llow
No-
tilla
geSt
anda
rd0-
5cm
5-15
cm15
-30
cmC
ropp
ing
Till
age
Dep
thcr
oppi
ng
N85
972
plusmn64
35
599
53plusmn
800
362
631
plusmn66
25
832
94plusmn
878
194
076
plusmn10
665
821
56plusmn
960
448
232
plusmn61
25
Plt
005
nsP
lt0
01S
761
plusmn0
157
85plusmn
012
781
plusmn0
127
65plusmn
015
745
plusmn0
157
74plusmn
017
795
plusmn0
17ns
nsP
lt0
05E
I65
66
plusmn2
0166
64
plusmn1
7264
77
plusmn1
5267
53
plusmn2
2073
58
plusmn1
7960
63
plusmn2
2064
03
plusmn2
30ns
nsP
lt0
01SI
262
9plusmn
315
436
2plusmn
209
343
3plusmn
259
355
7plusmn
300
291
1plusmn
364
297
7plusmn
283
422
7plusmn
332
Plt
000
1ns
Plt
001
BI
297
6plusmn
172
264
1plusmn
149
291
4plusmn
137
270
2plusmn
186
229
0plusmn
161
335
0plusmn
202
285
6plusmn
191
nsns
Plt
005
CI
408
5plusmn
371
432
6plusmn
320
471
7plusmn
328
369
3plusmn
348
239
3plusmn
233
533
4plusmn
417
483
7plusmn
428
nsP
lt0
001
Plt
001
Vol 8(5) 2006 707
S Saacutenchez-Moreno et al
Table 3 Direct effects of tillage (ST = standard tillage NT = no-till) cropping pattern (F = fallow CC = continuous cropping)and soil depth (0-5 5-15 and 15-30 cm) on abundance ofnematode taxa and on soil food web indices (S = taxa richnessN = total number of nematodes EI = Enrichment index SI =Structure index BI = Basal index CI = Channel index) Trophicgroup (Ba = bacterial feeders Fu = fungal feeders Pp = plantparasites P = predators O = omnivores) of nematode taxa areindicated
Trophic Cp Tillage Cropping Depthgroup pattern (cm)
Aphelenchus Fu 2 ST CC 0-5Tylenchidae PpFu 2 NT CC 5-15Acrobeloides Ba 2 ST CC 0-5Panagrolaimus Ba 1 ST CC 0-5Rhabditidae Ba 1 ST CC 0-5Tylenchorhynchus Pp 3 NT F 5-15Dorylaimidae O 4 ST F 5-15Small Dorylaimidae O 4 NT CC 5-15Plectus Ba 2 NT CC 5-15Pratylenchus Pp 3 NT CC 5-15Tylencholaimus Fu 4 NT CC 5-15N ST CC 0-5S NT F 5-15EI ST CC 0-5SI ST F 15-30BI NT CC 5-15CI NT F 15-30
related (r between 049 and 083 P lt 005) NH+4
was associated with intermittent fallow and correlatedwith ergosterol and MBC (r between 049 and 052P lt 005) PLFA of fungal markers were correlated withergosterol (r = 035 P lt 005) and with PLFA ofbacterial markers (r = 095 P lt 005)
Influence of environmental variables on nematode taxaand soil food web descriptors
In December 2004 at the end of the experiment inthe ordination of the nematode taxa in the multivariatespace defined by the environmental variables positivevalues for most of the soil properties grouped togetherindicating soil enrichment and high biological activity(Fig 3a b) The PLFA biomarkers of both bacteria andfungi were related with the abundance of AcrobeloidesMesorhabditis and Tylenchorhynchus Panagrolaimus andAcrobeles both bacterial feeders were not correlated witheither group of PLFAs and ordered in the opposite part ofthe graph Tylenchidae was associated with pH (r = 047P lt 005) Aphelenchoides was associated with NOminus
3
The abundance of all the omnivores and predators(Discolaimus Aporcelaimidae Qudsianematidae and My-lonchulus) except Prionchulus were inversely correlatedwith almost all soil properties The EI was negativelycorrelated with the CI (r = minus093 P lt 005) BI(r = minus095 P lt 005) taxa richness (r = minus056P lt 005) bulk density (r = minus040 P lt 005) andPLFA of bacterial markers (r = minus035 P lt 005) It waspositioned in the opposite part of the graph than BI andCI (Fig 3) CI was positively correlated with bulk densityand PLFA of fungal markers (r = 037 and 034 respec-tively P lt 005) SI was negatively correlated with NOminus
3 pH and K (r = minus037 minus033 and minus034 P lt 005)Taxa richness and number of nematodes were negativelycorrelated (r = minus036 P lt 005) Number of nematodeswas associated with total C and taxa richness with bulkdensity CI and BI were positively correlated (r = 086P lt 005)
Discussion
The aim of this study was to evaluate the relationshipsbetween nematode faunal composition and soil propertiesas determined by agricultural management It is generallyaccepted that nematodes are strongly influenced by theirmicroenvironment and provide a useful reflection ofsoil health status and several soil functions (Mulder etal 2005) The use of multivariate statistics especiallyCanonical Analysis has improved the understanding ofthe complex relationships between different groups of soilfauna and between organisms and soil physical-chemicalproperties (Popovici amp Ciobanu 2000 Wardle et al2001 Fiscus amp Neher 2002)
As expected from previous studies (eg Wardle 1995)total nematode abundance was not strongly influenced bytillage due to the varied responses of different taxa Ne-matode responses to tillage and cropping intensity var-ied with their trophic group bacterial feeders and fun-gal feeders were stimulated by tillage and reduced un-der intermittent fallow plant-feeders were generally in-hibited by both tillage and intermittent fallow and preda-tors and omnivores were stimulated by intermittent fallowand did not respond clearly to tillage practices In factthe few omnivores and predators in this and most agri-cultural fields probably represent the more tolerant taxawithin these trophic levels Taxa intolerant to disturbancemay no longer be present in arable soils These observa-tions agree with Lenz and Eisenbeis (2000) who found nochanges in total nematode abundance and an increase of
708 Nematology
Effects of soil management on soil food webs
Table 4 Average values (plusmn SE) of soil properties in the four different treatments across three depths Significant effects of treatments(NTCC STCC STF NTF) crop pattern (CC and F) and tillage (ST and NT) are indicated by level of significance Data are from thelast sampling date (December 2004 n = 36) Data from Minoshima et al (2006)
NTF STF NTCC STCC Treatment Crop Tillage
Total C () 106 plusmn 003 099 plusmn 001 107 plusmn 004 103 plusmn 002 P lt 005Total N () 012 plusmn 000 011 plusmn 000 012 plusmn 000 012 plusmn 000 P lt 005pH 707 plusmn 003 686 plusmn 003 708 plusmn 006 690 plusmn 004 P lt 001 P lt 0001K (mg lminus1) 700 plusmn 049 591 plusmn 013 786 plusmn 132 734 plusmn 080P (microg gminus1) 1738 plusmn 088 1578 plusmn 031 1908 plusmn 217 1598 plusmn 083NO3 454 plusmn 106 550 plusmn 148 646 plusmn 092 1203 plusmn 253 P lt 005 P lt 005
(microg N gminus1)
NH4 236 plusmn 131 127 plusmn 054 116 plusmn 027 106 plusmn 016(microg N gminus1)
MBC 17123 plusmn 2623 14816 plusmn 1905 26275 plusmn 6398 17158 plusmn 1823(microg C gminus1)
Ergosterol 99932 plusmn 16846 57594 plusmn 3631 224691 plusmn 82975 121820 plusmn 25685 P lt 005(ng gminus1)
Bulk density 134 plusmn 002 125 plusmn 003 132 plusmn 002 125 plusmn 002 P lt 005 P lt 001(gcm3)
PLFAba 190753 plusmn 50529 144540 plusmn 35185 230127 plusmn 55833 208676 plusmn 31240(mgm2)
PLFAfu 24662 plusmn 12047 14295 plusmn 4381 55785 plusmn 26261 27208 plusmn 7651(mgm2)
bacterial-feeder nematodes after the first tillage treatmentOur results indicate that the response of total nematodeabundance to management depends on the assemblagecomposition so no general patterns can be discerned with-out analysing separately the taxa and functional group re-sponses For example Liphadzi et al (2005) found gen-eral increase in nematode abundance in tilled plots due tothe predominance of fungal feeders and bacterial feeders(up to 90) in the assemblages they studied
Throughout the four sampling dates of this study mostof the microbial feeders (Panagrolaimus RhabditidaeAphelenchus and Acrobeloides) were positively associ-ated with standard tillage indicating the stimulatory effecton microbes of incorporating organic matter into the soilThe nematodes less responsive to incorporated organicmatter were the higher cp taxa (Tylenchorhynchus Tylen-cholaimus Pratylenchus and some Dorylaimidae) whichwere associated with no-tillage Even though a greaternumber of taxa (especially of upper trophic levels) andhigher resolution identification would be desirable to in-fer relationships more reliably (Yeates 2003 Mulder etal 2005) we observed significant relationships betweensensitivity to tillage and trophic or cp groups as similarlyreported by Fiscus and Neher (2002)
Plectus was the only bacterivore associated with thesoil properties of the NT treatments suggesting a highersensitivity to tillage practices While Fiscus and Neher(2002) suggested that Plectus is an indicator of distur-bance due to the concordance between its cp value (2)and its tolerance to chemical and mechanical perturba-tions we found it to be more sensitive to tillage than ex-pected from its cp value Different responses among ge-nera in the same trophic group are common (Porazinska etal 1999) and nematode genera within the same trophicgroup can exhibit asymmetric competition negatively in-fluencing the abundance of other genera (Postma-Blaaw etal 2005) so responses to perturbation may be influencedby the presence of other nematode taxa Greater taxo-nomic resolution may be necessary to resolve differencesin response to environmental variables among nematodeswithin higher taxonomic groupings (Yeates 2003) espe-cially for taxa that have numerous species and a broad sizerange (eg Plectus)
Bacterial feeders are usually abundant in cultivatedsoils while predators and omnivores often disappear withcultivation (Wardle et al 1995) Microbivorous nema-todes belonging to the cp 1 group (eg Panagrolaimusor Rhabditidae enrichment-opportunistic nematodes) andthose with longer life cycles in the cp 2 group (eg Aphe-
Vol 8(5) 2006 709
S Saacutenchez-Moreno et al
Fig 2 Canonical correspondence analysis bi-plot of effects of tillage system crop pattern and depth on nematode abundances andsoil food web indices Environmental variables are marked by arrows Aphel Aphelenchus Tyl Tylenchidae Acro Acrobeloides PanPanagrolaimus Rhab Rhabditidae Tylen Tylenchorhynchus Dor Dorylaimidae SDor Small Dorylaimidae Plec Plectus PratPratylenchus Tylo Tylencholaimus N Total number of nematodes S Taxa richness EI Enrichment index SI Structure index BIBasal index CI Channel index Eigenvalues were 0568 and 0362 for the first and the second root respectively Percentage of varianceexplained was 330 for both root 1 and root 2
lenchus and Acrobeloides) were also associated with con-tinuous cropping The combined effect of standard tillageand continuous cropping significantly enhanced the abun-dance of nematodes at the entry level of the soil foodweb Bacterial-feeding nematodes influence C- and N-
mineralisation by feeding on bacteria excreting NH+4 and
by spreading bacteria through the soil (Bouwman et al1994 Fu et al 2005) Mesorhabditis and Acrobeloidestwo of the most abundant bacterial-feeders in our plotswere positively associated with NH+
4 a reasonable expec-
Fig 3 Scatter plot of CCA ordination showing relationships between soil properties and nematode taxa abundance (a) and soil foodweb indices taxa richness and total number of nematodes (b) Acro Acrobeles Acrob Acrobeloides Aphel Aphelenchus AphoAphelenchoides Aporce Aporcelaimidae Diph Diphtherophora Disco Discolaimus Dity Ditylenchus Meso Mesorhabditis MylMylonchulus Pan Panagrolaimus Plec Plectus Prat Pratylenchus Prion Prionchulus Qudsi Qusianematidae Tyl TylenchidaeTylen Tylenchorhynchus Eigenvalues were 097 and 096 (a) and 080 and 058 (b) for roots 1 and 2 respectively Percentages ofexplained variance for roots 1 and 2 were 107 and 110 (a) and 114 and 64 (b) respectively
710 Nematology
Effects of soil management on soil food webs
Vol 8(5) 2006 711
S Saacutenchez-Moreno et al
tation for the group associated with increased N mineral-isation (Ferris et al 1997 2004) By contrast Panagro-laimus and Plectus ordered in an opposite position due totheir negative relationship with PLFA biomarkers of fungiand bacteria and with bulk density Panagrolaimus has ahigh metabolic rate and a broad non-selective microbialfeeding habit (De Mesel et al 2004) It may decreasebacterial populations (as indicated by lower PFLA frombacterial markers) to a greater extent than other bacter-ial feeders in our plots When microbivorous nematodespredominate in soils they enhance N mineralisation andthus the availability of N for plants (Ferris et al 2004)Total soil N may be correlated with abundance of certainnematodes (Nakamoto et al 2006) but potentially min-eralisable N is a better indicator of N availability Thatmight explain why total soil N was associated only withabundance of Tylenchidae in this study Total C on thecontrary was more strongly associated with total nema-tode abundance
Surprisingly the abundance of fungal-feeding nema-todes such as Aphelenchus and some Tylenchidae was notrelated as strongly with ergosterol as expected suggest-ing that fungal biomass may not determining the size offungal feeder populations Villenave et al (2004) founddiffering responses of fungal feeders to ergosterol contentfungal feeders in cp groups 2 and 4 were positively relatedwith ergosterol but fungal feeders in the cp 5 group werenot
The discrimination between responses of nematodesin the higher and the lower levels of the soil food webwas evident in the CCA ordination revealing a link be-tween lower trophic levels and MBC NH+
4 ergosteroltotal N total C and certain PLFA Bacterial- fungal-and plant-feeding taxa with low cp values ordered op-posite to predatory and omnivore nematodes such asPrionchulus Qudsianematidae Aporcelaimidae Disco-laimus and Mylonchulus With the only exceptions ofthe plant-feeder Tylenchorhynchus (cp 3) which orderedclose to Mesorhabditis (cp 1) and Acrobeles (cp 2) whichscored close to the predators (cp 4 5) nematodes belong-ing to cp groups 1 and 2 showed an opposite response toenvironmental variables than those in cp groups 3 4 and 5
Predatory and omnivore nematodes are in higher co-loniser-persistent groups (3) and are more sensitive tosoil perturbation Intermittent fallow and standard tillagesupported higher abundances of most of the predators andomnivores Mylonchulus Qudsianematidae Prionchulusand Aporcelaimidae It is generally accepted that nema-tode functional diversity decreases with increasing man-
Table 5 Summarized effects of treatments on nematode trophicgroups (Ba = bacterial-feeders Fu = fungal-feeders Pp =plant-feeders PO = predators and omnivores)
Standard tillage No-tillage
Fallow Small increase of Ba Decrease of BaSmall decrease of Fu Decrease of FuDecrease of Pp Small decrease of PpIncrease of PO Increase of POIncrease of SI values Increase of CI values
Continuous Increase of Ba Small decrease of Bacropping Small increase of Fu Increase of Fu
Increase of Pp Increase of PpDecrease of PO Decrease of POIncrease of EI values Increase of BI values
agement intensity (Mulder et al 2003) predatory nema-todes were in our case much more affected by the crop-ping pattern (being enhanced in the intermittent fallowtreatment) than by standard tillage Our results thus sug-gest that even though predatory nematodes are sensitive tosoil physical perturbation other soil forces can drive theirabundance In some studies 25 years of tillage did notstrongly affect predators but reduced fungal-feeder nema-todes (Wang et al 2004)
An increase in predator and omnivore nematodes wasexpected in CC treatments as a result of the continuousincorporation of C into the soil but was not found (Ta-ble 5) Minoshima et al (2006) found that nematodesin the higher trophic levels were not significantly asso-ciated with the C pools in the soil Previous studies foundomnivore and predatory nematodes much more abundantin recently abandoned fallow fields than in cultivated orseminatural meadow lands (Haacutenel 2003) Polis et al(2000) suggest that trophic cascades produced by com-plex trophic interactions are abundant in soil systemsbut bottom-up regulation is difficult to demonstrate insoil trophic levels due to the high complexity of the soilbiota interactions In forest soils Salomon et al (2006)found more abundant microbial grazers when abundantresources were added to the soil but the effects did notextend into higher trophic levels of the soil food webleading to the conclusion that the availability of resourcesplays a minor role structuring soil food webs
Responses of plant-parasites and root feeders to tillageare usually difficult to interpret and are more closely re-lated to plant status and phenology than to soil propertiesThe association between Pratylenchus (endoparasite) andstandard tillage might be explained by the release of the
712 Nematology
Effects of soil management on soil food webs
nematodes from the roots as a result of tillage (Lenz ampEisenbeis 2000)
Ammonium MBC C K P and ergosterol were pos-itively related with total number of nematodes and theEI The EI is based on the weighted abundance of bacte-rial feeding nematodes enrichment-opportunistic relativeto longer life cycle bacterial-feeders indicating highlyactive bacterial-mediated decomposition channels Whenthe field is organically enriched these nematodes exploitthe abundant resources (fungi and bacteria) and increaserapidly in abundance due to their short life cycles and highfecundity (Bongers 1990) On the contrary high valuesof the CI indicate slower fungal-mediated decompositionpathways so a significant relationship between CI and er-gosterol was expected but not found CI was positivelycorrelated with PLFA of fungal biomarkers and EI wasnegatively correlated with PLFA of bacterial markers butnot correlated with MBC Thus the relationship betweenPLFA and microbial grazers may reflect the strength of thegrazing pressure at the sampling time The prevalence ofopportunistic bacterial feeders over other microbial feed-ers (as expressed by the EI) may decrease bacterial bio-mass (indicated by PLFA of bacterial markers) more obvi-ously than the effect of fungal feeders on fungal biomassas indicated by the positive association between the CIindicator of the prevalence of fungal-feeding nematodesover bacterial feeders with fungal biomass (inferred fromPLFA of fungal markers) The absence of correlation be-tween MBC and nematode populations may thus indicatethat the grazing pressure affects only certain microbes andnot the total microbial community
CI and BI were strongly correlated and associatedwith deeper soil layers and no tillage across all samplingdates High BI values indicate a nematode assemblagecomposed of perturbation-resistant nematodes mainly oflower trophic levels The community structure was in thiscase associated with fungal-dominated organic matterdecomposition pathways The SI was associated withdeeper soil layers and intermittent fallow suggesting anegative relationship between predator abundance and thehigh physical disturbance and biological activity presentat the soil surface and in the continuous cropping plots
Conclusions
Different tillage practices and cropping systems deter-mine soil properties and thus nematode abundance Theseeffects vary with nematode trophic and functional group
By the end of the experiment each treatment supporteddifferent nematode assemblages and soil food webs
Each soil food web index describes a model nema-tode assemblage (Ferris et al 2001) Our four treat-ments structured four different nematode assemblagesThe combination of standard tillage and continuous crop-ping (STCC) was associated with high EI values reflect-ing an assemblage predominantly composed of bacterial-feeding nematodes with short life cycles This enrichedassemblage was especially characteristic of the upper soillayer Perhaps not surprisingly for a long-disturbed agri-cultural system we did not find the relationships we ex-pected between continuous cropping and the abundanceof predator and omnivore nematodes The organisms inthe higher levels of the soil food web did not respond tothe continuous input of C in the soil and a long recoveryperiod may be required for appropriate taxa to be rein-troduced and to increase Intermittent fallow (especiallySTF) supported a longer more structured soil food web(high SI values) especially in the deeper soil layers Thecombination of no tillage and intermittent fallow (NTF)supported a fungal-based community with slower organicmatter decomposition rates especially below the upper 5cm of soil The accumulation of plant residues on the soilsurface may result in slower incorporation of C into thefood web and exploitation by fungi Indeed the absenceof tillage and thus of physical perturbation would not dis-rupt fungal hyphae Finally the combination of no tillageand continuous cropping (NTCC) supported a less well-defined assemblage dominated by basal perturbation-resistant nematodes
Acknowledgements
This research was supported by California Bay DeltaAuthority (CBDA)-Ecosystem Restoration Program grant ERP-02-P36 by the California Department of Food andAgricultureKearney Foundation of Soil Science Projects2003011 and by the Kearney Foundation of Soil ScienceProject 2005210 We thank the LTRAS staff for fieldmanagement Many thanks to members of the Jackson andTemple lab groups for help with sampling and Dr S Goyalfor guidance with the HPLC
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BERKELMANS R FERRIS H TENUTA M amp VAN
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Effects of soil management on soil food webs
conventional and organic farming Functional Ecology 17516-525
MULDER C SCHOUTEN AJ HUND-RINKE K ampBREURE AM (2005) The use of nematodes in ecologi-cal soil classification and assessment concepts Ecotoxicologyand Environmental Safety 62 278-289
NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
PORAZINSKA DL DUNCAN LW MCSORLEY R ampGRAHAM JH (1999) Nematode communities as indicatorsof status and processes of a soil ecosystems influenced byagricultural management practices Applied Soil Ecology 1369-86
POSTMA-BLAAUW MB DE VRIES FT DE GOEDERGM BLOEM J FABER JH amp BRUSSAARD L(2005) Within-trophic group interactions of bacterivorousnematode species and their effects on the bacterial commu-nity and nitrogen mineralization Oecologia 142 428-439
ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
SALOMON J ALPHEI J RUF A SCHAEFER M SCHEUS SCHNEIDER K SUumlHRIG A amp MARAUN M (2006)Transitory dynamic effects in the soil invertebrate communityin a temperate deciduous forest Effects of resource qualitySoil Biology and Biochemistry 38 209-221
SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
STATSOFT INC (1996) STATISTICA for Windows (ComputerProgram Manual) Tulsa OK USA
THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
YAMADA M (2001) Methods of control injury associatedwith continuous vegetable cropping in Japan ndash Crop rotationand several cultural practices Japan Agricultural ResearchQuarterly 35 39-45
YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
YEATES GW BONGERS T DE GOEDE RGM FRECK-MAN DW amp GEORGIEVA SS (1993) Feeding-habits insoil nematode families and genera ndash an outline for soil ecolo-gists Journal of Nematology 25 315-331
Vol 8(5) 2006 715
S Saacutenchez-Moreno et al
are negatively related Dependent variables (nematodetaxa and food web indices) located near an environmental(independent) variable suggest a positive effect of thelatter on the former
Indirect effects of tillage system cropping pattern anddepth
Data from the last sampling date were subjected toANOVA to test differences in the soil properties amongtreatments Nematode abundances and soil propertieswere used to perform multivariate analyses (CCA) ofthe state of the nematode assemblage at the end ofthe cropping cycle (December 2004 n = 36) In theseanalyses nematode data were expressed at the highestlevel of taxonomic resolution available
Results
DIRECT EFFECTS OF TILLAGE SYSTEM CROPPING
PATTERN AND DEPTH
Cropping pattern tillage system and depth affected thecomposition of the nematode fauna and food web indicesacross the four sampling dates Tylenchidae Rhabditi-dae Acrobeloides and Pratylenchus were more abundantin continuously cropped plots while Dorylaimidae weremore abundant in the intermittent fallow treatments (Ta-ble 1) Consequently number of nematodes was lower andthe SI was higher under intermittent fallow (Table 2)
Tillage directly affected Aphelenchus and Rhabditidaewhich were more abundant in ST plots and Tylenchidaemore abundant in the NT treatments Depth affected Aphe-lenchus Tylenchidae Panagrolaimus and Dorylaimidaewhich were more abundant in the upper soil layers (0-15 cm) The CI was higher in NT plots Both BI and CIwere lower in the upper soil where EI was higher (Ta-ble 2)
Following Wardlersquos methodology to infer the resilienceof soil organisms to tillage (Wardle 1995) nematodes as awhole were mildly stimulated by tillage (V index = 014)In fact the response of nematodes varied depending ontheir trophic group bacterial-feeders and fungal-feederswere mildly stimulated by tillage (V = 029 and 003respectively) and herbivores and predators and omnivoreswere mildly inhibited by tillage (V = minus006 and minus0004respectively) By the same logic bacterial fungal andplant feeders were inhibited and predators and omnivoresstimulated by intermittent fallow (Fig 1)
Direct effects of cropping intensity tillage system anddepth on the nematode faunal data across the four sam-
Fig 1 V index values for nematode trophic groups (Ba =bacterial-feeders Fu = fungal-feeders Pp = plant parasitesPO = predators and omnivores) sensitivity to tillage (T) andfallow (F) Positive values indicate stimulation negative valuesindicate inhibition (after Wardle 1995)
pling dates were analysed and expressed in a CCA bi-plotTylenchidae were associated with CC and negatively af-fected by the F treatments while Aphelenchus Acrobeloi-des Rhabditidae and Panagrolaimus were positively asso-ciated with ST and negatively affected by soil depth theywere most abundant in the upper soil layers
For the four sampling dates the CI and the SI werehigher in the 15-30 cm depth and were associated withNT and F The EI was associated positively with uppersoil and the BI with medium depths and F (Fig 2)
Following Fiscus and Neher (2002) the analysis ofthe direct effects of tillage cropping pattern and depthon the nematode assemblage along the four samplingdates allowed classification of nematode taxa and foodweb descriptors as functions of their associations witheach variable Nematodes were classified as tolerant totillage if positioned in the bi-plot area defined by STand sensitive if positioned in the opposite half indicatingassociation with NT The same logic was used to scoreeach nematode taxon as sensitive or resistant to fallow andto infer associations with different soil depths (Table 3)
INDIRECT EFFECT OF TILLAGE AND COVER CROPS
Relationship between environmental variables andmanagement
On the last sampling date (December 2004) soil pHNOminus
3 and bulk density varied among the treatments pHand bulk density were higher in the NT treatments NOminus
3was significantly higher in STCC Total C total N pHergosterol and bulk density were all significantly affectedby tillage system and were higher in NT (Table 4)
Soil properties were in general strongly correlatedSoil pH and C N P and K concentrations were positively
706 Nematology
Effects of soil management on soil food websTa
ble
1E
ffect
sof
crop
ping
patt
ern
till
age
syst
eman
dso
ilde
pth
onab
unda
nce
ofne
mat
ode
taxa
(num
ber
ofne
mat
odes
100
gso
il)
Fva
lues
and
leve
lofs
igni
fican
cear
ein
dica
ted
(ns=
nots
igni
fican
t)D
ata
are
from
the
four
sam
plin
gda
tes
(n=
126)
Cro
ppin
gT
illag
eD
epth
Uni
vari
ate
effe
cts
F=
529
P
lt0
0001
F=
575
P
lt0
0001
F=
198
P
lt0
01
Con
tinuo
usFa
llow
No-
till
Stan
dard
0-5
cm5-
15cm
15-3
0cm
Cro
ppin
gT
illag
eD
epth
crop
ping
Aph
elen
chus
127
84plusmn
104
911
688
plusmn12
11
100
07plusmn
921
144
65plusmn
133
312
651
plusmn15
47
167
63plusmn
154
175
29
plusmn6
72ns
Plt
001
Plt
005
Tyle
nchi
dae
233
71plusmn
153
913
210
plusmn17
77
209
73plusmn
188
515
608
plusmn16
60
180
23plusmn
211
823
802
plusmn26
52
152
25plusmn
163
9P
lt0
001
Plt
005
Plt
001
Acr
obel
oide
s13
355
plusmn16
22
739
5plusmn
187
363
29
plusmn11
54
144
20plusmn
234
711
288
plusmn17
60
131
10plusmn
268
880
03
plusmn21
74
Plt
005
nsns
Pana
grol
aim
us14
108
plusmn34
50
123
28plusmn
398
411
335
plusmn33
48
151
01plusmn
403
231
343
plusmn67
07
580
0plusmn
182
728
92
plusmn7
55ns
nsP
lt0
001
Rha
bditi
dae
135
08plusmn
203
057
76
plusmn23
44
499
3plusmn
124
314
291
plusmn32
24
126
05plusmn
269
412
482
plusmn39
03
549
5plusmn
160
0P
lt0
05P
lt0
01Ty
lenc
horh
ynch
us19
29
plusmn4
9828
47
plusmn5
7526
15
plusmn4
1721
61
plusmn6
5316
89
plusmn6
5834
46
plusmn8
4718
32
plusmn2
93ns
nsns
Dor
ylai
mid
ae27
57
plusmn5
7648
78
plusmn6
6537
40
plusmn6
5838
94
plusmn5
6448
10
plusmn11
67
374
9plusmn
470
243
8plusmn
299
Plt
005
nsP
lt0
05Sm
all
197
plusmn0
671
08plusmn
078
251
plusmn0
900
54plusmn
024
164
plusmn0
962
59plusmn
110
054
plusmn0
30ns
nsns
Dor
ylai
mid
aeP
lect
us8
13plusmn
175
440
plusmn2
027
41plusmn
226
512
plusmn1
1010
24
plusmn3
334
93plusmn
155
443
plusmn1
30P
raty
lenc
hus
305
0plusmn
585
124
8plusmn
675
157
6plusmn
348
272
2plusmn
883
436
plusmn1
2421
58
plusmn5
6642
38
plusmn11
62
Plt
005
nsP
lt0
05Ty
lenc
hola
imus
101
plusmn0
430
36plusmn
050
070
plusmn0
260
66plusmn
064
042
plusmn0
250
93plusmn
087
084
plusmn0
38ns
nsns
Tabl
e2
Effe
cts
ofcr
oppi
ngpa
tter
nti
llag
esy
stem
and
soil
dept
hon
soil
food
web
indi
ces
(EI=
Enr
ichm
ent
inde
xSI
=St
ruct
ure
inde
xB
I=
Bas
alin
dex
CI=
Cha
nnel
inde
x)t
otal
num
ber
ofne
mat
odes
(N)
and
taxa
rich
ness
(S)
Fva
lues
and
leve
lof
sign
ifica
nce
are
indi
cate
d(n
s=
not
sign
ifica
nt)
Dat
aar
efr
omth
efo
ursa
mpl
ing
date
s(n
=12
6)
Cro
ppin
gT
illag
eD
epth
Uni
vari
ate
F=
452
P
lt0
0001
F=
269
P
lt0
05F
=5
34
Plt
000
01
Con
tinuo
usFa
llow
No-
tilla
geSt
anda
rd0-
5cm
5-15
cm15
-30
cmC
ropp
ing
Till
age
Dep
thcr
oppi
ng
N85
972
plusmn64
35
599
53plusmn
800
362
631
plusmn66
25
832
94plusmn
878
194
076
plusmn10
665
821
56plusmn
960
448
232
plusmn61
25
Plt
005
nsP
lt0
01S
761
plusmn0
157
85plusmn
012
781
plusmn0
127
65plusmn
015
745
plusmn0
157
74plusmn
017
795
plusmn0
17ns
nsP
lt0
05E
I65
66
plusmn2
0166
64
plusmn1
7264
77
plusmn1
5267
53
plusmn2
2073
58
plusmn1
7960
63
plusmn2
2064
03
plusmn2
30ns
nsP
lt0
01SI
262
9plusmn
315
436
2plusmn
209
343
3plusmn
259
355
7plusmn
300
291
1plusmn
364
297
7plusmn
283
422
7plusmn
332
Plt
000
1ns
Plt
001
BI
297
6plusmn
172
264
1plusmn
149
291
4plusmn
137
270
2plusmn
186
229
0plusmn
161
335
0plusmn
202
285
6plusmn
191
nsns
Plt
005
CI
408
5plusmn
371
432
6plusmn
320
471
7plusmn
328
369
3plusmn
348
239
3plusmn
233
533
4plusmn
417
483
7plusmn
428
nsP
lt0
001
Plt
001
Vol 8(5) 2006 707
S Saacutenchez-Moreno et al
Table 3 Direct effects of tillage (ST = standard tillage NT = no-till) cropping pattern (F = fallow CC = continuous cropping)and soil depth (0-5 5-15 and 15-30 cm) on abundance ofnematode taxa and on soil food web indices (S = taxa richnessN = total number of nematodes EI = Enrichment index SI =Structure index BI = Basal index CI = Channel index) Trophicgroup (Ba = bacterial feeders Fu = fungal feeders Pp = plantparasites P = predators O = omnivores) of nematode taxa areindicated
Trophic Cp Tillage Cropping Depthgroup pattern (cm)
Aphelenchus Fu 2 ST CC 0-5Tylenchidae PpFu 2 NT CC 5-15Acrobeloides Ba 2 ST CC 0-5Panagrolaimus Ba 1 ST CC 0-5Rhabditidae Ba 1 ST CC 0-5Tylenchorhynchus Pp 3 NT F 5-15Dorylaimidae O 4 ST F 5-15Small Dorylaimidae O 4 NT CC 5-15Plectus Ba 2 NT CC 5-15Pratylenchus Pp 3 NT CC 5-15Tylencholaimus Fu 4 NT CC 5-15N ST CC 0-5S NT F 5-15EI ST CC 0-5SI ST F 15-30BI NT CC 5-15CI NT F 15-30
related (r between 049 and 083 P lt 005) NH+4
was associated with intermittent fallow and correlatedwith ergosterol and MBC (r between 049 and 052P lt 005) PLFA of fungal markers were correlated withergosterol (r = 035 P lt 005) and with PLFA ofbacterial markers (r = 095 P lt 005)
Influence of environmental variables on nematode taxaand soil food web descriptors
In December 2004 at the end of the experiment inthe ordination of the nematode taxa in the multivariatespace defined by the environmental variables positivevalues for most of the soil properties grouped togetherindicating soil enrichment and high biological activity(Fig 3a b) The PLFA biomarkers of both bacteria andfungi were related with the abundance of AcrobeloidesMesorhabditis and Tylenchorhynchus Panagrolaimus andAcrobeles both bacterial feeders were not correlated witheither group of PLFAs and ordered in the opposite part ofthe graph Tylenchidae was associated with pH (r = 047P lt 005) Aphelenchoides was associated with NOminus
3
The abundance of all the omnivores and predators(Discolaimus Aporcelaimidae Qudsianematidae and My-lonchulus) except Prionchulus were inversely correlatedwith almost all soil properties The EI was negativelycorrelated with the CI (r = minus093 P lt 005) BI(r = minus095 P lt 005) taxa richness (r = minus056P lt 005) bulk density (r = minus040 P lt 005) andPLFA of bacterial markers (r = minus035 P lt 005) It waspositioned in the opposite part of the graph than BI andCI (Fig 3) CI was positively correlated with bulk densityand PLFA of fungal markers (r = 037 and 034 respec-tively P lt 005) SI was negatively correlated with NOminus
3 pH and K (r = minus037 minus033 and minus034 P lt 005)Taxa richness and number of nematodes were negativelycorrelated (r = minus036 P lt 005) Number of nematodeswas associated with total C and taxa richness with bulkdensity CI and BI were positively correlated (r = 086P lt 005)
Discussion
The aim of this study was to evaluate the relationshipsbetween nematode faunal composition and soil propertiesas determined by agricultural management It is generallyaccepted that nematodes are strongly influenced by theirmicroenvironment and provide a useful reflection ofsoil health status and several soil functions (Mulder etal 2005) The use of multivariate statistics especiallyCanonical Analysis has improved the understanding ofthe complex relationships between different groups of soilfauna and between organisms and soil physical-chemicalproperties (Popovici amp Ciobanu 2000 Wardle et al2001 Fiscus amp Neher 2002)
As expected from previous studies (eg Wardle 1995)total nematode abundance was not strongly influenced bytillage due to the varied responses of different taxa Ne-matode responses to tillage and cropping intensity var-ied with their trophic group bacterial feeders and fun-gal feeders were stimulated by tillage and reduced un-der intermittent fallow plant-feeders were generally in-hibited by both tillage and intermittent fallow and preda-tors and omnivores were stimulated by intermittent fallowand did not respond clearly to tillage practices In factthe few omnivores and predators in this and most agri-cultural fields probably represent the more tolerant taxawithin these trophic levels Taxa intolerant to disturbancemay no longer be present in arable soils These observa-tions agree with Lenz and Eisenbeis (2000) who found nochanges in total nematode abundance and an increase of
708 Nematology
Effects of soil management on soil food webs
Table 4 Average values (plusmn SE) of soil properties in the four different treatments across three depths Significant effects of treatments(NTCC STCC STF NTF) crop pattern (CC and F) and tillage (ST and NT) are indicated by level of significance Data are from thelast sampling date (December 2004 n = 36) Data from Minoshima et al (2006)
NTF STF NTCC STCC Treatment Crop Tillage
Total C () 106 plusmn 003 099 plusmn 001 107 plusmn 004 103 plusmn 002 P lt 005Total N () 012 plusmn 000 011 plusmn 000 012 plusmn 000 012 plusmn 000 P lt 005pH 707 plusmn 003 686 plusmn 003 708 plusmn 006 690 plusmn 004 P lt 001 P lt 0001K (mg lminus1) 700 plusmn 049 591 plusmn 013 786 plusmn 132 734 plusmn 080P (microg gminus1) 1738 plusmn 088 1578 plusmn 031 1908 plusmn 217 1598 plusmn 083NO3 454 plusmn 106 550 plusmn 148 646 plusmn 092 1203 plusmn 253 P lt 005 P lt 005
(microg N gminus1)
NH4 236 plusmn 131 127 plusmn 054 116 plusmn 027 106 plusmn 016(microg N gminus1)
MBC 17123 plusmn 2623 14816 plusmn 1905 26275 plusmn 6398 17158 plusmn 1823(microg C gminus1)
Ergosterol 99932 plusmn 16846 57594 plusmn 3631 224691 plusmn 82975 121820 plusmn 25685 P lt 005(ng gminus1)
Bulk density 134 plusmn 002 125 plusmn 003 132 plusmn 002 125 plusmn 002 P lt 005 P lt 001(gcm3)
PLFAba 190753 plusmn 50529 144540 plusmn 35185 230127 plusmn 55833 208676 plusmn 31240(mgm2)
PLFAfu 24662 plusmn 12047 14295 plusmn 4381 55785 plusmn 26261 27208 plusmn 7651(mgm2)
bacterial-feeder nematodes after the first tillage treatmentOur results indicate that the response of total nematodeabundance to management depends on the assemblagecomposition so no general patterns can be discerned with-out analysing separately the taxa and functional group re-sponses For example Liphadzi et al (2005) found gen-eral increase in nematode abundance in tilled plots due tothe predominance of fungal feeders and bacterial feeders(up to 90) in the assemblages they studied
Throughout the four sampling dates of this study mostof the microbial feeders (Panagrolaimus RhabditidaeAphelenchus and Acrobeloides) were positively associ-ated with standard tillage indicating the stimulatory effecton microbes of incorporating organic matter into the soilThe nematodes less responsive to incorporated organicmatter were the higher cp taxa (Tylenchorhynchus Tylen-cholaimus Pratylenchus and some Dorylaimidae) whichwere associated with no-tillage Even though a greaternumber of taxa (especially of upper trophic levels) andhigher resolution identification would be desirable to in-fer relationships more reliably (Yeates 2003 Mulder etal 2005) we observed significant relationships betweensensitivity to tillage and trophic or cp groups as similarlyreported by Fiscus and Neher (2002)
Plectus was the only bacterivore associated with thesoil properties of the NT treatments suggesting a highersensitivity to tillage practices While Fiscus and Neher(2002) suggested that Plectus is an indicator of distur-bance due to the concordance between its cp value (2)and its tolerance to chemical and mechanical perturba-tions we found it to be more sensitive to tillage than ex-pected from its cp value Different responses among ge-nera in the same trophic group are common (Porazinska etal 1999) and nematode genera within the same trophicgroup can exhibit asymmetric competition negatively in-fluencing the abundance of other genera (Postma-Blaaw etal 2005) so responses to perturbation may be influencedby the presence of other nematode taxa Greater taxo-nomic resolution may be necessary to resolve differencesin response to environmental variables among nematodeswithin higher taxonomic groupings (Yeates 2003) espe-cially for taxa that have numerous species and a broad sizerange (eg Plectus)
Bacterial feeders are usually abundant in cultivatedsoils while predators and omnivores often disappear withcultivation (Wardle et al 1995) Microbivorous nema-todes belonging to the cp 1 group (eg Panagrolaimusor Rhabditidae enrichment-opportunistic nematodes) andthose with longer life cycles in the cp 2 group (eg Aphe-
Vol 8(5) 2006 709
S Saacutenchez-Moreno et al
Fig 2 Canonical correspondence analysis bi-plot of effects of tillage system crop pattern and depth on nematode abundances andsoil food web indices Environmental variables are marked by arrows Aphel Aphelenchus Tyl Tylenchidae Acro Acrobeloides PanPanagrolaimus Rhab Rhabditidae Tylen Tylenchorhynchus Dor Dorylaimidae SDor Small Dorylaimidae Plec Plectus PratPratylenchus Tylo Tylencholaimus N Total number of nematodes S Taxa richness EI Enrichment index SI Structure index BIBasal index CI Channel index Eigenvalues were 0568 and 0362 for the first and the second root respectively Percentage of varianceexplained was 330 for both root 1 and root 2
lenchus and Acrobeloides) were also associated with con-tinuous cropping The combined effect of standard tillageand continuous cropping significantly enhanced the abun-dance of nematodes at the entry level of the soil foodweb Bacterial-feeding nematodes influence C- and N-
mineralisation by feeding on bacteria excreting NH+4 and
by spreading bacteria through the soil (Bouwman et al1994 Fu et al 2005) Mesorhabditis and Acrobeloidestwo of the most abundant bacterial-feeders in our plotswere positively associated with NH+
4 a reasonable expec-
Fig 3 Scatter plot of CCA ordination showing relationships between soil properties and nematode taxa abundance (a) and soil foodweb indices taxa richness and total number of nematodes (b) Acro Acrobeles Acrob Acrobeloides Aphel Aphelenchus AphoAphelenchoides Aporce Aporcelaimidae Diph Diphtherophora Disco Discolaimus Dity Ditylenchus Meso Mesorhabditis MylMylonchulus Pan Panagrolaimus Plec Plectus Prat Pratylenchus Prion Prionchulus Qudsi Qusianematidae Tyl TylenchidaeTylen Tylenchorhynchus Eigenvalues were 097 and 096 (a) and 080 and 058 (b) for roots 1 and 2 respectively Percentages ofexplained variance for roots 1 and 2 were 107 and 110 (a) and 114 and 64 (b) respectively
710 Nematology
Effects of soil management on soil food webs
Vol 8(5) 2006 711
S Saacutenchez-Moreno et al
tation for the group associated with increased N mineral-isation (Ferris et al 1997 2004) By contrast Panagro-laimus and Plectus ordered in an opposite position due totheir negative relationship with PLFA biomarkers of fungiand bacteria and with bulk density Panagrolaimus has ahigh metabolic rate and a broad non-selective microbialfeeding habit (De Mesel et al 2004) It may decreasebacterial populations (as indicated by lower PFLA frombacterial markers) to a greater extent than other bacter-ial feeders in our plots When microbivorous nematodespredominate in soils they enhance N mineralisation andthus the availability of N for plants (Ferris et al 2004)Total soil N may be correlated with abundance of certainnematodes (Nakamoto et al 2006) but potentially min-eralisable N is a better indicator of N availability Thatmight explain why total soil N was associated only withabundance of Tylenchidae in this study Total C on thecontrary was more strongly associated with total nema-tode abundance
Surprisingly the abundance of fungal-feeding nema-todes such as Aphelenchus and some Tylenchidae was notrelated as strongly with ergosterol as expected suggest-ing that fungal biomass may not determining the size offungal feeder populations Villenave et al (2004) founddiffering responses of fungal feeders to ergosterol contentfungal feeders in cp groups 2 and 4 were positively relatedwith ergosterol but fungal feeders in the cp 5 group werenot
The discrimination between responses of nematodesin the higher and the lower levels of the soil food webwas evident in the CCA ordination revealing a link be-tween lower trophic levels and MBC NH+
4 ergosteroltotal N total C and certain PLFA Bacterial- fungal-and plant-feeding taxa with low cp values ordered op-posite to predatory and omnivore nematodes such asPrionchulus Qudsianematidae Aporcelaimidae Disco-laimus and Mylonchulus With the only exceptions ofthe plant-feeder Tylenchorhynchus (cp 3) which orderedclose to Mesorhabditis (cp 1) and Acrobeles (cp 2) whichscored close to the predators (cp 4 5) nematodes belong-ing to cp groups 1 and 2 showed an opposite response toenvironmental variables than those in cp groups 3 4 and 5
Predatory and omnivore nematodes are in higher co-loniser-persistent groups (3) and are more sensitive tosoil perturbation Intermittent fallow and standard tillagesupported higher abundances of most of the predators andomnivores Mylonchulus Qudsianematidae Prionchulusand Aporcelaimidae It is generally accepted that nema-tode functional diversity decreases with increasing man-
Table 5 Summarized effects of treatments on nematode trophicgroups (Ba = bacterial-feeders Fu = fungal-feeders Pp =plant-feeders PO = predators and omnivores)
Standard tillage No-tillage
Fallow Small increase of Ba Decrease of BaSmall decrease of Fu Decrease of FuDecrease of Pp Small decrease of PpIncrease of PO Increase of POIncrease of SI values Increase of CI values
Continuous Increase of Ba Small decrease of Bacropping Small increase of Fu Increase of Fu
Increase of Pp Increase of PpDecrease of PO Decrease of POIncrease of EI values Increase of BI values
agement intensity (Mulder et al 2003) predatory nema-todes were in our case much more affected by the crop-ping pattern (being enhanced in the intermittent fallowtreatment) than by standard tillage Our results thus sug-gest that even though predatory nematodes are sensitive tosoil physical perturbation other soil forces can drive theirabundance In some studies 25 years of tillage did notstrongly affect predators but reduced fungal-feeder nema-todes (Wang et al 2004)
An increase in predator and omnivore nematodes wasexpected in CC treatments as a result of the continuousincorporation of C into the soil but was not found (Ta-ble 5) Minoshima et al (2006) found that nematodesin the higher trophic levels were not significantly asso-ciated with the C pools in the soil Previous studies foundomnivore and predatory nematodes much more abundantin recently abandoned fallow fields than in cultivated orseminatural meadow lands (Haacutenel 2003) Polis et al(2000) suggest that trophic cascades produced by com-plex trophic interactions are abundant in soil systemsbut bottom-up regulation is difficult to demonstrate insoil trophic levels due to the high complexity of the soilbiota interactions In forest soils Salomon et al (2006)found more abundant microbial grazers when abundantresources were added to the soil but the effects did notextend into higher trophic levels of the soil food webleading to the conclusion that the availability of resourcesplays a minor role structuring soil food webs
Responses of plant-parasites and root feeders to tillageare usually difficult to interpret and are more closely re-lated to plant status and phenology than to soil propertiesThe association between Pratylenchus (endoparasite) andstandard tillage might be explained by the release of the
712 Nematology
Effects of soil management on soil food webs
nematodes from the roots as a result of tillage (Lenz ampEisenbeis 2000)
Ammonium MBC C K P and ergosterol were pos-itively related with total number of nematodes and theEI The EI is based on the weighted abundance of bacte-rial feeding nematodes enrichment-opportunistic relativeto longer life cycle bacterial-feeders indicating highlyactive bacterial-mediated decomposition channels Whenthe field is organically enriched these nematodes exploitthe abundant resources (fungi and bacteria) and increaserapidly in abundance due to their short life cycles and highfecundity (Bongers 1990) On the contrary high valuesof the CI indicate slower fungal-mediated decompositionpathways so a significant relationship between CI and er-gosterol was expected but not found CI was positivelycorrelated with PLFA of fungal biomarkers and EI wasnegatively correlated with PLFA of bacterial markers butnot correlated with MBC Thus the relationship betweenPLFA and microbial grazers may reflect the strength of thegrazing pressure at the sampling time The prevalence ofopportunistic bacterial feeders over other microbial feed-ers (as expressed by the EI) may decrease bacterial bio-mass (indicated by PLFA of bacterial markers) more obvi-ously than the effect of fungal feeders on fungal biomassas indicated by the positive association between the CIindicator of the prevalence of fungal-feeding nematodesover bacterial feeders with fungal biomass (inferred fromPLFA of fungal markers) The absence of correlation be-tween MBC and nematode populations may thus indicatethat the grazing pressure affects only certain microbes andnot the total microbial community
CI and BI were strongly correlated and associatedwith deeper soil layers and no tillage across all samplingdates High BI values indicate a nematode assemblagecomposed of perturbation-resistant nematodes mainly oflower trophic levels The community structure was in thiscase associated with fungal-dominated organic matterdecomposition pathways The SI was associated withdeeper soil layers and intermittent fallow suggesting anegative relationship between predator abundance and thehigh physical disturbance and biological activity presentat the soil surface and in the continuous cropping plots
Conclusions
Different tillage practices and cropping systems deter-mine soil properties and thus nematode abundance Theseeffects vary with nematode trophic and functional group
By the end of the experiment each treatment supporteddifferent nematode assemblages and soil food webs
Each soil food web index describes a model nema-tode assemblage (Ferris et al 2001) Our four treat-ments structured four different nematode assemblagesThe combination of standard tillage and continuous crop-ping (STCC) was associated with high EI values reflect-ing an assemblage predominantly composed of bacterial-feeding nematodes with short life cycles This enrichedassemblage was especially characteristic of the upper soillayer Perhaps not surprisingly for a long-disturbed agri-cultural system we did not find the relationships we ex-pected between continuous cropping and the abundanceof predator and omnivore nematodes The organisms inthe higher levels of the soil food web did not respond tothe continuous input of C in the soil and a long recoveryperiod may be required for appropriate taxa to be rein-troduced and to increase Intermittent fallow (especiallySTF) supported a longer more structured soil food web(high SI values) especially in the deeper soil layers Thecombination of no tillage and intermittent fallow (NTF)supported a fungal-based community with slower organicmatter decomposition rates especially below the upper 5cm of soil The accumulation of plant residues on the soilsurface may result in slower incorporation of C into thefood web and exploitation by fungi Indeed the absenceof tillage and thus of physical perturbation would not dis-rupt fungal hyphae Finally the combination of no tillageand continuous cropping (NTCC) supported a less well-defined assemblage dominated by basal perturbation-resistant nematodes
Acknowledgements
This research was supported by California Bay DeltaAuthority (CBDA)-Ecosystem Restoration Program grant ERP-02-P36 by the California Department of Food andAgricultureKearney Foundation of Soil Science Projects2003011 and by the Kearney Foundation of Soil ScienceProject 2005210 We thank the LTRAS staff for fieldmanagement Many thanks to members of the Jackson andTemple lab groups for help with sampling and Dr S Goyalfor guidance with the HPLC
References
ADEDIRAN JA ADEGBITE AA AKINLOSOTU TAAGBAJE GO TAIWO LB OWOLADE OF amp
Vol 8(5) 2006 713
S Saacutenchez-Moreno et al
OLUWATOSIN GA (2005) Evaluation of fallow and covercrops for nematode suppression in three agroecologies ofsouth western Nigeria African Journal of Biotechnology 41034-1039
BERKELMANS R FERRIS H TENUTA M amp VAN
BRUGGEN AHC (2003) Effects of long-term crop man-agement on nematode trophic levels other than plant feedersdisappear after 1 year of disruptive soil management AppliedSoil Ecology 23 223-235
BONGERS T (1990) The maturity index an ecological mea-sure of environmental disturbance based on nematode speciescomposition Oecologia 83 14-19
BONGERS T amp BONGERS M (1998) Functional diversity ofnematodes Applied Soil Ecology 10 239-251
BOSSIO DA SCOW KM GUNAPALA N amp GRAHAMKJ (1998) Determinants soil microbial communities ef-fects of agricultural management season and soil type onphospholipids fatty acid profiles Microbial Ecology 36 1-12
BOUWMAN LA BLOEM J VAN DEN BOOGERT PHJFBREMER F HOENDERBOOM GHJ amp DE RUITER PC(1994) Short-term and long-term effects of bacterivorousnematodes and nematophagous fungi on carbon and nitrogenmineralization in microcosms Biology and Fertility of Soils17 249-256
BULLUCK III LR BARKER KR amp RISTAINO JB (2002)Influences of organic and synthetic soil fertility amendmentson nematode trophic groups and community dynamics undertomatoes Applied Soil Ecology 21 233-250
CADET P PATEacute E amp NrsquoDIAYE-FAYE N (2003) Nematodecommunity changes and survival rates under natural fallow inthe sudano sahelian area of Senegal Pedobiologia 47 149-160
CHAN KY (2001) An overview of some tillage impacts onearthworm population abundance and diversity ndash implicationsfor functioning in soils Soil and Tillage Research 57 179-191
DE MESEL I DERYCKE S MOENS T VAN DER GUCHTK VINCX M amp SWINGS J (2004) Top-down impactof bacteriovorous nematodes on the bacterial communitystructure a microcosm study Environmental Microbiology 6733-744
EKSCHMITT E STIERHOF T DAUBER J KREIMES Kamp WOLTERS V (2003) On the quality of soil biodiversityindicators abiotic parameters as predictor of soil faunalrichness at different spatial scales Agriculture Ecosystemsand Environment 98 273-283
ETTEMA CH (1998) Soil nematode diversity species coex-istence and ecosystem function Journal of Nematology 30159-169
FERRIS H VENETTE RC amp LAU SS (1997) Populationenergetics of bacterial-feeding nematodes Carbon and nitro-gen budgets Soil Biology and Biochemistry 29 1183-1194
FERRIS H BONGERS T amp DE GOEDE RGM (2001) Aframework for soil food web diagnostics extension of the
nematode faunal analysis concept Applied Soil Ecology 1813-29
FERRIS H VENETTE RC amp SCOW KM (2004) Soil man-agement to enhance bacteriovore and fungivore nematodepopulations and their nitrogen mineralization function Ap-plied Soil Ecology 25 19-35
FISCUS DA amp NEHER DA (2002) Distinguishing sensi-tivity of free-leaving soil nematode genera to physical andchemical disturbances Ecological Applications 12 565-575
FU S FERRIS H BROWN D amp PLANT R (2005) Doespositive feedback effect of nematodes on the biomass andactivity of their bacteria prey vary with nematode speciesand population size Soil Biology and Biochemistry 37 1979-1987
GYEDU-ABABIO TK FURTENBERG JP BAIRD D ampVANREUSEL A (1999) Nematodes as indicators of pollu-tion a case study from the Swartkops river system SouthAfrica Hydrobiologia 397 155-169
HAacuteNEL L (2003) Recovery of soil nematode populations fromcropping stress by natural secondary succession to meadowland Applied Soil Ecology 22 255-270
KLADIVCO EJ (2001) Tillage systems and soil ecology Soiland Tillage Research 61 61-76
KORTHALS GW VAN DE ENDE A VAN MEGEN HLEXMOND THM KAMMENGA JE amp BONGERS T(1996) Short-term effects of cadmium copper nickel andzinc on soil nematodes from different feeding and life-historystrategy groups Applied Soil Ecology 4 107-117
LENZ R amp EISENBEIS G (2000) Short-term effects ofdifferent tillage in a sustainable farming system on nematodecommunity structure Biology and Fertility of Soils 31 237-244
LIPHADZI KB AL-KHATIB K BENSCH C STAHLMANPW DILLE JA TODD T RICE CW HORAK MJamp HEAD G (2005) Soil microbial and nematode commu-nities as affected by glyphosate and tillage practices in aglyphosate-resistant cropping system Weed Science 53 536-545
MIKOLA J amp SETAumlLAuml H (1998a) No evidence of trophiccascades in an experimental microbial-based soil food webEcology 79 153-164
MIKOLA J amp SETAumlLAuml H (1998b) Relating species diversityto ecosystem functioning mechanistic backgrounds and ex-perimental approach with a decomposer food web Oikos 83180-194
MINOSHIMA H JACKSON LE CAVAGNARO TRSAacuteNCHEZ-MORENO S FERRIS H TEMPLE S ampMITCHELL J (2006) Soil food webs and carbon dynam-ics in response to conservation tillage in legume rotations inCalifornia Soil Science Society of America in press
MULDER C DE ZWART D VAN WIJNEN HJSCHOUTEN AJ amp BREURE AM (2003) Observa-tional and simulated evidence of ecological shifts withinthe soil nematode community of agroecosystems under
714 Nematology
Effects of soil management on soil food webs
conventional and organic farming Functional Ecology 17516-525
MULDER C SCHOUTEN AJ HUND-RINKE K ampBREURE AM (2005) The use of nematodes in ecologi-cal soil classification and assessment concepts Ecotoxicologyand Environmental Safety 62 278-289
NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
PORAZINSKA DL DUNCAN LW MCSORLEY R ampGRAHAM JH (1999) Nematode communities as indicatorsof status and processes of a soil ecosystems influenced byagricultural management practices Applied Soil Ecology 1369-86
POSTMA-BLAAUW MB DE VRIES FT DE GOEDERGM BLOEM J FABER JH amp BRUSSAARD L(2005) Within-trophic group interactions of bacterivorousnematode species and their effects on the bacterial commu-nity and nitrogen mineralization Oecologia 142 428-439
ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
SALOMON J ALPHEI J RUF A SCHAEFER M SCHEUS SCHNEIDER K SUumlHRIG A amp MARAUN M (2006)Transitory dynamic effects in the soil invertebrate communityin a temperate deciduous forest Effects of resource qualitySoil Biology and Biochemistry 38 209-221
SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
STATSOFT INC (1996) STATISTICA for Windows (ComputerProgram Manual) Tulsa OK USA
THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
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YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
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Vol 8(5) 2006 715
Effects of soil management on soil food websTa
ble
1E
ffect
sof
crop
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till
age
syst
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Con
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Stan
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and
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food
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Con
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53plusmn
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94plusmn
878
194
076
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960
448
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761
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plusmn2
30ns
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9plusmn
315
436
2plusmn
209
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3plusmn
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355
7plusmn
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291
1plusmn
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297
7plusmn
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422
7plusmn
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6plusmn
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264
1plusmn
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0plusmn
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335
0plusmn
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285
6plusmn
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Vol 8(5) 2006 707
S Saacutenchez-Moreno et al
Table 3 Direct effects of tillage (ST = standard tillage NT = no-till) cropping pattern (F = fallow CC = continuous cropping)and soil depth (0-5 5-15 and 15-30 cm) on abundance ofnematode taxa and on soil food web indices (S = taxa richnessN = total number of nematodes EI = Enrichment index SI =Structure index BI = Basal index CI = Channel index) Trophicgroup (Ba = bacterial feeders Fu = fungal feeders Pp = plantparasites P = predators O = omnivores) of nematode taxa areindicated
Trophic Cp Tillage Cropping Depthgroup pattern (cm)
Aphelenchus Fu 2 ST CC 0-5Tylenchidae PpFu 2 NT CC 5-15Acrobeloides Ba 2 ST CC 0-5Panagrolaimus Ba 1 ST CC 0-5Rhabditidae Ba 1 ST CC 0-5Tylenchorhynchus Pp 3 NT F 5-15Dorylaimidae O 4 ST F 5-15Small Dorylaimidae O 4 NT CC 5-15Plectus Ba 2 NT CC 5-15Pratylenchus Pp 3 NT CC 5-15Tylencholaimus Fu 4 NT CC 5-15N ST CC 0-5S NT F 5-15EI ST CC 0-5SI ST F 15-30BI NT CC 5-15CI NT F 15-30
related (r between 049 and 083 P lt 005) NH+4
was associated with intermittent fallow and correlatedwith ergosterol and MBC (r between 049 and 052P lt 005) PLFA of fungal markers were correlated withergosterol (r = 035 P lt 005) and with PLFA ofbacterial markers (r = 095 P lt 005)
Influence of environmental variables on nematode taxaand soil food web descriptors
In December 2004 at the end of the experiment inthe ordination of the nematode taxa in the multivariatespace defined by the environmental variables positivevalues for most of the soil properties grouped togetherindicating soil enrichment and high biological activity(Fig 3a b) The PLFA biomarkers of both bacteria andfungi were related with the abundance of AcrobeloidesMesorhabditis and Tylenchorhynchus Panagrolaimus andAcrobeles both bacterial feeders were not correlated witheither group of PLFAs and ordered in the opposite part ofthe graph Tylenchidae was associated with pH (r = 047P lt 005) Aphelenchoides was associated with NOminus
3
The abundance of all the omnivores and predators(Discolaimus Aporcelaimidae Qudsianematidae and My-lonchulus) except Prionchulus were inversely correlatedwith almost all soil properties The EI was negativelycorrelated with the CI (r = minus093 P lt 005) BI(r = minus095 P lt 005) taxa richness (r = minus056P lt 005) bulk density (r = minus040 P lt 005) andPLFA of bacterial markers (r = minus035 P lt 005) It waspositioned in the opposite part of the graph than BI andCI (Fig 3) CI was positively correlated with bulk densityand PLFA of fungal markers (r = 037 and 034 respec-tively P lt 005) SI was negatively correlated with NOminus
3 pH and K (r = minus037 minus033 and minus034 P lt 005)Taxa richness and number of nematodes were negativelycorrelated (r = minus036 P lt 005) Number of nematodeswas associated with total C and taxa richness with bulkdensity CI and BI were positively correlated (r = 086P lt 005)
Discussion
The aim of this study was to evaluate the relationshipsbetween nematode faunal composition and soil propertiesas determined by agricultural management It is generallyaccepted that nematodes are strongly influenced by theirmicroenvironment and provide a useful reflection ofsoil health status and several soil functions (Mulder etal 2005) The use of multivariate statistics especiallyCanonical Analysis has improved the understanding ofthe complex relationships between different groups of soilfauna and between organisms and soil physical-chemicalproperties (Popovici amp Ciobanu 2000 Wardle et al2001 Fiscus amp Neher 2002)
As expected from previous studies (eg Wardle 1995)total nematode abundance was not strongly influenced bytillage due to the varied responses of different taxa Ne-matode responses to tillage and cropping intensity var-ied with their trophic group bacterial feeders and fun-gal feeders were stimulated by tillage and reduced un-der intermittent fallow plant-feeders were generally in-hibited by both tillage and intermittent fallow and preda-tors and omnivores were stimulated by intermittent fallowand did not respond clearly to tillage practices In factthe few omnivores and predators in this and most agri-cultural fields probably represent the more tolerant taxawithin these trophic levels Taxa intolerant to disturbancemay no longer be present in arable soils These observa-tions agree with Lenz and Eisenbeis (2000) who found nochanges in total nematode abundance and an increase of
708 Nematology
Effects of soil management on soil food webs
Table 4 Average values (plusmn SE) of soil properties in the four different treatments across three depths Significant effects of treatments(NTCC STCC STF NTF) crop pattern (CC and F) and tillage (ST and NT) are indicated by level of significance Data are from thelast sampling date (December 2004 n = 36) Data from Minoshima et al (2006)
NTF STF NTCC STCC Treatment Crop Tillage
Total C () 106 plusmn 003 099 plusmn 001 107 plusmn 004 103 plusmn 002 P lt 005Total N () 012 plusmn 000 011 plusmn 000 012 plusmn 000 012 plusmn 000 P lt 005pH 707 plusmn 003 686 plusmn 003 708 plusmn 006 690 plusmn 004 P lt 001 P lt 0001K (mg lminus1) 700 plusmn 049 591 plusmn 013 786 plusmn 132 734 plusmn 080P (microg gminus1) 1738 plusmn 088 1578 plusmn 031 1908 plusmn 217 1598 plusmn 083NO3 454 plusmn 106 550 plusmn 148 646 plusmn 092 1203 plusmn 253 P lt 005 P lt 005
(microg N gminus1)
NH4 236 plusmn 131 127 plusmn 054 116 plusmn 027 106 plusmn 016(microg N gminus1)
MBC 17123 plusmn 2623 14816 plusmn 1905 26275 plusmn 6398 17158 plusmn 1823(microg C gminus1)
Ergosterol 99932 plusmn 16846 57594 plusmn 3631 224691 plusmn 82975 121820 plusmn 25685 P lt 005(ng gminus1)
Bulk density 134 plusmn 002 125 plusmn 003 132 plusmn 002 125 plusmn 002 P lt 005 P lt 001(gcm3)
PLFAba 190753 plusmn 50529 144540 plusmn 35185 230127 plusmn 55833 208676 plusmn 31240(mgm2)
PLFAfu 24662 plusmn 12047 14295 plusmn 4381 55785 plusmn 26261 27208 plusmn 7651(mgm2)
bacterial-feeder nematodes after the first tillage treatmentOur results indicate that the response of total nematodeabundance to management depends on the assemblagecomposition so no general patterns can be discerned with-out analysing separately the taxa and functional group re-sponses For example Liphadzi et al (2005) found gen-eral increase in nematode abundance in tilled plots due tothe predominance of fungal feeders and bacterial feeders(up to 90) in the assemblages they studied
Throughout the four sampling dates of this study mostof the microbial feeders (Panagrolaimus RhabditidaeAphelenchus and Acrobeloides) were positively associ-ated with standard tillage indicating the stimulatory effecton microbes of incorporating organic matter into the soilThe nematodes less responsive to incorporated organicmatter were the higher cp taxa (Tylenchorhynchus Tylen-cholaimus Pratylenchus and some Dorylaimidae) whichwere associated with no-tillage Even though a greaternumber of taxa (especially of upper trophic levels) andhigher resolution identification would be desirable to in-fer relationships more reliably (Yeates 2003 Mulder etal 2005) we observed significant relationships betweensensitivity to tillage and trophic or cp groups as similarlyreported by Fiscus and Neher (2002)
Plectus was the only bacterivore associated with thesoil properties of the NT treatments suggesting a highersensitivity to tillage practices While Fiscus and Neher(2002) suggested that Plectus is an indicator of distur-bance due to the concordance between its cp value (2)and its tolerance to chemical and mechanical perturba-tions we found it to be more sensitive to tillage than ex-pected from its cp value Different responses among ge-nera in the same trophic group are common (Porazinska etal 1999) and nematode genera within the same trophicgroup can exhibit asymmetric competition negatively in-fluencing the abundance of other genera (Postma-Blaaw etal 2005) so responses to perturbation may be influencedby the presence of other nematode taxa Greater taxo-nomic resolution may be necessary to resolve differencesin response to environmental variables among nematodeswithin higher taxonomic groupings (Yeates 2003) espe-cially for taxa that have numerous species and a broad sizerange (eg Plectus)
Bacterial feeders are usually abundant in cultivatedsoils while predators and omnivores often disappear withcultivation (Wardle et al 1995) Microbivorous nema-todes belonging to the cp 1 group (eg Panagrolaimusor Rhabditidae enrichment-opportunistic nematodes) andthose with longer life cycles in the cp 2 group (eg Aphe-
Vol 8(5) 2006 709
S Saacutenchez-Moreno et al
Fig 2 Canonical correspondence analysis bi-plot of effects of tillage system crop pattern and depth on nematode abundances andsoil food web indices Environmental variables are marked by arrows Aphel Aphelenchus Tyl Tylenchidae Acro Acrobeloides PanPanagrolaimus Rhab Rhabditidae Tylen Tylenchorhynchus Dor Dorylaimidae SDor Small Dorylaimidae Plec Plectus PratPratylenchus Tylo Tylencholaimus N Total number of nematodes S Taxa richness EI Enrichment index SI Structure index BIBasal index CI Channel index Eigenvalues were 0568 and 0362 for the first and the second root respectively Percentage of varianceexplained was 330 for both root 1 and root 2
lenchus and Acrobeloides) were also associated with con-tinuous cropping The combined effect of standard tillageand continuous cropping significantly enhanced the abun-dance of nematodes at the entry level of the soil foodweb Bacterial-feeding nematodes influence C- and N-
mineralisation by feeding on bacteria excreting NH+4 and
by spreading bacteria through the soil (Bouwman et al1994 Fu et al 2005) Mesorhabditis and Acrobeloidestwo of the most abundant bacterial-feeders in our plotswere positively associated with NH+
4 a reasonable expec-
Fig 3 Scatter plot of CCA ordination showing relationships between soil properties and nematode taxa abundance (a) and soil foodweb indices taxa richness and total number of nematodes (b) Acro Acrobeles Acrob Acrobeloides Aphel Aphelenchus AphoAphelenchoides Aporce Aporcelaimidae Diph Diphtherophora Disco Discolaimus Dity Ditylenchus Meso Mesorhabditis MylMylonchulus Pan Panagrolaimus Plec Plectus Prat Pratylenchus Prion Prionchulus Qudsi Qusianematidae Tyl TylenchidaeTylen Tylenchorhynchus Eigenvalues were 097 and 096 (a) and 080 and 058 (b) for roots 1 and 2 respectively Percentages ofexplained variance for roots 1 and 2 were 107 and 110 (a) and 114 and 64 (b) respectively
710 Nematology
Effects of soil management on soil food webs
Vol 8(5) 2006 711
S Saacutenchez-Moreno et al
tation for the group associated with increased N mineral-isation (Ferris et al 1997 2004) By contrast Panagro-laimus and Plectus ordered in an opposite position due totheir negative relationship with PLFA biomarkers of fungiand bacteria and with bulk density Panagrolaimus has ahigh metabolic rate and a broad non-selective microbialfeeding habit (De Mesel et al 2004) It may decreasebacterial populations (as indicated by lower PFLA frombacterial markers) to a greater extent than other bacter-ial feeders in our plots When microbivorous nematodespredominate in soils they enhance N mineralisation andthus the availability of N for plants (Ferris et al 2004)Total soil N may be correlated with abundance of certainnematodes (Nakamoto et al 2006) but potentially min-eralisable N is a better indicator of N availability Thatmight explain why total soil N was associated only withabundance of Tylenchidae in this study Total C on thecontrary was more strongly associated with total nema-tode abundance
Surprisingly the abundance of fungal-feeding nema-todes such as Aphelenchus and some Tylenchidae was notrelated as strongly with ergosterol as expected suggest-ing that fungal biomass may not determining the size offungal feeder populations Villenave et al (2004) founddiffering responses of fungal feeders to ergosterol contentfungal feeders in cp groups 2 and 4 were positively relatedwith ergosterol but fungal feeders in the cp 5 group werenot
The discrimination between responses of nematodesin the higher and the lower levels of the soil food webwas evident in the CCA ordination revealing a link be-tween lower trophic levels and MBC NH+
4 ergosteroltotal N total C and certain PLFA Bacterial- fungal-and plant-feeding taxa with low cp values ordered op-posite to predatory and omnivore nematodes such asPrionchulus Qudsianematidae Aporcelaimidae Disco-laimus and Mylonchulus With the only exceptions ofthe plant-feeder Tylenchorhynchus (cp 3) which orderedclose to Mesorhabditis (cp 1) and Acrobeles (cp 2) whichscored close to the predators (cp 4 5) nematodes belong-ing to cp groups 1 and 2 showed an opposite response toenvironmental variables than those in cp groups 3 4 and 5
Predatory and omnivore nematodes are in higher co-loniser-persistent groups (3) and are more sensitive tosoil perturbation Intermittent fallow and standard tillagesupported higher abundances of most of the predators andomnivores Mylonchulus Qudsianematidae Prionchulusand Aporcelaimidae It is generally accepted that nema-tode functional diversity decreases with increasing man-
Table 5 Summarized effects of treatments on nematode trophicgroups (Ba = bacterial-feeders Fu = fungal-feeders Pp =plant-feeders PO = predators and omnivores)
Standard tillage No-tillage
Fallow Small increase of Ba Decrease of BaSmall decrease of Fu Decrease of FuDecrease of Pp Small decrease of PpIncrease of PO Increase of POIncrease of SI values Increase of CI values
Continuous Increase of Ba Small decrease of Bacropping Small increase of Fu Increase of Fu
Increase of Pp Increase of PpDecrease of PO Decrease of POIncrease of EI values Increase of BI values
agement intensity (Mulder et al 2003) predatory nema-todes were in our case much more affected by the crop-ping pattern (being enhanced in the intermittent fallowtreatment) than by standard tillage Our results thus sug-gest that even though predatory nematodes are sensitive tosoil physical perturbation other soil forces can drive theirabundance In some studies 25 years of tillage did notstrongly affect predators but reduced fungal-feeder nema-todes (Wang et al 2004)
An increase in predator and omnivore nematodes wasexpected in CC treatments as a result of the continuousincorporation of C into the soil but was not found (Ta-ble 5) Minoshima et al (2006) found that nematodesin the higher trophic levels were not significantly asso-ciated with the C pools in the soil Previous studies foundomnivore and predatory nematodes much more abundantin recently abandoned fallow fields than in cultivated orseminatural meadow lands (Haacutenel 2003) Polis et al(2000) suggest that trophic cascades produced by com-plex trophic interactions are abundant in soil systemsbut bottom-up regulation is difficult to demonstrate insoil trophic levels due to the high complexity of the soilbiota interactions In forest soils Salomon et al (2006)found more abundant microbial grazers when abundantresources were added to the soil but the effects did notextend into higher trophic levels of the soil food webleading to the conclusion that the availability of resourcesplays a minor role structuring soil food webs
Responses of plant-parasites and root feeders to tillageare usually difficult to interpret and are more closely re-lated to plant status and phenology than to soil propertiesThe association between Pratylenchus (endoparasite) andstandard tillage might be explained by the release of the
712 Nematology
Effects of soil management on soil food webs
nematodes from the roots as a result of tillage (Lenz ampEisenbeis 2000)
Ammonium MBC C K P and ergosterol were pos-itively related with total number of nematodes and theEI The EI is based on the weighted abundance of bacte-rial feeding nematodes enrichment-opportunistic relativeto longer life cycle bacterial-feeders indicating highlyactive bacterial-mediated decomposition channels Whenthe field is organically enriched these nematodes exploitthe abundant resources (fungi and bacteria) and increaserapidly in abundance due to their short life cycles and highfecundity (Bongers 1990) On the contrary high valuesof the CI indicate slower fungal-mediated decompositionpathways so a significant relationship between CI and er-gosterol was expected but not found CI was positivelycorrelated with PLFA of fungal biomarkers and EI wasnegatively correlated with PLFA of bacterial markers butnot correlated with MBC Thus the relationship betweenPLFA and microbial grazers may reflect the strength of thegrazing pressure at the sampling time The prevalence ofopportunistic bacterial feeders over other microbial feed-ers (as expressed by the EI) may decrease bacterial bio-mass (indicated by PLFA of bacterial markers) more obvi-ously than the effect of fungal feeders on fungal biomassas indicated by the positive association between the CIindicator of the prevalence of fungal-feeding nematodesover bacterial feeders with fungal biomass (inferred fromPLFA of fungal markers) The absence of correlation be-tween MBC and nematode populations may thus indicatethat the grazing pressure affects only certain microbes andnot the total microbial community
CI and BI were strongly correlated and associatedwith deeper soil layers and no tillage across all samplingdates High BI values indicate a nematode assemblagecomposed of perturbation-resistant nematodes mainly oflower trophic levels The community structure was in thiscase associated with fungal-dominated organic matterdecomposition pathways The SI was associated withdeeper soil layers and intermittent fallow suggesting anegative relationship between predator abundance and thehigh physical disturbance and biological activity presentat the soil surface and in the continuous cropping plots
Conclusions
Different tillage practices and cropping systems deter-mine soil properties and thus nematode abundance Theseeffects vary with nematode trophic and functional group
By the end of the experiment each treatment supporteddifferent nematode assemblages and soil food webs
Each soil food web index describes a model nema-tode assemblage (Ferris et al 2001) Our four treat-ments structured four different nematode assemblagesThe combination of standard tillage and continuous crop-ping (STCC) was associated with high EI values reflect-ing an assemblage predominantly composed of bacterial-feeding nematodes with short life cycles This enrichedassemblage was especially characteristic of the upper soillayer Perhaps not surprisingly for a long-disturbed agri-cultural system we did not find the relationships we ex-pected between continuous cropping and the abundanceof predator and omnivore nematodes The organisms inthe higher levels of the soil food web did not respond tothe continuous input of C in the soil and a long recoveryperiod may be required for appropriate taxa to be rein-troduced and to increase Intermittent fallow (especiallySTF) supported a longer more structured soil food web(high SI values) especially in the deeper soil layers Thecombination of no tillage and intermittent fallow (NTF)supported a fungal-based community with slower organicmatter decomposition rates especially below the upper 5cm of soil The accumulation of plant residues on the soilsurface may result in slower incorporation of C into thefood web and exploitation by fungi Indeed the absenceof tillage and thus of physical perturbation would not dis-rupt fungal hyphae Finally the combination of no tillageand continuous cropping (NTCC) supported a less well-defined assemblage dominated by basal perturbation-resistant nematodes
Acknowledgements
This research was supported by California Bay DeltaAuthority (CBDA)-Ecosystem Restoration Program grant ERP-02-P36 by the California Department of Food andAgricultureKearney Foundation of Soil Science Projects2003011 and by the Kearney Foundation of Soil ScienceProject 2005210 We thank the LTRAS staff for fieldmanagement Many thanks to members of the Jackson andTemple lab groups for help with sampling and Dr S Goyalfor guidance with the HPLC
References
ADEDIRAN JA ADEGBITE AA AKINLOSOTU TAAGBAJE GO TAIWO LB OWOLADE OF amp
Vol 8(5) 2006 713
S Saacutenchez-Moreno et al
OLUWATOSIN GA (2005) Evaluation of fallow and covercrops for nematode suppression in three agroecologies ofsouth western Nigeria African Journal of Biotechnology 41034-1039
BERKELMANS R FERRIS H TENUTA M amp VAN
BRUGGEN AHC (2003) Effects of long-term crop man-agement on nematode trophic levels other than plant feedersdisappear after 1 year of disruptive soil management AppliedSoil Ecology 23 223-235
BONGERS T (1990) The maturity index an ecological mea-sure of environmental disturbance based on nematode speciescomposition Oecologia 83 14-19
BONGERS T amp BONGERS M (1998) Functional diversity ofnematodes Applied Soil Ecology 10 239-251
BOSSIO DA SCOW KM GUNAPALA N amp GRAHAMKJ (1998) Determinants soil microbial communities ef-fects of agricultural management season and soil type onphospholipids fatty acid profiles Microbial Ecology 36 1-12
BOUWMAN LA BLOEM J VAN DEN BOOGERT PHJFBREMER F HOENDERBOOM GHJ amp DE RUITER PC(1994) Short-term and long-term effects of bacterivorousnematodes and nematophagous fungi on carbon and nitrogenmineralization in microcosms Biology and Fertility of Soils17 249-256
BULLUCK III LR BARKER KR amp RISTAINO JB (2002)Influences of organic and synthetic soil fertility amendmentson nematode trophic groups and community dynamics undertomatoes Applied Soil Ecology 21 233-250
CADET P PATEacute E amp NrsquoDIAYE-FAYE N (2003) Nematodecommunity changes and survival rates under natural fallow inthe sudano sahelian area of Senegal Pedobiologia 47 149-160
CHAN KY (2001) An overview of some tillage impacts onearthworm population abundance and diversity ndash implicationsfor functioning in soils Soil and Tillage Research 57 179-191
DE MESEL I DERYCKE S MOENS T VAN DER GUCHTK VINCX M amp SWINGS J (2004) Top-down impactof bacteriovorous nematodes on the bacterial communitystructure a microcosm study Environmental Microbiology 6733-744
EKSCHMITT E STIERHOF T DAUBER J KREIMES Kamp WOLTERS V (2003) On the quality of soil biodiversityindicators abiotic parameters as predictor of soil faunalrichness at different spatial scales Agriculture Ecosystemsand Environment 98 273-283
ETTEMA CH (1998) Soil nematode diversity species coex-istence and ecosystem function Journal of Nematology 30159-169
FERRIS H VENETTE RC amp LAU SS (1997) Populationenergetics of bacterial-feeding nematodes Carbon and nitro-gen budgets Soil Biology and Biochemistry 29 1183-1194
FERRIS H BONGERS T amp DE GOEDE RGM (2001) Aframework for soil food web diagnostics extension of the
nematode faunal analysis concept Applied Soil Ecology 1813-29
FERRIS H VENETTE RC amp SCOW KM (2004) Soil man-agement to enhance bacteriovore and fungivore nematodepopulations and their nitrogen mineralization function Ap-plied Soil Ecology 25 19-35
FISCUS DA amp NEHER DA (2002) Distinguishing sensi-tivity of free-leaving soil nematode genera to physical andchemical disturbances Ecological Applications 12 565-575
FU S FERRIS H BROWN D amp PLANT R (2005) Doespositive feedback effect of nematodes on the biomass andactivity of their bacteria prey vary with nematode speciesand population size Soil Biology and Biochemistry 37 1979-1987
GYEDU-ABABIO TK FURTENBERG JP BAIRD D ampVANREUSEL A (1999) Nematodes as indicators of pollu-tion a case study from the Swartkops river system SouthAfrica Hydrobiologia 397 155-169
HAacuteNEL L (2003) Recovery of soil nematode populations fromcropping stress by natural secondary succession to meadowland Applied Soil Ecology 22 255-270
KLADIVCO EJ (2001) Tillage systems and soil ecology Soiland Tillage Research 61 61-76
KORTHALS GW VAN DE ENDE A VAN MEGEN HLEXMOND THM KAMMENGA JE amp BONGERS T(1996) Short-term effects of cadmium copper nickel andzinc on soil nematodes from different feeding and life-historystrategy groups Applied Soil Ecology 4 107-117
LENZ R amp EISENBEIS G (2000) Short-term effects ofdifferent tillage in a sustainable farming system on nematodecommunity structure Biology and Fertility of Soils 31 237-244
LIPHADZI KB AL-KHATIB K BENSCH C STAHLMANPW DILLE JA TODD T RICE CW HORAK MJamp HEAD G (2005) Soil microbial and nematode commu-nities as affected by glyphosate and tillage practices in aglyphosate-resistant cropping system Weed Science 53 536-545
MIKOLA J amp SETAumlLAuml H (1998a) No evidence of trophiccascades in an experimental microbial-based soil food webEcology 79 153-164
MIKOLA J amp SETAumlLAuml H (1998b) Relating species diversityto ecosystem functioning mechanistic backgrounds and ex-perimental approach with a decomposer food web Oikos 83180-194
MINOSHIMA H JACKSON LE CAVAGNARO TRSAacuteNCHEZ-MORENO S FERRIS H TEMPLE S ampMITCHELL J (2006) Soil food webs and carbon dynam-ics in response to conservation tillage in legume rotations inCalifornia Soil Science Society of America in press
MULDER C DE ZWART D VAN WIJNEN HJSCHOUTEN AJ amp BREURE AM (2003) Observa-tional and simulated evidence of ecological shifts withinthe soil nematode community of agroecosystems under
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Effects of soil management on soil food webs
conventional and organic farming Functional Ecology 17516-525
MULDER C SCHOUTEN AJ HUND-RINKE K ampBREURE AM (2005) The use of nematodes in ecologi-cal soil classification and assessment concepts Ecotoxicologyand Environmental Safety 62 278-289
NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
PORAZINSKA DL DUNCAN LW MCSORLEY R ampGRAHAM JH (1999) Nematode communities as indicatorsof status and processes of a soil ecosystems influenced byagricultural management practices Applied Soil Ecology 1369-86
POSTMA-BLAAUW MB DE VRIES FT DE GOEDERGM BLOEM J FABER JH amp BRUSSAARD L(2005) Within-trophic group interactions of bacterivorousnematode species and their effects on the bacterial commu-nity and nitrogen mineralization Oecologia 142 428-439
ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
SALOMON J ALPHEI J RUF A SCHAEFER M SCHEUS SCHNEIDER K SUumlHRIG A amp MARAUN M (2006)Transitory dynamic effects in the soil invertebrate communityin a temperate deciduous forest Effects of resource qualitySoil Biology and Biochemistry 38 209-221
SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
STATSOFT INC (1996) STATISTICA for Windows (ComputerProgram Manual) Tulsa OK USA
THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
YAMADA M (2001) Methods of control injury associatedwith continuous vegetable cropping in Japan ndash Crop rotationand several cultural practices Japan Agricultural ResearchQuarterly 35 39-45
YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
YEATES GW BONGERS T DE GOEDE RGM FRECK-MAN DW amp GEORGIEVA SS (1993) Feeding-habits insoil nematode families and genera ndash an outline for soil ecolo-gists Journal of Nematology 25 315-331
Vol 8(5) 2006 715
S Saacutenchez-Moreno et al
Table 3 Direct effects of tillage (ST = standard tillage NT = no-till) cropping pattern (F = fallow CC = continuous cropping)and soil depth (0-5 5-15 and 15-30 cm) on abundance ofnematode taxa and on soil food web indices (S = taxa richnessN = total number of nematodes EI = Enrichment index SI =Structure index BI = Basal index CI = Channel index) Trophicgroup (Ba = bacterial feeders Fu = fungal feeders Pp = plantparasites P = predators O = omnivores) of nematode taxa areindicated
Trophic Cp Tillage Cropping Depthgroup pattern (cm)
Aphelenchus Fu 2 ST CC 0-5Tylenchidae PpFu 2 NT CC 5-15Acrobeloides Ba 2 ST CC 0-5Panagrolaimus Ba 1 ST CC 0-5Rhabditidae Ba 1 ST CC 0-5Tylenchorhynchus Pp 3 NT F 5-15Dorylaimidae O 4 ST F 5-15Small Dorylaimidae O 4 NT CC 5-15Plectus Ba 2 NT CC 5-15Pratylenchus Pp 3 NT CC 5-15Tylencholaimus Fu 4 NT CC 5-15N ST CC 0-5S NT F 5-15EI ST CC 0-5SI ST F 15-30BI NT CC 5-15CI NT F 15-30
related (r between 049 and 083 P lt 005) NH+4
was associated with intermittent fallow and correlatedwith ergosterol and MBC (r between 049 and 052P lt 005) PLFA of fungal markers were correlated withergosterol (r = 035 P lt 005) and with PLFA ofbacterial markers (r = 095 P lt 005)
Influence of environmental variables on nematode taxaand soil food web descriptors
In December 2004 at the end of the experiment inthe ordination of the nematode taxa in the multivariatespace defined by the environmental variables positivevalues for most of the soil properties grouped togetherindicating soil enrichment and high biological activity(Fig 3a b) The PLFA biomarkers of both bacteria andfungi were related with the abundance of AcrobeloidesMesorhabditis and Tylenchorhynchus Panagrolaimus andAcrobeles both bacterial feeders were not correlated witheither group of PLFAs and ordered in the opposite part ofthe graph Tylenchidae was associated with pH (r = 047P lt 005) Aphelenchoides was associated with NOminus
3
The abundance of all the omnivores and predators(Discolaimus Aporcelaimidae Qudsianematidae and My-lonchulus) except Prionchulus were inversely correlatedwith almost all soil properties The EI was negativelycorrelated with the CI (r = minus093 P lt 005) BI(r = minus095 P lt 005) taxa richness (r = minus056P lt 005) bulk density (r = minus040 P lt 005) andPLFA of bacterial markers (r = minus035 P lt 005) It waspositioned in the opposite part of the graph than BI andCI (Fig 3) CI was positively correlated with bulk densityand PLFA of fungal markers (r = 037 and 034 respec-tively P lt 005) SI was negatively correlated with NOminus
3 pH and K (r = minus037 minus033 and minus034 P lt 005)Taxa richness and number of nematodes were negativelycorrelated (r = minus036 P lt 005) Number of nematodeswas associated with total C and taxa richness with bulkdensity CI and BI were positively correlated (r = 086P lt 005)
Discussion
The aim of this study was to evaluate the relationshipsbetween nematode faunal composition and soil propertiesas determined by agricultural management It is generallyaccepted that nematodes are strongly influenced by theirmicroenvironment and provide a useful reflection ofsoil health status and several soil functions (Mulder etal 2005) The use of multivariate statistics especiallyCanonical Analysis has improved the understanding ofthe complex relationships between different groups of soilfauna and between organisms and soil physical-chemicalproperties (Popovici amp Ciobanu 2000 Wardle et al2001 Fiscus amp Neher 2002)
As expected from previous studies (eg Wardle 1995)total nematode abundance was not strongly influenced bytillage due to the varied responses of different taxa Ne-matode responses to tillage and cropping intensity var-ied with their trophic group bacterial feeders and fun-gal feeders were stimulated by tillage and reduced un-der intermittent fallow plant-feeders were generally in-hibited by both tillage and intermittent fallow and preda-tors and omnivores were stimulated by intermittent fallowand did not respond clearly to tillage practices In factthe few omnivores and predators in this and most agri-cultural fields probably represent the more tolerant taxawithin these trophic levels Taxa intolerant to disturbancemay no longer be present in arable soils These observa-tions agree with Lenz and Eisenbeis (2000) who found nochanges in total nematode abundance and an increase of
708 Nematology
Effects of soil management on soil food webs
Table 4 Average values (plusmn SE) of soil properties in the four different treatments across three depths Significant effects of treatments(NTCC STCC STF NTF) crop pattern (CC and F) and tillage (ST and NT) are indicated by level of significance Data are from thelast sampling date (December 2004 n = 36) Data from Minoshima et al (2006)
NTF STF NTCC STCC Treatment Crop Tillage
Total C () 106 plusmn 003 099 plusmn 001 107 plusmn 004 103 plusmn 002 P lt 005Total N () 012 plusmn 000 011 plusmn 000 012 plusmn 000 012 plusmn 000 P lt 005pH 707 plusmn 003 686 plusmn 003 708 plusmn 006 690 plusmn 004 P lt 001 P lt 0001K (mg lminus1) 700 plusmn 049 591 plusmn 013 786 plusmn 132 734 plusmn 080P (microg gminus1) 1738 plusmn 088 1578 plusmn 031 1908 plusmn 217 1598 plusmn 083NO3 454 plusmn 106 550 plusmn 148 646 plusmn 092 1203 plusmn 253 P lt 005 P lt 005
(microg N gminus1)
NH4 236 plusmn 131 127 plusmn 054 116 plusmn 027 106 plusmn 016(microg N gminus1)
MBC 17123 plusmn 2623 14816 plusmn 1905 26275 plusmn 6398 17158 plusmn 1823(microg C gminus1)
Ergosterol 99932 plusmn 16846 57594 plusmn 3631 224691 plusmn 82975 121820 plusmn 25685 P lt 005(ng gminus1)
Bulk density 134 plusmn 002 125 plusmn 003 132 plusmn 002 125 plusmn 002 P lt 005 P lt 001(gcm3)
PLFAba 190753 plusmn 50529 144540 plusmn 35185 230127 plusmn 55833 208676 plusmn 31240(mgm2)
PLFAfu 24662 plusmn 12047 14295 plusmn 4381 55785 plusmn 26261 27208 plusmn 7651(mgm2)
bacterial-feeder nematodes after the first tillage treatmentOur results indicate that the response of total nematodeabundance to management depends on the assemblagecomposition so no general patterns can be discerned with-out analysing separately the taxa and functional group re-sponses For example Liphadzi et al (2005) found gen-eral increase in nematode abundance in tilled plots due tothe predominance of fungal feeders and bacterial feeders(up to 90) in the assemblages they studied
Throughout the four sampling dates of this study mostof the microbial feeders (Panagrolaimus RhabditidaeAphelenchus and Acrobeloides) were positively associ-ated with standard tillage indicating the stimulatory effecton microbes of incorporating organic matter into the soilThe nematodes less responsive to incorporated organicmatter were the higher cp taxa (Tylenchorhynchus Tylen-cholaimus Pratylenchus and some Dorylaimidae) whichwere associated with no-tillage Even though a greaternumber of taxa (especially of upper trophic levels) andhigher resolution identification would be desirable to in-fer relationships more reliably (Yeates 2003 Mulder etal 2005) we observed significant relationships betweensensitivity to tillage and trophic or cp groups as similarlyreported by Fiscus and Neher (2002)
Plectus was the only bacterivore associated with thesoil properties of the NT treatments suggesting a highersensitivity to tillage practices While Fiscus and Neher(2002) suggested that Plectus is an indicator of distur-bance due to the concordance between its cp value (2)and its tolerance to chemical and mechanical perturba-tions we found it to be more sensitive to tillage than ex-pected from its cp value Different responses among ge-nera in the same trophic group are common (Porazinska etal 1999) and nematode genera within the same trophicgroup can exhibit asymmetric competition negatively in-fluencing the abundance of other genera (Postma-Blaaw etal 2005) so responses to perturbation may be influencedby the presence of other nematode taxa Greater taxo-nomic resolution may be necessary to resolve differencesin response to environmental variables among nematodeswithin higher taxonomic groupings (Yeates 2003) espe-cially for taxa that have numerous species and a broad sizerange (eg Plectus)
Bacterial feeders are usually abundant in cultivatedsoils while predators and omnivores often disappear withcultivation (Wardle et al 1995) Microbivorous nema-todes belonging to the cp 1 group (eg Panagrolaimusor Rhabditidae enrichment-opportunistic nematodes) andthose with longer life cycles in the cp 2 group (eg Aphe-
Vol 8(5) 2006 709
S Saacutenchez-Moreno et al
Fig 2 Canonical correspondence analysis bi-plot of effects of tillage system crop pattern and depth on nematode abundances andsoil food web indices Environmental variables are marked by arrows Aphel Aphelenchus Tyl Tylenchidae Acro Acrobeloides PanPanagrolaimus Rhab Rhabditidae Tylen Tylenchorhynchus Dor Dorylaimidae SDor Small Dorylaimidae Plec Plectus PratPratylenchus Tylo Tylencholaimus N Total number of nematodes S Taxa richness EI Enrichment index SI Structure index BIBasal index CI Channel index Eigenvalues were 0568 and 0362 for the first and the second root respectively Percentage of varianceexplained was 330 for both root 1 and root 2
lenchus and Acrobeloides) were also associated with con-tinuous cropping The combined effect of standard tillageand continuous cropping significantly enhanced the abun-dance of nematodes at the entry level of the soil foodweb Bacterial-feeding nematodes influence C- and N-
mineralisation by feeding on bacteria excreting NH+4 and
by spreading bacteria through the soil (Bouwman et al1994 Fu et al 2005) Mesorhabditis and Acrobeloidestwo of the most abundant bacterial-feeders in our plotswere positively associated with NH+
4 a reasonable expec-
Fig 3 Scatter plot of CCA ordination showing relationships between soil properties and nematode taxa abundance (a) and soil foodweb indices taxa richness and total number of nematodes (b) Acro Acrobeles Acrob Acrobeloides Aphel Aphelenchus AphoAphelenchoides Aporce Aporcelaimidae Diph Diphtherophora Disco Discolaimus Dity Ditylenchus Meso Mesorhabditis MylMylonchulus Pan Panagrolaimus Plec Plectus Prat Pratylenchus Prion Prionchulus Qudsi Qusianematidae Tyl TylenchidaeTylen Tylenchorhynchus Eigenvalues were 097 and 096 (a) and 080 and 058 (b) for roots 1 and 2 respectively Percentages ofexplained variance for roots 1 and 2 were 107 and 110 (a) and 114 and 64 (b) respectively
710 Nematology
Effects of soil management on soil food webs
Vol 8(5) 2006 711
S Saacutenchez-Moreno et al
tation for the group associated with increased N mineral-isation (Ferris et al 1997 2004) By contrast Panagro-laimus and Plectus ordered in an opposite position due totheir negative relationship with PLFA biomarkers of fungiand bacteria and with bulk density Panagrolaimus has ahigh metabolic rate and a broad non-selective microbialfeeding habit (De Mesel et al 2004) It may decreasebacterial populations (as indicated by lower PFLA frombacterial markers) to a greater extent than other bacter-ial feeders in our plots When microbivorous nematodespredominate in soils they enhance N mineralisation andthus the availability of N for plants (Ferris et al 2004)Total soil N may be correlated with abundance of certainnematodes (Nakamoto et al 2006) but potentially min-eralisable N is a better indicator of N availability Thatmight explain why total soil N was associated only withabundance of Tylenchidae in this study Total C on thecontrary was more strongly associated with total nema-tode abundance
Surprisingly the abundance of fungal-feeding nema-todes such as Aphelenchus and some Tylenchidae was notrelated as strongly with ergosterol as expected suggest-ing that fungal biomass may not determining the size offungal feeder populations Villenave et al (2004) founddiffering responses of fungal feeders to ergosterol contentfungal feeders in cp groups 2 and 4 were positively relatedwith ergosterol but fungal feeders in the cp 5 group werenot
The discrimination between responses of nematodesin the higher and the lower levels of the soil food webwas evident in the CCA ordination revealing a link be-tween lower trophic levels and MBC NH+
4 ergosteroltotal N total C and certain PLFA Bacterial- fungal-and plant-feeding taxa with low cp values ordered op-posite to predatory and omnivore nematodes such asPrionchulus Qudsianematidae Aporcelaimidae Disco-laimus and Mylonchulus With the only exceptions ofthe plant-feeder Tylenchorhynchus (cp 3) which orderedclose to Mesorhabditis (cp 1) and Acrobeles (cp 2) whichscored close to the predators (cp 4 5) nematodes belong-ing to cp groups 1 and 2 showed an opposite response toenvironmental variables than those in cp groups 3 4 and 5
Predatory and omnivore nematodes are in higher co-loniser-persistent groups (3) and are more sensitive tosoil perturbation Intermittent fallow and standard tillagesupported higher abundances of most of the predators andomnivores Mylonchulus Qudsianematidae Prionchulusand Aporcelaimidae It is generally accepted that nema-tode functional diversity decreases with increasing man-
Table 5 Summarized effects of treatments on nematode trophicgroups (Ba = bacterial-feeders Fu = fungal-feeders Pp =plant-feeders PO = predators and omnivores)
Standard tillage No-tillage
Fallow Small increase of Ba Decrease of BaSmall decrease of Fu Decrease of FuDecrease of Pp Small decrease of PpIncrease of PO Increase of POIncrease of SI values Increase of CI values
Continuous Increase of Ba Small decrease of Bacropping Small increase of Fu Increase of Fu
Increase of Pp Increase of PpDecrease of PO Decrease of POIncrease of EI values Increase of BI values
agement intensity (Mulder et al 2003) predatory nema-todes were in our case much more affected by the crop-ping pattern (being enhanced in the intermittent fallowtreatment) than by standard tillage Our results thus sug-gest that even though predatory nematodes are sensitive tosoil physical perturbation other soil forces can drive theirabundance In some studies 25 years of tillage did notstrongly affect predators but reduced fungal-feeder nema-todes (Wang et al 2004)
An increase in predator and omnivore nematodes wasexpected in CC treatments as a result of the continuousincorporation of C into the soil but was not found (Ta-ble 5) Minoshima et al (2006) found that nematodesin the higher trophic levels were not significantly asso-ciated with the C pools in the soil Previous studies foundomnivore and predatory nematodes much more abundantin recently abandoned fallow fields than in cultivated orseminatural meadow lands (Haacutenel 2003) Polis et al(2000) suggest that trophic cascades produced by com-plex trophic interactions are abundant in soil systemsbut bottom-up regulation is difficult to demonstrate insoil trophic levels due to the high complexity of the soilbiota interactions In forest soils Salomon et al (2006)found more abundant microbial grazers when abundantresources were added to the soil but the effects did notextend into higher trophic levels of the soil food webleading to the conclusion that the availability of resourcesplays a minor role structuring soil food webs
Responses of plant-parasites and root feeders to tillageare usually difficult to interpret and are more closely re-lated to plant status and phenology than to soil propertiesThe association between Pratylenchus (endoparasite) andstandard tillage might be explained by the release of the
712 Nematology
Effects of soil management on soil food webs
nematodes from the roots as a result of tillage (Lenz ampEisenbeis 2000)
Ammonium MBC C K P and ergosterol were pos-itively related with total number of nematodes and theEI The EI is based on the weighted abundance of bacte-rial feeding nematodes enrichment-opportunistic relativeto longer life cycle bacterial-feeders indicating highlyactive bacterial-mediated decomposition channels Whenthe field is organically enriched these nematodes exploitthe abundant resources (fungi and bacteria) and increaserapidly in abundance due to their short life cycles and highfecundity (Bongers 1990) On the contrary high valuesof the CI indicate slower fungal-mediated decompositionpathways so a significant relationship between CI and er-gosterol was expected but not found CI was positivelycorrelated with PLFA of fungal biomarkers and EI wasnegatively correlated with PLFA of bacterial markers butnot correlated with MBC Thus the relationship betweenPLFA and microbial grazers may reflect the strength of thegrazing pressure at the sampling time The prevalence ofopportunistic bacterial feeders over other microbial feed-ers (as expressed by the EI) may decrease bacterial bio-mass (indicated by PLFA of bacterial markers) more obvi-ously than the effect of fungal feeders on fungal biomassas indicated by the positive association between the CIindicator of the prevalence of fungal-feeding nematodesover bacterial feeders with fungal biomass (inferred fromPLFA of fungal markers) The absence of correlation be-tween MBC and nematode populations may thus indicatethat the grazing pressure affects only certain microbes andnot the total microbial community
CI and BI were strongly correlated and associatedwith deeper soil layers and no tillage across all samplingdates High BI values indicate a nematode assemblagecomposed of perturbation-resistant nematodes mainly oflower trophic levels The community structure was in thiscase associated with fungal-dominated organic matterdecomposition pathways The SI was associated withdeeper soil layers and intermittent fallow suggesting anegative relationship between predator abundance and thehigh physical disturbance and biological activity presentat the soil surface and in the continuous cropping plots
Conclusions
Different tillage practices and cropping systems deter-mine soil properties and thus nematode abundance Theseeffects vary with nematode trophic and functional group
By the end of the experiment each treatment supporteddifferent nematode assemblages and soil food webs
Each soil food web index describes a model nema-tode assemblage (Ferris et al 2001) Our four treat-ments structured four different nematode assemblagesThe combination of standard tillage and continuous crop-ping (STCC) was associated with high EI values reflect-ing an assemblage predominantly composed of bacterial-feeding nematodes with short life cycles This enrichedassemblage was especially characteristic of the upper soillayer Perhaps not surprisingly for a long-disturbed agri-cultural system we did not find the relationships we ex-pected between continuous cropping and the abundanceof predator and omnivore nematodes The organisms inthe higher levels of the soil food web did not respond tothe continuous input of C in the soil and a long recoveryperiod may be required for appropriate taxa to be rein-troduced and to increase Intermittent fallow (especiallySTF) supported a longer more structured soil food web(high SI values) especially in the deeper soil layers Thecombination of no tillage and intermittent fallow (NTF)supported a fungal-based community with slower organicmatter decomposition rates especially below the upper 5cm of soil The accumulation of plant residues on the soilsurface may result in slower incorporation of C into thefood web and exploitation by fungi Indeed the absenceof tillage and thus of physical perturbation would not dis-rupt fungal hyphae Finally the combination of no tillageand continuous cropping (NTCC) supported a less well-defined assemblage dominated by basal perturbation-resistant nematodes
Acknowledgements
This research was supported by California Bay DeltaAuthority (CBDA)-Ecosystem Restoration Program grant ERP-02-P36 by the California Department of Food andAgricultureKearney Foundation of Soil Science Projects2003011 and by the Kearney Foundation of Soil ScienceProject 2005210 We thank the LTRAS staff for fieldmanagement Many thanks to members of the Jackson andTemple lab groups for help with sampling and Dr S Goyalfor guidance with the HPLC
References
ADEDIRAN JA ADEGBITE AA AKINLOSOTU TAAGBAJE GO TAIWO LB OWOLADE OF amp
Vol 8(5) 2006 713
S Saacutenchez-Moreno et al
OLUWATOSIN GA (2005) Evaluation of fallow and covercrops for nematode suppression in three agroecologies ofsouth western Nigeria African Journal of Biotechnology 41034-1039
BERKELMANS R FERRIS H TENUTA M amp VAN
BRUGGEN AHC (2003) Effects of long-term crop man-agement on nematode trophic levels other than plant feedersdisappear after 1 year of disruptive soil management AppliedSoil Ecology 23 223-235
BONGERS T (1990) The maturity index an ecological mea-sure of environmental disturbance based on nematode speciescomposition Oecologia 83 14-19
BONGERS T amp BONGERS M (1998) Functional diversity ofnematodes Applied Soil Ecology 10 239-251
BOSSIO DA SCOW KM GUNAPALA N amp GRAHAMKJ (1998) Determinants soil microbial communities ef-fects of agricultural management season and soil type onphospholipids fatty acid profiles Microbial Ecology 36 1-12
BOUWMAN LA BLOEM J VAN DEN BOOGERT PHJFBREMER F HOENDERBOOM GHJ amp DE RUITER PC(1994) Short-term and long-term effects of bacterivorousnematodes and nematophagous fungi on carbon and nitrogenmineralization in microcosms Biology and Fertility of Soils17 249-256
BULLUCK III LR BARKER KR amp RISTAINO JB (2002)Influences of organic and synthetic soil fertility amendmentson nematode trophic groups and community dynamics undertomatoes Applied Soil Ecology 21 233-250
CADET P PATEacute E amp NrsquoDIAYE-FAYE N (2003) Nematodecommunity changes and survival rates under natural fallow inthe sudano sahelian area of Senegal Pedobiologia 47 149-160
CHAN KY (2001) An overview of some tillage impacts onearthworm population abundance and diversity ndash implicationsfor functioning in soils Soil and Tillage Research 57 179-191
DE MESEL I DERYCKE S MOENS T VAN DER GUCHTK VINCX M amp SWINGS J (2004) Top-down impactof bacteriovorous nematodes on the bacterial communitystructure a microcosm study Environmental Microbiology 6733-744
EKSCHMITT E STIERHOF T DAUBER J KREIMES Kamp WOLTERS V (2003) On the quality of soil biodiversityindicators abiotic parameters as predictor of soil faunalrichness at different spatial scales Agriculture Ecosystemsand Environment 98 273-283
ETTEMA CH (1998) Soil nematode diversity species coex-istence and ecosystem function Journal of Nematology 30159-169
FERRIS H VENETTE RC amp LAU SS (1997) Populationenergetics of bacterial-feeding nematodes Carbon and nitro-gen budgets Soil Biology and Biochemistry 29 1183-1194
FERRIS H BONGERS T amp DE GOEDE RGM (2001) Aframework for soil food web diagnostics extension of the
nematode faunal analysis concept Applied Soil Ecology 1813-29
FERRIS H VENETTE RC amp SCOW KM (2004) Soil man-agement to enhance bacteriovore and fungivore nematodepopulations and their nitrogen mineralization function Ap-plied Soil Ecology 25 19-35
FISCUS DA amp NEHER DA (2002) Distinguishing sensi-tivity of free-leaving soil nematode genera to physical andchemical disturbances Ecological Applications 12 565-575
FU S FERRIS H BROWN D amp PLANT R (2005) Doespositive feedback effect of nematodes on the biomass andactivity of their bacteria prey vary with nematode speciesand population size Soil Biology and Biochemistry 37 1979-1987
GYEDU-ABABIO TK FURTENBERG JP BAIRD D ampVANREUSEL A (1999) Nematodes as indicators of pollu-tion a case study from the Swartkops river system SouthAfrica Hydrobiologia 397 155-169
HAacuteNEL L (2003) Recovery of soil nematode populations fromcropping stress by natural secondary succession to meadowland Applied Soil Ecology 22 255-270
KLADIVCO EJ (2001) Tillage systems and soil ecology Soiland Tillage Research 61 61-76
KORTHALS GW VAN DE ENDE A VAN MEGEN HLEXMOND THM KAMMENGA JE amp BONGERS T(1996) Short-term effects of cadmium copper nickel andzinc on soil nematodes from different feeding and life-historystrategy groups Applied Soil Ecology 4 107-117
LENZ R amp EISENBEIS G (2000) Short-term effects ofdifferent tillage in a sustainable farming system on nematodecommunity structure Biology and Fertility of Soils 31 237-244
LIPHADZI KB AL-KHATIB K BENSCH C STAHLMANPW DILLE JA TODD T RICE CW HORAK MJamp HEAD G (2005) Soil microbial and nematode commu-nities as affected by glyphosate and tillage practices in aglyphosate-resistant cropping system Weed Science 53 536-545
MIKOLA J amp SETAumlLAuml H (1998a) No evidence of trophiccascades in an experimental microbial-based soil food webEcology 79 153-164
MIKOLA J amp SETAumlLAuml H (1998b) Relating species diversityto ecosystem functioning mechanistic backgrounds and ex-perimental approach with a decomposer food web Oikos 83180-194
MINOSHIMA H JACKSON LE CAVAGNARO TRSAacuteNCHEZ-MORENO S FERRIS H TEMPLE S ampMITCHELL J (2006) Soil food webs and carbon dynam-ics in response to conservation tillage in legume rotations inCalifornia Soil Science Society of America in press
MULDER C DE ZWART D VAN WIJNEN HJSCHOUTEN AJ amp BREURE AM (2003) Observa-tional and simulated evidence of ecological shifts withinthe soil nematode community of agroecosystems under
714 Nematology
Effects of soil management on soil food webs
conventional and organic farming Functional Ecology 17516-525
MULDER C SCHOUTEN AJ HUND-RINKE K ampBREURE AM (2005) The use of nematodes in ecologi-cal soil classification and assessment concepts Ecotoxicologyand Environmental Safety 62 278-289
NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
PORAZINSKA DL DUNCAN LW MCSORLEY R ampGRAHAM JH (1999) Nematode communities as indicatorsof status and processes of a soil ecosystems influenced byagricultural management practices Applied Soil Ecology 1369-86
POSTMA-BLAAUW MB DE VRIES FT DE GOEDERGM BLOEM J FABER JH amp BRUSSAARD L(2005) Within-trophic group interactions of bacterivorousnematode species and their effects on the bacterial commu-nity and nitrogen mineralization Oecologia 142 428-439
ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
SALOMON J ALPHEI J RUF A SCHAEFER M SCHEUS SCHNEIDER K SUumlHRIG A amp MARAUN M (2006)Transitory dynamic effects in the soil invertebrate communityin a temperate deciduous forest Effects of resource qualitySoil Biology and Biochemistry 38 209-221
SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
STATSOFT INC (1996) STATISTICA for Windows (ComputerProgram Manual) Tulsa OK USA
THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
YAMADA M (2001) Methods of control injury associatedwith continuous vegetable cropping in Japan ndash Crop rotationand several cultural practices Japan Agricultural ResearchQuarterly 35 39-45
YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
YEATES GW BONGERS T DE GOEDE RGM FRECK-MAN DW amp GEORGIEVA SS (1993) Feeding-habits insoil nematode families and genera ndash an outline for soil ecolo-gists Journal of Nematology 25 315-331
Vol 8(5) 2006 715
Effects of soil management on soil food webs
Table 4 Average values (plusmn SE) of soil properties in the four different treatments across three depths Significant effects of treatments(NTCC STCC STF NTF) crop pattern (CC and F) and tillage (ST and NT) are indicated by level of significance Data are from thelast sampling date (December 2004 n = 36) Data from Minoshima et al (2006)
NTF STF NTCC STCC Treatment Crop Tillage
Total C () 106 plusmn 003 099 plusmn 001 107 plusmn 004 103 plusmn 002 P lt 005Total N () 012 plusmn 000 011 plusmn 000 012 plusmn 000 012 plusmn 000 P lt 005pH 707 plusmn 003 686 plusmn 003 708 plusmn 006 690 plusmn 004 P lt 001 P lt 0001K (mg lminus1) 700 plusmn 049 591 plusmn 013 786 plusmn 132 734 plusmn 080P (microg gminus1) 1738 plusmn 088 1578 plusmn 031 1908 plusmn 217 1598 plusmn 083NO3 454 plusmn 106 550 plusmn 148 646 plusmn 092 1203 plusmn 253 P lt 005 P lt 005
(microg N gminus1)
NH4 236 plusmn 131 127 plusmn 054 116 plusmn 027 106 plusmn 016(microg N gminus1)
MBC 17123 plusmn 2623 14816 plusmn 1905 26275 plusmn 6398 17158 plusmn 1823(microg C gminus1)
Ergosterol 99932 plusmn 16846 57594 plusmn 3631 224691 plusmn 82975 121820 plusmn 25685 P lt 005(ng gminus1)
Bulk density 134 plusmn 002 125 plusmn 003 132 plusmn 002 125 plusmn 002 P lt 005 P lt 001(gcm3)
PLFAba 190753 plusmn 50529 144540 plusmn 35185 230127 plusmn 55833 208676 plusmn 31240(mgm2)
PLFAfu 24662 plusmn 12047 14295 plusmn 4381 55785 plusmn 26261 27208 plusmn 7651(mgm2)
bacterial-feeder nematodes after the first tillage treatmentOur results indicate that the response of total nematodeabundance to management depends on the assemblagecomposition so no general patterns can be discerned with-out analysing separately the taxa and functional group re-sponses For example Liphadzi et al (2005) found gen-eral increase in nematode abundance in tilled plots due tothe predominance of fungal feeders and bacterial feeders(up to 90) in the assemblages they studied
Throughout the four sampling dates of this study mostof the microbial feeders (Panagrolaimus RhabditidaeAphelenchus and Acrobeloides) were positively associ-ated with standard tillage indicating the stimulatory effecton microbes of incorporating organic matter into the soilThe nematodes less responsive to incorporated organicmatter were the higher cp taxa (Tylenchorhynchus Tylen-cholaimus Pratylenchus and some Dorylaimidae) whichwere associated with no-tillage Even though a greaternumber of taxa (especially of upper trophic levels) andhigher resolution identification would be desirable to in-fer relationships more reliably (Yeates 2003 Mulder etal 2005) we observed significant relationships betweensensitivity to tillage and trophic or cp groups as similarlyreported by Fiscus and Neher (2002)
Plectus was the only bacterivore associated with thesoil properties of the NT treatments suggesting a highersensitivity to tillage practices While Fiscus and Neher(2002) suggested that Plectus is an indicator of distur-bance due to the concordance between its cp value (2)and its tolerance to chemical and mechanical perturba-tions we found it to be more sensitive to tillage than ex-pected from its cp value Different responses among ge-nera in the same trophic group are common (Porazinska etal 1999) and nematode genera within the same trophicgroup can exhibit asymmetric competition negatively in-fluencing the abundance of other genera (Postma-Blaaw etal 2005) so responses to perturbation may be influencedby the presence of other nematode taxa Greater taxo-nomic resolution may be necessary to resolve differencesin response to environmental variables among nematodeswithin higher taxonomic groupings (Yeates 2003) espe-cially for taxa that have numerous species and a broad sizerange (eg Plectus)
Bacterial feeders are usually abundant in cultivatedsoils while predators and omnivores often disappear withcultivation (Wardle et al 1995) Microbivorous nema-todes belonging to the cp 1 group (eg Panagrolaimusor Rhabditidae enrichment-opportunistic nematodes) andthose with longer life cycles in the cp 2 group (eg Aphe-
Vol 8(5) 2006 709
S Saacutenchez-Moreno et al
Fig 2 Canonical correspondence analysis bi-plot of effects of tillage system crop pattern and depth on nematode abundances andsoil food web indices Environmental variables are marked by arrows Aphel Aphelenchus Tyl Tylenchidae Acro Acrobeloides PanPanagrolaimus Rhab Rhabditidae Tylen Tylenchorhynchus Dor Dorylaimidae SDor Small Dorylaimidae Plec Plectus PratPratylenchus Tylo Tylencholaimus N Total number of nematodes S Taxa richness EI Enrichment index SI Structure index BIBasal index CI Channel index Eigenvalues were 0568 and 0362 for the first and the second root respectively Percentage of varianceexplained was 330 for both root 1 and root 2
lenchus and Acrobeloides) were also associated with con-tinuous cropping The combined effect of standard tillageand continuous cropping significantly enhanced the abun-dance of nematodes at the entry level of the soil foodweb Bacterial-feeding nematodes influence C- and N-
mineralisation by feeding on bacteria excreting NH+4 and
by spreading bacteria through the soil (Bouwman et al1994 Fu et al 2005) Mesorhabditis and Acrobeloidestwo of the most abundant bacterial-feeders in our plotswere positively associated with NH+
4 a reasonable expec-
Fig 3 Scatter plot of CCA ordination showing relationships between soil properties and nematode taxa abundance (a) and soil foodweb indices taxa richness and total number of nematodes (b) Acro Acrobeles Acrob Acrobeloides Aphel Aphelenchus AphoAphelenchoides Aporce Aporcelaimidae Diph Diphtherophora Disco Discolaimus Dity Ditylenchus Meso Mesorhabditis MylMylonchulus Pan Panagrolaimus Plec Plectus Prat Pratylenchus Prion Prionchulus Qudsi Qusianematidae Tyl TylenchidaeTylen Tylenchorhynchus Eigenvalues were 097 and 096 (a) and 080 and 058 (b) for roots 1 and 2 respectively Percentages ofexplained variance for roots 1 and 2 were 107 and 110 (a) and 114 and 64 (b) respectively
710 Nematology
Effects of soil management on soil food webs
Vol 8(5) 2006 711
S Saacutenchez-Moreno et al
tation for the group associated with increased N mineral-isation (Ferris et al 1997 2004) By contrast Panagro-laimus and Plectus ordered in an opposite position due totheir negative relationship with PLFA biomarkers of fungiand bacteria and with bulk density Panagrolaimus has ahigh metabolic rate and a broad non-selective microbialfeeding habit (De Mesel et al 2004) It may decreasebacterial populations (as indicated by lower PFLA frombacterial markers) to a greater extent than other bacter-ial feeders in our plots When microbivorous nematodespredominate in soils they enhance N mineralisation andthus the availability of N for plants (Ferris et al 2004)Total soil N may be correlated with abundance of certainnematodes (Nakamoto et al 2006) but potentially min-eralisable N is a better indicator of N availability Thatmight explain why total soil N was associated only withabundance of Tylenchidae in this study Total C on thecontrary was more strongly associated with total nema-tode abundance
Surprisingly the abundance of fungal-feeding nema-todes such as Aphelenchus and some Tylenchidae was notrelated as strongly with ergosterol as expected suggest-ing that fungal biomass may not determining the size offungal feeder populations Villenave et al (2004) founddiffering responses of fungal feeders to ergosterol contentfungal feeders in cp groups 2 and 4 were positively relatedwith ergosterol but fungal feeders in the cp 5 group werenot
The discrimination between responses of nematodesin the higher and the lower levels of the soil food webwas evident in the CCA ordination revealing a link be-tween lower trophic levels and MBC NH+
4 ergosteroltotal N total C and certain PLFA Bacterial- fungal-and plant-feeding taxa with low cp values ordered op-posite to predatory and omnivore nematodes such asPrionchulus Qudsianematidae Aporcelaimidae Disco-laimus and Mylonchulus With the only exceptions ofthe plant-feeder Tylenchorhynchus (cp 3) which orderedclose to Mesorhabditis (cp 1) and Acrobeles (cp 2) whichscored close to the predators (cp 4 5) nematodes belong-ing to cp groups 1 and 2 showed an opposite response toenvironmental variables than those in cp groups 3 4 and 5
Predatory and omnivore nematodes are in higher co-loniser-persistent groups (3) and are more sensitive tosoil perturbation Intermittent fallow and standard tillagesupported higher abundances of most of the predators andomnivores Mylonchulus Qudsianematidae Prionchulusand Aporcelaimidae It is generally accepted that nema-tode functional diversity decreases with increasing man-
Table 5 Summarized effects of treatments on nematode trophicgroups (Ba = bacterial-feeders Fu = fungal-feeders Pp =plant-feeders PO = predators and omnivores)
Standard tillage No-tillage
Fallow Small increase of Ba Decrease of BaSmall decrease of Fu Decrease of FuDecrease of Pp Small decrease of PpIncrease of PO Increase of POIncrease of SI values Increase of CI values
Continuous Increase of Ba Small decrease of Bacropping Small increase of Fu Increase of Fu
Increase of Pp Increase of PpDecrease of PO Decrease of POIncrease of EI values Increase of BI values
agement intensity (Mulder et al 2003) predatory nema-todes were in our case much more affected by the crop-ping pattern (being enhanced in the intermittent fallowtreatment) than by standard tillage Our results thus sug-gest that even though predatory nematodes are sensitive tosoil physical perturbation other soil forces can drive theirabundance In some studies 25 years of tillage did notstrongly affect predators but reduced fungal-feeder nema-todes (Wang et al 2004)
An increase in predator and omnivore nematodes wasexpected in CC treatments as a result of the continuousincorporation of C into the soil but was not found (Ta-ble 5) Minoshima et al (2006) found that nematodesin the higher trophic levels were not significantly asso-ciated with the C pools in the soil Previous studies foundomnivore and predatory nematodes much more abundantin recently abandoned fallow fields than in cultivated orseminatural meadow lands (Haacutenel 2003) Polis et al(2000) suggest that trophic cascades produced by com-plex trophic interactions are abundant in soil systemsbut bottom-up regulation is difficult to demonstrate insoil trophic levels due to the high complexity of the soilbiota interactions In forest soils Salomon et al (2006)found more abundant microbial grazers when abundantresources were added to the soil but the effects did notextend into higher trophic levels of the soil food webleading to the conclusion that the availability of resourcesplays a minor role structuring soil food webs
Responses of plant-parasites and root feeders to tillageare usually difficult to interpret and are more closely re-lated to plant status and phenology than to soil propertiesThe association between Pratylenchus (endoparasite) andstandard tillage might be explained by the release of the
712 Nematology
Effects of soil management on soil food webs
nematodes from the roots as a result of tillage (Lenz ampEisenbeis 2000)
Ammonium MBC C K P and ergosterol were pos-itively related with total number of nematodes and theEI The EI is based on the weighted abundance of bacte-rial feeding nematodes enrichment-opportunistic relativeto longer life cycle bacterial-feeders indicating highlyactive bacterial-mediated decomposition channels Whenthe field is organically enriched these nematodes exploitthe abundant resources (fungi and bacteria) and increaserapidly in abundance due to their short life cycles and highfecundity (Bongers 1990) On the contrary high valuesof the CI indicate slower fungal-mediated decompositionpathways so a significant relationship between CI and er-gosterol was expected but not found CI was positivelycorrelated with PLFA of fungal biomarkers and EI wasnegatively correlated with PLFA of bacterial markers butnot correlated with MBC Thus the relationship betweenPLFA and microbial grazers may reflect the strength of thegrazing pressure at the sampling time The prevalence ofopportunistic bacterial feeders over other microbial feed-ers (as expressed by the EI) may decrease bacterial bio-mass (indicated by PLFA of bacterial markers) more obvi-ously than the effect of fungal feeders on fungal biomassas indicated by the positive association between the CIindicator of the prevalence of fungal-feeding nematodesover bacterial feeders with fungal biomass (inferred fromPLFA of fungal markers) The absence of correlation be-tween MBC and nematode populations may thus indicatethat the grazing pressure affects only certain microbes andnot the total microbial community
CI and BI were strongly correlated and associatedwith deeper soil layers and no tillage across all samplingdates High BI values indicate a nematode assemblagecomposed of perturbation-resistant nematodes mainly oflower trophic levels The community structure was in thiscase associated with fungal-dominated organic matterdecomposition pathways The SI was associated withdeeper soil layers and intermittent fallow suggesting anegative relationship between predator abundance and thehigh physical disturbance and biological activity presentat the soil surface and in the continuous cropping plots
Conclusions
Different tillage practices and cropping systems deter-mine soil properties and thus nematode abundance Theseeffects vary with nematode trophic and functional group
By the end of the experiment each treatment supporteddifferent nematode assemblages and soil food webs
Each soil food web index describes a model nema-tode assemblage (Ferris et al 2001) Our four treat-ments structured four different nematode assemblagesThe combination of standard tillage and continuous crop-ping (STCC) was associated with high EI values reflect-ing an assemblage predominantly composed of bacterial-feeding nematodes with short life cycles This enrichedassemblage was especially characteristic of the upper soillayer Perhaps not surprisingly for a long-disturbed agri-cultural system we did not find the relationships we ex-pected between continuous cropping and the abundanceof predator and omnivore nematodes The organisms inthe higher levels of the soil food web did not respond tothe continuous input of C in the soil and a long recoveryperiod may be required for appropriate taxa to be rein-troduced and to increase Intermittent fallow (especiallySTF) supported a longer more structured soil food web(high SI values) especially in the deeper soil layers Thecombination of no tillage and intermittent fallow (NTF)supported a fungal-based community with slower organicmatter decomposition rates especially below the upper 5cm of soil The accumulation of plant residues on the soilsurface may result in slower incorporation of C into thefood web and exploitation by fungi Indeed the absenceof tillage and thus of physical perturbation would not dis-rupt fungal hyphae Finally the combination of no tillageand continuous cropping (NTCC) supported a less well-defined assemblage dominated by basal perturbation-resistant nematodes
Acknowledgements
This research was supported by California Bay DeltaAuthority (CBDA)-Ecosystem Restoration Program grant ERP-02-P36 by the California Department of Food andAgricultureKearney Foundation of Soil Science Projects2003011 and by the Kearney Foundation of Soil ScienceProject 2005210 We thank the LTRAS staff for fieldmanagement Many thanks to members of the Jackson andTemple lab groups for help with sampling and Dr S Goyalfor guidance with the HPLC
References
ADEDIRAN JA ADEGBITE AA AKINLOSOTU TAAGBAJE GO TAIWO LB OWOLADE OF amp
Vol 8(5) 2006 713
S Saacutenchez-Moreno et al
OLUWATOSIN GA (2005) Evaluation of fallow and covercrops for nematode suppression in three agroecologies ofsouth western Nigeria African Journal of Biotechnology 41034-1039
BERKELMANS R FERRIS H TENUTA M amp VAN
BRUGGEN AHC (2003) Effects of long-term crop man-agement on nematode trophic levels other than plant feedersdisappear after 1 year of disruptive soil management AppliedSoil Ecology 23 223-235
BONGERS T (1990) The maturity index an ecological mea-sure of environmental disturbance based on nematode speciescomposition Oecologia 83 14-19
BONGERS T amp BONGERS M (1998) Functional diversity ofnematodes Applied Soil Ecology 10 239-251
BOSSIO DA SCOW KM GUNAPALA N amp GRAHAMKJ (1998) Determinants soil microbial communities ef-fects of agricultural management season and soil type onphospholipids fatty acid profiles Microbial Ecology 36 1-12
BOUWMAN LA BLOEM J VAN DEN BOOGERT PHJFBREMER F HOENDERBOOM GHJ amp DE RUITER PC(1994) Short-term and long-term effects of bacterivorousnematodes and nematophagous fungi on carbon and nitrogenmineralization in microcosms Biology and Fertility of Soils17 249-256
BULLUCK III LR BARKER KR amp RISTAINO JB (2002)Influences of organic and synthetic soil fertility amendmentson nematode trophic groups and community dynamics undertomatoes Applied Soil Ecology 21 233-250
CADET P PATEacute E amp NrsquoDIAYE-FAYE N (2003) Nematodecommunity changes and survival rates under natural fallow inthe sudano sahelian area of Senegal Pedobiologia 47 149-160
CHAN KY (2001) An overview of some tillage impacts onearthworm population abundance and diversity ndash implicationsfor functioning in soils Soil and Tillage Research 57 179-191
DE MESEL I DERYCKE S MOENS T VAN DER GUCHTK VINCX M amp SWINGS J (2004) Top-down impactof bacteriovorous nematodes on the bacterial communitystructure a microcosm study Environmental Microbiology 6733-744
EKSCHMITT E STIERHOF T DAUBER J KREIMES Kamp WOLTERS V (2003) On the quality of soil biodiversityindicators abiotic parameters as predictor of soil faunalrichness at different spatial scales Agriculture Ecosystemsand Environment 98 273-283
ETTEMA CH (1998) Soil nematode diversity species coex-istence and ecosystem function Journal of Nematology 30159-169
FERRIS H VENETTE RC amp LAU SS (1997) Populationenergetics of bacterial-feeding nematodes Carbon and nitro-gen budgets Soil Biology and Biochemistry 29 1183-1194
FERRIS H BONGERS T amp DE GOEDE RGM (2001) Aframework for soil food web diagnostics extension of the
nematode faunal analysis concept Applied Soil Ecology 1813-29
FERRIS H VENETTE RC amp SCOW KM (2004) Soil man-agement to enhance bacteriovore and fungivore nematodepopulations and their nitrogen mineralization function Ap-plied Soil Ecology 25 19-35
FISCUS DA amp NEHER DA (2002) Distinguishing sensi-tivity of free-leaving soil nematode genera to physical andchemical disturbances Ecological Applications 12 565-575
FU S FERRIS H BROWN D amp PLANT R (2005) Doespositive feedback effect of nematodes on the biomass andactivity of their bacteria prey vary with nematode speciesand population size Soil Biology and Biochemistry 37 1979-1987
GYEDU-ABABIO TK FURTENBERG JP BAIRD D ampVANREUSEL A (1999) Nematodes as indicators of pollu-tion a case study from the Swartkops river system SouthAfrica Hydrobiologia 397 155-169
HAacuteNEL L (2003) Recovery of soil nematode populations fromcropping stress by natural secondary succession to meadowland Applied Soil Ecology 22 255-270
KLADIVCO EJ (2001) Tillage systems and soil ecology Soiland Tillage Research 61 61-76
KORTHALS GW VAN DE ENDE A VAN MEGEN HLEXMOND THM KAMMENGA JE amp BONGERS T(1996) Short-term effects of cadmium copper nickel andzinc on soil nematodes from different feeding and life-historystrategy groups Applied Soil Ecology 4 107-117
LENZ R amp EISENBEIS G (2000) Short-term effects ofdifferent tillage in a sustainable farming system on nematodecommunity structure Biology and Fertility of Soils 31 237-244
LIPHADZI KB AL-KHATIB K BENSCH C STAHLMANPW DILLE JA TODD T RICE CW HORAK MJamp HEAD G (2005) Soil microbial and nematode commu-nities as affected by glyphosate and tillage practices in aglyphosate-resistant cropping system Weed Science 53 536-545
MIKOLA J amp SETAumlLAuml H (1998a) No evidence of trophiccascades in an experimental microbial-based soil food webEcology 79 153-164
MIKOLA J amp SETAumlLAuml H (1998b) Relating species diversityto ecosystem functioning mechanistic backgrounds and ex-perimental approach with a decomposer food web Oikos 83180-194
MINOSHIMA H JACKSON LE CAVAGNARO TRSAacuteNCHEZ-MORENO S FERRIS H TEMPLE S ampMITCHELL J (2006) Soil food webs and carbon dynam-ics in response to conservation tillage in legume rotations inCalifornia Soil Science Society of America in press
MULDER C DE ZWART D VAN WIJNEN HJSCHOUTEN AJ amp BREURE AM (2003) Observa-tional and simulated evidence of ecological shifts withinthe soil nematode community of agroecosystems under
714 Nematology
Effects of soil management on soil food webs
conventional and organic farming Functional Ecology 17516-525
MULDER C SCHOUTEN AJ HUND-RINKE K ampBREURE AM (2005) The use of nematodes in ecologi-cal soil classification and assessment concepts Ecotoxicologyand Environmental Safety 62 278-289
NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
PORAZINSKA DL DUNCAN LW MCSORLEY R ampGRAHAM JH (1999) Nematode communities as indicatorsof status and processes of a soil ecosystems influenced byagricultural management practices Applied Soil Ecology 1369-86
POSTMA-BLAAUW MB DE VRIES FT DE GOEDERGM BLOEM J FABER JH amp BRUSSAARD L(2005) Within-trophic group interactions of bacterivorousnematode species and their effects on the bacterial commu-nity and nitrogen mineralization Oecologia 142 428-439
ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
SALOMON J ALPHEI J RUF A SCHAEFER M SCHEUS SCHNEIDER K SUumlHRIG A amp MARAUN M (2006)Transitory dynamic effects in the soil invertebrate communityin a temperate deciduous forest Effects of resource qualitySoil Biology and Biochemistry 38 209-221
SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
STATSOFT INC (1996) STATISTICA for Windows (ComputerProgram Manual) Tulsa OK USA
THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
YAMADA M (2001) Methods of control injury associatedwith continuous vegetable cropping in Japan ndash Crop rotationand several cultural practices Japan Agricultural ResearchQuarterly 35 39-45
YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
YEATES GW BONGERS T DE GOEDE RGM FRECK-MAN DW amp GEORGIEVA SS (1993) Feeding-habits insoil nematode families and genera ndash an outline for soil ecolo-gists Journal of Nematology 25 315-331
Vol 8(5) 2006 715
S Saacutenchez-Moreno et al
Fig 2 Canonical correspondence analysis bi-plot of effects of tillage system crop pattern and depth on nematode abundances andsoil food web indices Environmental variables are marked by arrows Aphel Aphelenchus Tyl Tylenchidae Acro Acrobeloides PanPanagrolaimus Rhab Rhabditidae Tylen Tylenchorhynchus Dor Dorylaimidae SDor Small Dorylaimidae Plec Plectus PratPratylenchus Tylo Tylencholaimus N Total number of nematodes S Taxa richness EI Enrichment index SI Structure index BIBasal index CI Channel index Eigenvalues were 0568 and 0362 for the first and the second root respectively Percentage of varianceexplained was 330 for both root 1 and root 2
lenchus and Acrobeloides) were also associated with con-tinuous cropping The combined effect of standard tillageand continuous cropping significantly enhanced the abun-dance of nematodes at the entry level of the soil foodweb Bacterial-feeding nematodes influence C- and N-
mineralisation by feeding on bacteria excreting NH+4 and
by spreading bacteria through the soil (Bouwman et al1994 Fu et al 2005) Mesorhabditis and Acrobeloidestwo of the most abundant bacterial-feeders in our plotswere positively associated with NH+
4 a reasonable expec-
Fig 3 Scatter plot of CCA ordination showing relationships between soil properties and nematode taxa abundance (a) and soil foodweb indices taxa richness and total number of nematodes (b) Acro Acrobeles Acrob Acrobeloides Aphel Aphelenchus AphoAphelenchoides Aporce Aporcelaimidae Diph Diphtherophora Disco Discolaimus Dity Ditylenchus Meso Mesorhabditis MylMylonchulus Pan Panagrolaimus Plec Plectus Prat Pratylenchus Prion Prionchulus Qudsi Qusianematidae Tyl TylenchidaeTylen Tylenchorhynchus Eigenvalues were 097 and 096 (a) and 080 and 058 (b) for roots 1 and 2 respectively Percentages ofexplained variance for roots 1 and 2 were 107 and 110 (a) and 114 and 64 (b) respectively
710 Nematology
Effects of soil management on soil food webs
Vol 8(5) 2006 711
S Saacutenchez-Moreno et al
tation for the group associated with increased N mineral-isation (Ferris et al 1997 2004) By contrast Panagro-laimus and Plectus ordered in an opposite position due totheir negative relationship with PLFA biomarkers of fungiand bacteria and with bulk density Panagrolaimus has ahigh metabolic rate and a broad non-selective microbialfeeding habit (De Mesel et al 2004) It may decreasebacterial populations (as indicated by lower PFLA frombacterial markers) to a greater extent than other bacter-ial feeders in our plots When microbivorous nematodespredominate in soils they enhance N mineralisation andthus the availability of N for plants (Ferris et al 2004)Total soil N may be correlated with abundance of certainnematodes (Nakamoto et al 2006) but potentially min-eralisable N is a better indicator of N availability Thatmight explain why total soil N was associated only withabundance of Tylenchidae in this study Total C on thecontrary was more strongly associated with total nema-tode abundance
Surprisingly the abundance of fungal-feeding nema-todes such as Aphelenchus and some Tylenchidae was notrelated as strongly with ergosterol as expected suggest-ing that fungal biomass may not determining the size offungal feeder populations Villenave et al (2004) founddiffering responses of fungal feeders to ergosterol contentfungal feeders in cp groups 2 and 4 were positively relatedwith ergosterol but fungal feeders in the cp 5 group werenot
The discrimination between responses of nematodesin the higher and the lower levels of the soil food webwas evident in the CCA ordination revealing a link be-tween lower trophic levels and MBC NH+
4 ergosteroltotal N total C and certain PLFA Bacterial- fungal-and plant-feeding taxa with low cp values ordered op-posite to predatory and omnivore nematodes such asPrionchulus Qudsianematidae Aporcelaimidae Disco-laimus and Mylonchulus With the only exceptions ofthe plant-feeder Tylenchorhynchus (cp 3) which orderedclose to Mesorhabditis (cp 1) and Acrobeles (cp 2) whichscored close to the predators (cp 4 5) nematodes belong-ing to cp groups 1 and 2 showed an opposite response toenvironmental variables than those in cp groups 3 4 and 5
Predatory and omnivore nematodes are in higher co-loniser-persistent groups (3) and are more sensitive tosoil perturbation Intermittent fallow and standard tillagesupported higher abundances of most of the predators andomnivores Mylonchulus Qudsianematidae Prionchulusand Aporcelaimidae It is generally accepted that nema-tode functional diversity decreases with increasing man-
Table 5 Summarized effects of treatments on nematode trophicgroups (Ba = bacterial-feeders Fu = fungal-feeders Pp =plant-feeders PO = predators and omnivores)
Standard tillage No-tillage
Fallow Small increase of Ba Decrease of BaSmall decrease of Fu Decrease of FuDecrease of Pp Small decrease of PpIncrease of PO Increase of POIncrease of SI values Increase of CI values
Continuous Increase of Ba Small decrease of Bacropping Small increase of Fu Increase of Fu
Increase of Pp Increase of PpDecrease of PO Decrease of POIncrease of EI values Increase of BI values
agement intensity (Mulder et al 2003) predatory nema-todes were in our case much more affected by the crop-ping pattern (being enhanced in the intermittent fallowtreatment) than by standard tillage Our results thus sug-gest that even though predatory nematodes are sensitive tosoil physical perturbation other soil forces can drive theirabundance In some studies 25 years of tillage did notstrongly affect predators but reduced fungal-feeder nema-todes (Wang et al 2004)
An increase in predator and omnivore nematodes wasexpected in CC treatments as a result of the continuousincorporation of C into the soil but was not found (Ta-ble 5) Minoshima et al (2006) found that nematodesin the higher trophic levels were not significantly asso-ciated with the C pools in the soil Previous studies foundomnivore and predatory nematodes much more abundantin recently abandoned fallow fields than in cultivated orseminatural meadow lands (Haacutenel 2003) Polis et al(2000) suggest that trophic cascades produced by com-plex trophic interactions are abundant in soil systemsbut bottom-up regulation is difficult to demonstrate insoil trophic levels due to the high complexity of the soilbiota interactions In forest soils Salomon et al (2006)found more abundant microbial grazers when abundantresources were added to the soil but the effects did notextend into higher trophic levels of the soil food webleading to the conclusion that the availability of resourcesplays a minor role structuring soil food webs
Responses of plant-parasites and root feeders to tillageare usually difficult to interpret and are more closely re-lated to plant status and phenology than to soil propertiesThe association between Pratylenchus (endoparasite) andstandard tillage might be explained by the release of the
712 Nematology
Effects of soil management on soil food webs
nematodes from the roots as a result of tillage (Lenz ampEisenbeis 2000)
Ammonium MBC C K P and ergosterol were pos-itively related with total number of nematodes and theEI The EI is based on the weighted abundance of bacte-rial feeding nematodes enrichment-opportunistic relativeto longer life cycle bacterial-feeders indicating highlyactive bacterial-mediated decomposition channels Whenthe field is organically enriched these nematodes exploitthe abundant resources (fungi and bacteria) and increaserapidly in abundance due to their short life cycles and highfecundity (Bongers 1990) On the contrary high valuesof the CI indicate slower fungal-mediated decompositionpathways so a significant relationship between CI and er-gosterol was expected but not found CI was positivelycorrelated with PLFA of fungal biomarkers and EI wasnegatively correlated with PLFA of bacterial markers butnot correlated with MBC Thus the relationship betweenPLFA and microbial grazers may reflect the strength of thegrazing pressure at the sampling time The prevalence ofopportunistic bacterial feeders over other microbial feed-ers (as expressed by the EI) may decrease bacterial bio-mass (indicated by PLFA of bacterial markers) more obvi-ously than the effect of fungal feeders on fungal biomassas indicated by the positive association between the CIindicator of the prevalence of fungal-feeding nematodesover bacterial feeders with fungal biomass (inferred fromPLFA of fungal markers) The absence of correlation be-tween MBC and nematode populations may thus indicatethat the grazing pressure affects only certain microbes andnot the total microbial community
CI and BI were strongly correlated and associatedwith deeper soil layers and no tillage across all samplingdates High BI values indicate a nematode assemblagecomposed of perturbation-resistant nematodes mainly oflower trophic levels The community structure was in thiscase associated with fungal-dominated organic matterdecomposition pathways The SI was associated withdeeper soil layers and intermittent fallow suggesting anegative relationship between predator abundance and thehigh physical disturbance and biological activity presentat the soil surface and in the continuous cropping plots
Conclusions
Different tillage practices and cropping systems deter-mine soil properties and thus nematode abundance Theseeffects vary with nematode trophic and functional group
By the end of the experiment each treatment supporteddifferent nematode assemblages and soil food webs
Each soil food web index describes a model nema-tode assemblage (Ferris et al 2001) Our four treat-ments structured four different nematode assemblagesThe combination of standard tillage and continuous crop-ping (STCC) was associated with high EI values reflect-ing an assemblage predominantly composed of bacterial-feeding nematodes with short life cycles This enrichedassemblage was especially characteristic of the upper soillayer Perhaps not surprisingly for a long-disturbed agri-cultural system we did not find the relationships we ex-pected between continuous cropping and the abundanceof predator and omnivore nematodes The organisms inthe higher levels of the soil food web did not respond tothe continuous input of C in the soil and a long recoveryperiod may be required for appropriate taxa to be rein-troduced and to increase Intermittent fallow (especiallySTF) supported a longer more structured soil food web(high SI values) especially in the deeper soil layers Thecombination of no tillage and intermittent fallow (NTF)supported a fungal-based community with slower organicmatter decomposition rates especially below the upper 5cm of soil The accumulation of plant residues on the soilsurface may result in slower incorporation of C into thefood web and exploitation by fungi Indeed the absenceof tillage and thus of physical perturbation would not dis-rupt fungal hyphae Finally the combination of no tillageand continuous cropping (NTCC) supported a less well-defined assemblage dominated by basal perturbation-resistant nematodes
Acknowledgements
This research was supported by California Bay DeltaAuthority (CBDA)-Ecosystem Restoration Program grant ERP-02-P36 by the California Department of Food andAgricultureKearney Foundation of Soil Science Projects2003011 and by the Kearney Foundation of Soil ScienceProject 2005210 We thank the LTRAS staff for fieldmanagement Many thanks to members of the Jackson andTemple lab groups for help with sampling and Dr S Goyalfor guidance with the HPLC
References
ADEDIRAN JA ADEGBITE AA AKINLOSOTU TAAGBAJE GO TAIWO LB OWOLADE OF amp
Vol 8(5) 2006 713
S Saacutenchez-Moreno et al
OLUWATOSIN GA (2005) Evaluation of fallow and covercrops for nematode suppression in three agroecologies ofsouth western Nigeria African Journal of Biotechnology 41034-1039
BERKELMANS R FERRIS H TENUTA M amp VAN
BRUGGEN AHC (2003) Effects of long-term crop man-agement on nematode trophic levels other than plant feedersdisappear after 1 year of disruptive soil management AppliedSoil Ecology 23 223-235
BONGERS T (1990) The maturity index an ecological mea-sure of environmental disturbance based on nematode speciescomposition Oecologia 83 14-19
BONGERS T amp BONGERS M (1998) Functional diversity ofnematodes Applied Soil Ecology 10 239-251
BOSSIO DA SCOW KM GUNAPALA N amp GRAHAMKJ (1998) Determinants soil microbial communities ef-fects of agricultural management season and soil type onphospholipids fatty acid profiles Microbial Ecology 36 1-12
BOUWMAN LA BLOEM J VAN DEN BOOGERT PHJFBREMER F HOENDERBOOM GHJ amp DE RUITER PC(1994) Short-term and long-term effects of bacterivorousnematodes and nematophagous fungi on carbon and nitrogenmineralization in microcosms Biology and Fertility of Soils17 249-256
BULLUCK III LR BARKER KR amp RISTAINO JB (2002)Influences of organic and synthetic soil fertility amendmentson nematode trophic groups and community dynamics undertomatoes Applied Soil Ecology 21 233-250
CADET P PATEacute E amp NrsquoDIAYE-FAYE N (2003) Nematodecommunity changes and survival rates under natural fallow inthe sudano sahelian area of Senegal Pedobiologia 47 149-160
CHAN KY (2001) An overview of some tillage impacts onearthworm population abundance and diversity ndash implicationsfor functioning in soils Soil and Tillage Research 57 179-191
DE MESEL I DERYCKE S MOENS T VAN DER GUCHTK VINCX M amp SWINGS J (2004) Top-down impactof bacteriovorous nematodes on the bacterial communitystructure a microcosm study Environmental Microbiology 6733-744
EKSCHMITT E STIERHOF T DAUBER J KREIMES Kamp WOLTERS V (2003) On the quality of soil biodiversityindicators abiotic parameters as predictor of soil faunalrichness at different spatial scales Agriculture Ecosystemsand Environment 98 273-283
ETTEMA CH (1998) Soil nematode diversity species coex-istence and ecosystem function Journal of Nematology 30159-169
FERRIS H VENETTE RC amp LAU SS (1997) Populationenergetics of bacterial-feeding nematodes Carbon and nitro-gen budgets Soil Biology and Biochemistry 29 1183-1194
FERRIS H BONGERS T amp DE GOEDE RGM (2001) Aframework for soil food web diagnostics extension of the
nematode faunal analysis concept Applied Soil Ecology 1813-29
FERRIS H VENETTE RC amp SCOW KM (2004) Soil man-agement to enhance bacteriovore and fungivore nematodepopulations and their nitrogen mineralization function Ap-plied Soil Ecology 25 19-35
FISCUS DA amp NEHER DA (2002) Distinguishing sensi-tivity of free-leaving soil nematode genera to physical andchemical disturbances Ecological Applications 12 565-575
FU S FERRIS H BROWN D amp PLANT R (2005) Doespositive feedback effect of nematodes on the biomass andactivity of their bacteria prey vary with nematode speciesand population size Soil Biology and Biochemistry 37 1979-1987
GYEDU-ABABIO TK FURTENBERG JP BAIRD D ampVANREUSEL A (1999) Nematodes as indicators of pollu-tion a case study from the Swartkops river system SouthAfrica Hydrobiologia 397 155-169
HAacuteNEL L (2003) Recovery of soil nematode populations fromcropping stress by natural secondary succession to meadowland Applied Soil Ecology 22 255-270
KLADIVCO EJ (2001) Tillage systems and soil ecology Soiland Tillage Research 61 61-76
KORTHALS GW VAN DE ENDE A VAN MEGEN HLEXMOND THM KAMMENGA JE amp BONGERS T(1996) Short-term effects of cadmium copper nickel andzinc on soil nematodes from different feeding and life-historystrategy groups Applied Soil Ecology 4 107-117
LENZ R amp EISENBEIS G (2000) Short-term effects ofdifferent tillage in a sustainable farming system on nematodecommunity structure Biology and Fertility of Soils 31 237-244
LIPHADZI KB AL-KHATIB K BENSCH C STAHLMANPW DILLE JA TODD T RICE CW HORAK MJamp HEAD G (2005) Soil microbial and nematode commu-nities as affected by glyphosate and tillage practices in aglyphosate-resistant cropping system Weed Science 53 536-545
MIKOLA J amp SETAumlLAuml H (1998a) No evidence of trophiccascades in an experimental microbial-based soil food webEcology 79 153-164
MIKOLA J amp SETAumlLAuml H (1998b) Relating species diversityto ecosystem functioning mechanistic backgrounds and ex-perimental approach with a decomposer food web Oikos 83180-194
MINOSHIMA H JACKSON LE CAVAGNARO TRSAacuteNCHEZ-MORENO S FERRIS H TEMPLE S ampMITCHELL J (2006) Soil food webs and carbon dynam-ics in response to conservation tillage in legume rotations inCalifornia Soil Science Society of America in press
MULDER C DE ZWART D VAN WIJNEN HJSCHOUTEN AJ amp BREURE AM (2003) Observa-tional and simulated evidence of ecological shifts withinthe soil nematode community of agroecosystems under
714 Nematology
Effects of soil management on soil food webs
conventional and organic farming Functional Ecology 17516-525
MULDER C SCHOUTEN AJ HUND-RINKE K ampBREURE AM (2005) The use of nematodes in ecologi-cal soil classification and assessment concepts Ecotoxicologyand Environmental Safety 62 278-289
NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
PORAZINSKA DL DUNCAN LW MCSORLEY R ampGRAHAM JH (1999) Nematode communities as indicatorsof status and processes of a soil ecosystems influenced byagricultural management practices Applied Soil Ecology 1369-86
POSTMA-BLAAUW MB DE VRIES FT DE GOEDERGM BLOEM J FABER JH amp BRUSSAARD L(2005) Within-trophic group interactions of bacterivorousnematode species and their effects on the bacterial commu-nity and nitrogen mineralization Oecologia 142 428-439
ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
SALOMON J ALPHEI J RUF A SCHAEFER M SCHEUS SCHNEIDER K SUumlHRIG A amp MARAUN M (2006)Transitory dynamic effects in the soil invertebrate communityin a temperate deciduous forest Effects of resource qualitySoil Biology and Biochemistry 38 209-221
SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
STATSOFT INC (1996) STATISTICA for Windows (ComputerProgram Manual) Tulsa OK USA
THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
YAMADA M (2001) Methods of control injury associatedwith continuous vegetable cropping in Japan ndash Crop rotationand several cultural practices Japan Agricultural ResearchQuarterly 35 39-45
YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
YEATES GW BONGERS T DE GOEDE RGM FRECK-MAN DW amp GEORGIEVA SS (1993) Feeding-habits insoil nematode families and genera ndash an outline for soil ecolo-gists Journal of Nematology 25 315-331
Vol 8(5) 2006 715
Effects of soil management on soil food webs
Vol 8(5) 2006 711
S Saacutenchez-Moreno et al
tation for the group associated with increased N mineral-isation (Ferris et al 1997 2004) By contrast Panagro-laimus and Plectus ordered in an opposite position due totheir negative relationship with PLFA biomarkers of fungiand bacteria and with bulk density Panagrolaimus has ahigh metabolic rate and a broad non-selective microbialfeeding habit (De Mesel et al 2004) It may decreasebacterial populations (as indicated by lower PFLA frombacterial markers) to a greater extent than other bacter-ial feeders in our plots When microbivorous nematodespredominate in soils they enhance N mineralisation andthus the availability of N for plants (Ferris et al 2004)Total soil N may be correlated with abundance of certainnematodes (Nakamoto et al 2006) but potentially min-eralisable N is a better indicator of N availability Thatmight explain why total soil N was associated only withabundance of Tylenchidae in this study Total C on thecontrary was more strongly associated with total nema-tode abundance
Surprisingly the abundance of fungal-feeding nema-todes such as Aphelenchus and some Tylenchidae was notrelated as strongly with ergosterol as expected suggest-ing that fungal biomass may not determining the size offungal feeder populations Villenave et al (2004) founddiffering responses of fungal feeders to ergosterol contentfungal feeders in cp groups 2 and 4 were positively relatedwith ergosterol but fungal feeders in the cp 5 group werenot
The discrimination between responses of nematodesin the higher and the lower levels of the soil food webwas evident in the CCA ordination revealing a link be-tween lower trophic levels and MBC NH+
4 ergosteroltotal N total C and certain PLFA Bacterial- fungal-and plant-feeding taxa with low cp values ordered op-posite to predatory and omnivore nematodes such asPrionchulus Qudsianematidae Aporcelaimidae Disco-laimus and Mylonchulus With the only exceptions ofthe plant-feeder Tylenchorhynchus (cp 3) which orderedclose to Mesorhabditis (cp 1) and Acrobeles (cp 2) whichscored close to the predators (cp 4 5) nematodes belong-ing to cp groups 1 and 2 showed an opposite response toenvironmental variables than those in cp groups 3 4 and 5
Predatory and omnivore nematodes are in higher co-loniser-persistent groups (3) and are more sensitive tosoil perturbation Intermittent fallow and standard tillagesupported higher abundances of most of the predators andomnivores Mylonchulus Qudsianematidae Prionchulusand Aporcelaimidae It is generally accepted that nema-tode functional diversity decreases with increasing man-
Table 5 Summarized effects of treatments on nematode trophicgroups (Ba = bacterial-feeders Fu = fungal-feeders Pp =plant-feeders PO = predators and omnivores)
Standard tillage No-tillage
Fallow Small increase of Ba Decrease of BaSmall decrease of Fu Decrease of FuDecrease of Pp Small decrease of PpIncrease of PO Increase of POIncrease of SI values Increase of CI values
Continuous Increase of Ba Small decrease of Bacropping Small increase of Fu Increase of Fu
Increase of Pp Increase of PpDecrease of PO Decrease of POIncrease of EI values Increase of BI values
agement intensity (Mulder et al 2003) predatory nema-todes were in our case much more affected by the crop-ping pattern (being enhanced in the intermittent fallowtreatment) than by standard tillage Our results thus sug-gest that even though predatory nematodes are sensitive tosoil physical perturbation other soil forces can drive theirabundance In some studies 25 years of tillage did notstrongly affect predators but reduced fungal-feeder nema-todes (Wang et al 2004)
An increase in predator and omnivore nematodes wasexpected in CC treatments as a result of the continuousincorporation of C into the soil but was not found (Ta-ble 5) Minoshima et al (2006) found that nematodesin the higher trophic levels were not significantly asso-ciated with the C pools in the soil Previous studies foundomnivore and predatory nematodes much more abundantin recently abandoned fallow fields than in cultivated orseminatural meadow lands (Haacutenel 2003) Polis et al(2000) suggest that trophic cascades produced by com-plex trophic interactions are abundant in soil systemsbut bottom-up regulation is difficult to demonstrate insoil trophic levels due to the high complexity of the soilbiota interactions In forest soils Salomon et al (2006)found more abundant microbial grazers when abundantresources were added to the soil but the effects did notextend into higher trophic levels of the soil food webleading to the conclusion that the availability of resourcesplays a minor role structuring soil food webs
Responses of plant-parasites and root feeders to tillageare usually difficult to interpret and are more closely re-lated to plant status and phenology than to soil propertiesThe association between Pratylenchus (endoparasite) andstandard tillage might be explained by the release of the
712 Nematology
Effects of soil management on soil food webs
nematodes from the roots as a result of tillage (Lenz ampEisenbeis 2000)
Ammonium MBC C K P and ergosterol were pos-itively related with total number of nematodes and theEI The EI is based on the weighted abundance of bacte-rial feeding nematodes enrichment-opportunistic relativeto longer life cycle bacterial-feeders indicating highlyactive bacterial-mediated decomposition channels Whenthe field is organically enriched these nematodes exploitthe abundant resources (fungi and bacteria) and increaserapidly in abundance due to their short life cycles and highfecundity (Bongers 1990) On the contrary high valuesof the CI indicate slower fungal-mediated decompositionpathways so a significant relationship between CI and er-gosterol was expected but not found CI was positivelycorrelated with PLFA of fungal biomarkers and EI wasnegatively correlated with PLFA of bacterial markers butnot correlated with MBC Thus the relationship betweenPLFA and microbial grazers may reflect the strength of thegrazing pressure at the sampling time The prevalence ofopportunistic bacterial feeders over other microbial feed-ers (as expressed by the EI) may decrease bacterial bio-mass (indicated by PLFA of bacterial markers) more obvi-ously than the effect of fungal feeders on fungal biomassas indicated by the positive association between the CIindicator of the prevalence of fungal-feeding nematodesover bacterial feeders with fungal biomass (inferred fromPLFA of fungal markers) The absence of correlation be-tween MBC and nematode populations may thus indicatethat the grazing pressure affects only certain microbes andnot the total microbial community
CI and BI were strongly correlated and associatedwith deeper soil layers and no tillage across all samplingdates High BI values indicate a nematode assemblagecomposed of perturbation-resistant nematodes mainly oflower trophic levels The community structure was in thiscase associated with fungal-dominated organic matterdecomposition pathways The SI was associated withdeeper soil layers and intermittent fallow suggesting anegative relationship between predator abundance and thehigh physical disturbance and biological activity presentat the soil surface and in the continuous cropping plots
Conclusions
Different tillage practices and cropping systems deter-mine soil properties and thus nematode abundance Theseeffects vary with nematode trophic and functional group
By the end of the experiment each treatment supporteddifferent nematode assemblages and soil food webs
Each soil food web index describes a model nema-tode assemblage (Ferris et al 2001) Our four treat-ments structured four different nematode assemblagesThe combination of standard tillage and continuous crop-ping (STCC) was associated with high EI values reflect-ing an assemblage predominantly composed of bacterial-feeding nematodes with short life cycles This enrichedassemblage was especially characteristic of the upper soillayer Perhaps not surprisingly for a long-disturbed agri-cultural system we did not find the relationships we ex-pected between continuous cropping and the abundanceof predator and omnivore nematodes The organisms inthe higher levels of the soil food web did not respond tothe continuous input of C in the soil and a long recoveryperiod may be required for appropriate taxa to be rein-troduced and to increase Intermittent fallow (especiallySTF) supported a longer more structured soil food web(high SI values) especially in the deeper soil layers Thecombination of no tillage and intermittent fallow (NTF)supported a fungal-based community with slower organicmatter decomposition rates especially below the upper 5cm of soil The accumulation of plant residues on the soilsurface may result in slower incorporation of C into thefood web and exploitation by fungi Indeed the absenceof tillage and thus of physical perturbation would not dis-rupt fungal hyphae Finally the combination of no tillageand continuous cropping (NTCC) supported a less well-defined assemblage dominated by basal perturbation-resistant nematodes
Acknowledgements
This research was supported by California Bay DeltaAuthority (CBDA)-Ecosystem Restoration Program grant ERP-02-P36 by the California Department of Food andAgricultureKearney Foundation of Soil Science Projects2003011 and by the Kearney Foundation of Soil ScienceProject 2005210 We thank the LTRAS staff for fieldmanagement Many thanks to members of the Jackson andTemple lab groups for help with sampling and Dr S Goyalfor guidance with the HPLC
References
ADEDIRAN JA ADEGBITE AA AKINLOSOTU TAAGBAJE GO TAIWO LB OWOLADE OF amp
Vol 8(5) 2006 713
S Saacutenchez-Moreno et al
OLUWATOSIN GA (2005) Evaluation of fallow and covercrops for nematode suppression in three agroecologies ofsouth western Nigeria African Journal of Biotechnology 41034-1039
BERKELMANS R FERRIS H TENUTA M amp VAN
BRUGGEN AHC (2003) Effects of long-term crop man-agement on nematode trophic levels other than plant feedersdisappear after 1 year of disruptive soil management AppliedSoil Ecology 23 223-235
BONGERS T (1990) The maturity index an ecological mea-sure of environmental disturbance based on nematode speciescomposition Oecologia 83 14-19
BONGERS T amp BONGERS M (1998) Functional diversity ofnematodes Applied Soil Ecology 10 239-251
BOSSIO DA SCOW KM GUNAPALA N amp GRAHAMKJ (1998) Determinants soil microbial communities ef-fects of agricultural management season and soil type onphospholipids fatty acid profiles Microbial Ecology 36 1-12
BOUWMAN LA BLOEM J VAN DEN BOOGERT PHJFBREMER F HOENDERBOOM GHJ amp DE RUITER PC(1994) Short-term and long-term effects of bacterivorousnematodes and nematophagous fungi on carbon and nitrogenmineralization in microcosms Biology and Fertility of Soils17 249-256
BULLUCK III LR BARKER KR amp RISTAINO JB (2002)Influences of organic and synthetic soil fertility amendmentson nematode trophic groups and community dynamics undertomatoes Applied Soil Ecology 21 233-250
CADET P PATEacute E amp NrsquoDIAYE-FAYE N (2003) Nematodecommunity changes and survival rates under natural fallow inthe sudano sahelian area of Senegal Pedobiologia 47 149-160
CHAN KY (2001) An overview of some tillage impacts onearthworm population abundance and diversity ndash implicationsfor functioning in soils Soil and Tillage Research 57 179-191
DE MESEL I DERYCKE S MOENS T VAN DER GUCHTK VINCX M amp SWINGS J (2004) Top-down impactof bacteriovorous nematodes on the bacterial communitystructure a microcosm study Environmental Microbiology 6733-744
EKSCHMITT E STIERHOF T DAUBER J KREIMES Kamp WOLTERS V (2003) On the quality of soil biodiversityindicators abiotic parameters as predictor of soil faunalrichness at different spatial scales Agriculture Ecosystemsand Environment 98 273-283
ETTEMA CH (1998) Soil nematode diversity species coex-istence and ecosystem function Journal of Nematology 30159-169
FERRIS H VENETTE RC amp LAU SS (1997) Populationenergetics of bacterial-feeding nematodes Carbon and nitro-gen budgets Soil Biology and Biochemistry 29 1183-1194
FERRIS H BONGERS T amp DE GOEDE RGM (2001) Aframework for soil food web diagnostics extension of the
nematode faunal analysis concept Applied Soil Ecology 1813-29
FERRIS H VENETTE RC amp SCOW KM (2004) Soil man-agement to enhance bacteriovore and fungivore nematodepopulations and their nitrogen mineralization function Ap-plied Soil Ecology 25 19-35
FISCUS DA amp NEHER DA (2002) Distinguishing sensi-tivity of free-leaving soil nematode genera to physical andchemical disturbances Ecological Applications 12 565-575
FU S FERRIS H BROWN D amp PLANT R (2005) Doespositive feedback effect of nematodes on the biomass andactivity of their bacteria prey vary with nematode speciesand population size Soil Biology and Biochemistry 37 1979-1987
GYEDU-ABABIO TK FURTENBERG JP BAIRD D ampVANREUSEL A (1999) Nematodes as indicators of pollu-tion a case study from the Swartkops river system SouthAfrica Hydrobiologia 397 155-169
HAacuteNEL L (2003) Recovery of soil nematode populations fromcropping stress by natural secondary succession to meadowland Applied Soil Ecology 22 255-270
KLADIVCO EJ (2001) Tillage systems and soil ecology Soiland Tillage Research 61 61-76
KORTHALS GW VAN DE ENDE A VAN MEGEN HLEXMOND THM KAMMENGA JE amp BONGERS T(1996) Short-term effects of cadmium copper nickel andzinc on soil nematodes from different feeding and life-historystrategy groups Applied Soil Ecology 4 107-117
LENZ R amp EISENBEIS G (2000) Short-term effects ofdifferent tillage in a sustainable farming system on nematodecommunity structure Biology and Fertility of Soils 31 237-244
LIPHADZI KB AL-KHATIB K BENSCH C STAHLMANPW DILLE JA TODD T RICE CW HORAK MJamp HEAD G (2005) Soil microbial and nematode commu-nities as affected by glyphosate and tillage practices in aglyphosate-resistant cropping system Weed Science 53 536-545
MIKOLA J amp SETAumlLAuml H (1998a) No evidence of trophiccascades in an experimental microbial-based soil food webEcology 79 153-164
MIKOLA J amp SETAumlLAuml H (1998b) Relating species diversityto ecosystem functioning mechanistic backgrounds and ex-perimental approach with a decomposer food web Oikos 83180-194
MINOSHIMA H JACKSON LE CAVAGNARO TRSAacuteNCHEZ-MORENO S FERRIS H TEMPLE S ampMITCHELL J (2006) Soil food webs and carbon dynam-ics in response to conservation tillage in legume rotations inCalifornia Soil Science Society of America in press
MULDER C DE ZWART D VAN WIJNEN HJSCHOUTEN AJ amp BREURE AM (2003) Observa-tional and simulated evidence of ecological shifts withinthe soil nematode community of agroecosystems under
714 Nematology
Effects of soil management on soil food webs
conventional and organic farming Functional Ecology 17516-525
MULDER C SCHOUTEN AJ HUND-RINKE K ampBREURE AM (2005) The use of nematodes in ecologi-cal soil classification and assessment concepts Ecotoxicologyand Environmental Safety 62 278-289
NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
PORAZINSKA DL DUNCAN LW MCSORLEY R ampGRAHAM JH (1999) Nematode communities as indicatorsof status and processes of a soil ecosystems influenced byagricultural management practices Applied Soil Ecology 1369-86
POSTMA-BLAAUW MB DE VRIES FT DE GOEDERGM BLOEM J FABER JH amp BRUSSAARD L(2005) Within-trophic group interactions of bacterivorousnematode species and their effects on the bacterial commu-nity and nitrogen mineralization Oecologia 142 428-439
ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
SALOMON J ALPHEI J RUF A SCHAEFER M SCHEUS SCHNEIDER K SUumlHRIG A amp MARAUN M (2006)Transitory dynamic effects in the soil invertebrate communityin a temperate deciduous forest Effects of resource qualitySoil Biology and Biochemistry 38 209-221
SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
STATSOFT INC (1996) STATISTICA for Windows (ComputerProgram Manual) Tulsa OK USA
THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
YAMADA M (2001) Methods of control injury associatedwith continuous vegetable cropping in Japan ndash Crop rotationand several cultural practices Japan Agricultural ResearchQuarterly 35 39-45
YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
YEATES GW BONGERS T DE GOEDE RGM FRECK-MAN DW amp GEORGIEVA SS (1993) Feeding-habits insoil nematode families and genera ndash an outline for soil ecolo-gists Journal of Nematology 25 315-331
Vol 8(5) 2006 715
S Saacutenchez-Moreno et al
tation for the group associated with increased N mineral-isation (Ferris et al 1997 2004) By contrast Panagro-laimus and Plectus ordered in an opposite position due totheir negative relationship with PLFA biomarkers of fungiand bacteria and with bulk density Panagrolaimus has ahigh metabolic rate and a broad non-selective microbialfeeding habit (De Mesel et al 2004) It may decreasebacterial populations (as indicated by lower PFLA frombacterial markers) to a greater extent than other bacter-ial feeders in our plots When microbivorous nematodespredominate in soils they enhance N mineralisation andthus the availability of N for plants (Ferris et al 2004)Total soil N may be correlated with abundance of certainnematodes (Nakamoto et al 2006) but potentially min-eralisable N is a better indicator of N availability Thatmight explain why total soil N was associated only withabundance of Tylenchidae in this study Total C on thecontrary was more strongly associated with total nema-tode abundance
Surprisingly the abundance of fungal-feeding nema-todes such as Aphelenchus and some Tylenchidae was notrelated as strongly with ergosterol as expected suggest-ing that fungal biomass may not determining the size offungal feeder populations Villenave et al (2004) founddiffering responses of fungal feeders to ergosterol contentfungal feeders in cp groups 2 and 4 were positively relatedwith ergosterol but fungal feeders in the cp 5 group werenot
The discrimination between responses of nematodesin the higher and the lower levels of the soil food webwas evident in the CCA ordination revealing a link be-tween lower trophic levels and MBC NH+
4 ergosteroltotal N total C and certain PLFA Bacterial- fungal-and plant-feeding taxa with low cp values ordered op-posite to predatory and omnivore nematodes such asPrionchulus Qudsianematidae Aporcelaimidae Disco-laimus and Mylonchulus With the only exceptions ofthe plant-feeder Tylenchorhynchus (cp 3) which orderedclose to Mesorhabditis (cp 1) and Acrobeles (cp 2) whichscored close to the predators (cp 4 5) nematodes belong-ing to cp groups 1 and 2 showed an opposite response toenvironmental variables than those in cp groups 3 4 and 5
Predatory and omnivore nematodes are in higher co-loniser-persistent groups (3) and are more sensitive tosoil perturbation Intermittent fallow and standard tillagesupported higher abundances of most of the predators andomnivores Mylonchulus Qudsianematidae Prionchulusand Aporcelaimidae It is generally accepted that nema-tode functional diversity decreases with increasing man-
Table 5 Summarized effects of treatments on nematode trophicgroups (Ba = bacterial-feeders Fu = fungal-feeders Pp =plant-feeders PO = predators and omnivores)
Standard tillage No-tillage
Fallow Small increase of Ba Decrease of BaSmall decrease of Fu Decrease of FuDecrease of Pp Small decrease of PpIncrease of PO Increase of POIncrease of SI values Increase of CI values
Continuous Increase of Ba Small decrease of Bacropping Small increase of Fu Increase of Fu
Increase of Pp Increase of PpDecrease of PO Decrease of POIncrease of EI values Increase of BI values
agement intensity (Mulder et al 2003) predatory nema-todes were in our case much more affected by the crop-ping pattern (being enhanced in the intermittent fallowtreatment) than by standard tillage Our results thus sug-gest that even though predatory nematodes are sensitive tosoil physical perturbation other soil forces can drive theirabundance In some studies 25 years of tillage did notstrongly affect predators but reduced fungal-feeder nema-todes (Wang et al 2004)
An increase in predator and omnivore nematodes wasexpected in CC treatments as a result of the continuousincorporation of C into the soil but was not found (Ta-ble 5) Minoshima et al (2006) found that nematodesin the higher trophic levels were not significantly asso-ciated with the C pools in the soil Previous studies foundomnivore and predatory nematodes much more abundantin recently abandoned fallow fields than in cultivated orseminatural meadow lands (Haacutenel 2003) Polis et al(2000) suggest that trophic cascades produced by com-plex trophic interactions are abundant in soil systemsbut bottom-up regulation is difficult to demonstrate insoil trophic levels due to the high complexity of the soilbiota interactions In forest soils Salomon et al (2006)found more abundant microbial grazers when abundantresources were added to the soil but the effects did notextend into higher trophic levels of the soil food webleading to the conclusion that the availability of resourcesplays a minor role structuring soil food webs
Responses of plant-parasites and root feeders to tillageare usually difficult to interpret and are more closely re-lated to plant status and phenology than to soil propertiesThe association between Pratylenchus (endoparasite) andstandard tillage might be explained by the release of the
712 Nematology
Effects of soil management on soil food webs
nematodes from the roots as a result of tillage (Lenz ampEisenbeis 2000)
Ammonium MBC C K P and ergosterol were pos-itively related with total number of nematodes and theEI The EI is based on the weighted abundance of bacte-rial feeding nematodes enrichment-opportunistic relativeto longer life cycle bacterial-feeders indicating highlyactive bacterial-mediated decomposition channels Whenthe field is organically enriched these nematodes exploitthe abundant resources (fungi and bacteria) and increaserapidly in abundance due to their short life cycles and highfecundity (Bongers 1990) On the contrary high valuesof the CI indicate slower fungal-mediated decompositionpathways so a significant relationship between CI and er-gosterol was expected but not found CI was positivelycorrelated with PLFA of fungal biomarkers and EI wasnegatively correlated with PLFA of bacterial markers butnot correlated with MBC Thus the relationship betweenPLFA and microbial grazers may reflect the strength of thegrazing pressure at the sampling time The prevalence ofopportunistic bacterial feeders over other microbial feed-ers (as expressed by the EI) may decrease bacterial bio-mass (indicated by PLFA of bacterial markers) more obvi-ously than the effect of fungal feeders on fungal biomassas indicated by the positive association between the CIindicator of the prevalence of fungal-feeding nematodesover bacterial feeders with fungal biomass (inferred fromPLFA of fungal markers) The absence of correlation be-tween MBC and nematode populations may thus indicatethat the grazing pressure affects only certain microbes andnot the total microbial community
CI and BI were strongly correlated and associatedwith deeper soil layers and no tillage across all samplingdates High BI values indicate a nematode assemblagecomposed of perturbation-resistant nematodes mainly oflower trophic levels The community structure was in thiscase associated with fungal-dominated organic matterdecomposition pathways The SI was associated withdeeper soil layers and intermittent fallow suggesting anegative relationship between predator abundance and thehigh physical disturbance and biological activity presentat the soil surface and in the continuous cropping plots
Conclusions
Different tillage practices and cropping systems deter-mine soil properties and thus nematode abundance Theseeffects vary with nematode trophic and functional group
By the end of the experiment each treatment supporteddifferent nematode assemblages and soil food webs
Each soil food web index describes a model nema-tode assemblage (Ferris et al 2001) Our four treat-ments structured four different nematode assemblagesThe combination of standard tillage and continuous crop-ping (STCC) was associated with high EI values reflect-ing an assemblage predominantly composed of bacterial-feeding nematodes with short life cycles This enrichedassemblage was especially characteristic of the upper soillayer Perhaps not surprisingly for a long-disturbed agri-cultural system we did not find the relationships we ex-pected between continuous cropping and the abundanceof predator and omnivore nematodes The organisms inthe higher levels of the soil food web did not respond tothe continuous input of C in the soil and a long recoveryperiod may be required for appropriate taxa to be rein-troduced and to increase Intermittent fallow (especiallySTF) supported a longer more structured soil food web(high SI values) especially in the deeper soil layers Thecombination of no tillage and intermittent fallow (NTF)supported a fungal-based community with slower organicmatter decomposition rates especially below the upper 5cm of soil The accumulation of plant residues on the soilsurface may result in slower incorporation of C into thefood web and exploitation by fungi Indeed the absenceof tillage and thus of physical perturbation would not dis-rupt fungal hyphae Finally the combination of no tillageand continuous cropping (NTCC) supported a less well-defined assemblage dominated by basal perturbation-resistant nematodes
Acknowledgements
This research was supported by California Bay DeltaAuthority (CBDA)-Ecosystem Restoration Program grant ERP-02-P36 by the California Department of Food andAgricultureKearney Foundation of Soil Science Projects2003011 and by the Kearney Foundation of Soil ScienceProject 2005210 We thank the LTRAS staff for fieldmanagement Many thanks to members of the Jackson andTemple lab groups for help with sampling and Dr S Goyalfor guidance with the HPLC
References
ADEDIRAN JA ADEGBITE AA AKINLOSOTU TAAGBAJE GO TAIWO LB OWOLADE OF amp
Vol 8(5) 2006 713
S Saacutenchez-Moreno et al
OLUWATOSIN GA (2005) Evaluation of fallow and covercrops for nematode suppression in three agroecologies ofsouth western Nigeria African Journal of Biotechnology 41034-1039
BERKELMANS R FERRIS H TENUTA M amp VAN
BRUGGEN AHC (2003) Effects of long-term crop man-agement on nematode trophic levels other than plant feedersdisappear after 1 year of disruptive soil management AppliedSoil Ecology 23 223-235
BONGERS T (1990) The maturity index an ecological mea-sure of environmental disturbance based on nematode speciescomposition Oecologia 83 14-19
BONGERS T amp BONGERS M (1998) Functional diversity ofnematodes Applied Soil Ecology 10 239-251
BOSSIO DA SCOW KM GUNAPALA N amp GRAHAMKJ (1998) Determinants soil microbial communities ef-fects of agricultural management season and soil type onphospholipids fatty acid profiles Microbial Ecology 36 1-12
BOUWMAN LA BLOEM J VAN DEN BOOGERT PHJFBREMER F HOENDERBOOM GHJ amp DE RUITER PC(1994) Short-term and long-term effects of bacterivorousnematodes and nematophagous fungi on carbon and nitrogenmineralization in microcosms Biology and Fertility of Soils17 249-256
BULLUCK III LR BARKER KR amp RISTAINO JB (2002)Influences of organic and synthetic soil fertility amendmentson nematode trophic groups and community dynamics undertomatoes Applied Soil Ecology 21 233-250
CADET P PATEacute E amp NrsquoDIAYE-FAYE N (2003) Nematodecommunity changes and survival rates under natural fallow inthe sudano sahelian area of Senegal Pedobiologia 47 149-160
CHAN KY (2001) An overview of some tillage impacts onearthworm population abundance and diversity ndash implicationsfor functioning in soils Soil and Tillage Research 57 179-191
DE MESEL I DERYCKE S MOENS T VAN DER GUCHTK VINCX M amp SWINGS J (2004) Top-down impactof bacteriovorous nematodes on the bacterial communitystructure a microcosm study Environmental Microbiology 6733-744
EKSCHMITT E STIERHOF T DAUBER J KREIMES Kamp WOLTERS V (2003) On the quality of soil biodiversityindicators abiotic parameters as predictor of soil faunalrichness at different spatial scales Agriculture Ecosystemsand Environment 98 273-283
ETTEMA CH (1998) Soil nematode diversity species coex-istence and ecosystem function Journal of Nematology 30159-169
FERRIS H VENETTE RC amp LAU SS (1997) Populationenergetics of bacterial-feeding nematodes Carbon and nitro-gen budgets Soil Biology and Biochemistry 29 1183-1194
FERRIS H BONGERS T amp DE GOEDE RGM (2001) Aframework for soil food web diagnostics extension of the
nematode faunal analysis concept Applied Soil Ecology 1813-29
FERRIS H VENETTE RC amp SCOW KM (2004) Soil man-agement to enhance bacteriovore and fungivore nematodepopulations and their nitrogen mineralization function Ap-plied Soil Ecology 25 19-35
FISCUS DA amp NEHER DA (2002) Distinguishing sensi-tivity of free-leaving soil nematode genera to physical andchemical disturbances Ecological Applications 12 565-575
FU S FERRIS H BROWN D amp PLANT R (2005) Doespositive feedback effect of nematodes on the biomass andactivity of their bacteria prey vary with nematode speciesand population size Soil Biology and Biochemistry 37 1979-1987
GYEDU-ABABIO TK FURTENBERG JP BAIRD D ampVANREUSEL A (1999) Nematodes as indicators of pollu-tion a case study from the Swartkops river system SouthAfrica Hydrobiologia 397 155-169
HAacuteNEL L (2003) Recovery of soil nematode populations fromcropping stress by natural secondary succession to meadowland Applied Soil Ecology 22 255-270
KLADIVCO EJ (2001) Tillage systems and soil ecology Soiland Tillage Research 61 61-76
KORTHALS GW VAN DE ENDE A VAN MEGEN HLEXMOND THM KAMMENGA JE amp BONGERS T(1996) Short-term effects of cadmium copper nickel andzinc on soil nematodes from different feeding and life-historystrategy groups Applied Soil Ecology 4 107-117
LENZ R amp EISENBEIS G (2000) Short-term effects ofdifferent tillage in a sustainable farming system on nematodecommunity structure Biology and Fertility of Soils 31 237-244
LIPHADZI KB AL-KHATIB K BENSCH C STAHLMANPW DILLE JA TODD T RICE CW HORAK MJamp HEAD G (2005) Soil microbial and nematode commu-nities as affected by glyphosate and tillage practices in aglyphosate-resistant cropping system Weed Science 53 536-545
MIKOLA J amp SETAumlLAuml H (1998a) No evidence of trophiccascades in an experimental microbial-based soil food webEcology 79 153-164
MIKOLA J amp SETAumlLAuml H (1998b) Relating species diversityto ecosystem functioning mechanistic backgrounds and ex-perimental approach with a decomposer food web Oikos 83180-194
MINOSHIMA H JACKSON LE CAVAGNARO TRSAacuteNCHEZ-MORENO S FERRIS H TEMPLE S ampMITCHELL J (2006) Soil food webs and carbon dynam-ics in response to conservation tillage in legume rotations inCalifornia Soil Science Society of America in press
MULDER C DE ZWART D VAN WIJNEN HJSCHOUTEN AJ amp BREURE AM (2003) Observa-tional and simulated evidence of ecological shifts withinthe soil nematode community of agroecosystems under
714 Nematology
Effects of soil management on soil food webs
conventional and organic farming Functional Ecology 17516-525
MULDER C SCHOUTEN AJ HUND-RINKE K ampBREURE AM (2005) The use of nematodes in ecologi-cal soil classification and assessment concepts Ecotoxicologyand Environmental Safety 62 278-289
NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
PORAZINSKA DL DUNCAN LW MCSORLEY R ampGRAHAM JH (1999) Nematode communities as indicatorsof status and processes of a soil ecosystems influenced byagricultural management practices Applied Soil Ecology 1369-86
POSTMA-BLAAUW MB DE VRIES FT DE GOEDERGM BLOEM J FABER JH amp BRUSSAARD L(2005) Within-trophic group interactions of bacterivorousnematode species and their effects on the bacterial commu-nity and nitrogen mineralization Oecologia 142 428-439
ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
SALOMON J ALPHEI J RUF A SCHAEFER M SCHEUS SCHNEIDER K SUumlHRIG A amp MARAUN M (2006)Transitory dynamic effects in the soil invertebrate communityin a temperate deciduous forest Effects of resource qualitySoil Biology and Biochemistry 38 209-221
SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
STATSOFT INC (1996) STATISTICA for Windows (ComputerProgram Manual) Tulsa OK USA
THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
YAMADA M (2001) Methods of control injury associatedwith continuous vegetable cropping in Japan ndash Crop rotationand several cultural practices Japan Agricultural ResearchQuarterly 35 39-45
YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
YEATES GW BONGERS T DE GOEDE RGM FRECK-MAN DW amp GEORGIEVA SS (1993) Feeding-habits insoil nematode families and genera ndash an outline for soil ecolo-gists Journal of Nematology 25 315-331
Vol 8(5) 2006 715
Effects of soil management on soil food webs
nematodes from the roots as a result of tillage (Lenz ampEisenbeis 2000)
Ammonium MBC C K P and ergosterol were pos-itively related with total number of nematodes and theEI The EI is based on the weighted abundance of bacte-rial feeding nematodes enrichment-opportunistic relativeto longer life cycle bacterial-feeders indicating highlyactive bacterial-mediated decomposition channels Whenthe field is organically enriched these nematodes exploitthe abundant resources (fungi and bacteria) and increaserapidly in abundance due to their short life cycles and highfecundity (Bongers 1990) On the contrary high valuesof the CI indicate slower fungal-mediated decompositionpathways so a significant relationship between CI and er-gosterol was expected but not found CI was positivelycorrelated with PLFA of fungal biomarkers and EI wasnegatively correlated with PLFA of bacterial markers butnot correlated with MBC Thus the relationship betweenPLFA and microbial grazers may reflect the strength of thegrazing pressure at the sampling time The prevalence ofopportunistic bacterial feeders over other microbial feed-ers (as expressed by the EI) may decrease bacterial bio-mass (indicated by PLFA of bacterial markers) more obvi-ously than the effect of fungal feeders on fungal biomassas indicated by the positive association between the CIindicator of the prevalence of fungal-feeding nematodesover bacterial feeders with fungal biomass (inferred fromPLFA of fungal markers) The absence of correlation be-tween MBC and nematode populations may thus indicatethat the grazing pressure affects only certain microbes andnot the total microbial community
CI and BI were strongly correlated and associatedwith deeper soil layers and no tillage across all samplingdates High BI values indicate a nematode assemblagecomposed of perturbation-resistant nematodes mainly oflower trophic levels The community structure was in thiscase associated with fungal-dominated organic matterdecomposition pathways The SI was associated withdeeper soil layers and intermittent fallow suggesting anegative relationship between predator abundance and thehigh physical disturbance and biological activity presentat the soil surface and in the continuous cropping plots
Conclusions
Different tillage practices and cropping systems deter-mine soil properties and thus nematode abundance Theseeffects vary with nematode trophic and functional group
By the end of the experiment each treatment supporteddifferent nematode assemblages and soil food webs
Each soil food web index describes a model nema-tode assemblage (Ferris et al 2001) Our four treat-ments structured four different nematode assemblagesThe combination of standard tillage and continuous crop-ping (STCC) was associated with high EI values reflect-ing an assemblage predominantly composed of bacterial-feeding nematodes with short life cycles This enrichedassemblage was especially characteristic of the upper soillayer Perhaps not surprisingly for a long-disturbed agri-cultural system we did not find the relationships we ex-pected between continuous cropping and the abundanceof predator and omnivore nematodes The organisms inthe higher levels of the soil food web did not respond tothe continuous input of C in the soil and a long recoveryperiod may be required for appropriate taxa to be rein-troduced and to increase Intermittent fallow (especiallySTF) supported a longer more structured soil food web(high SI values) especially in the deeper soil layers Thecombination of no tillage and intermittent fallow (NTF)supported a fungal-based community with slower organicmatter decomposition rates especially below the upper 5cm of soil The accumulation of plant residues on the soilsurface may result in slower incorporation of C into thefood web and exploitation by fungi Indeed the absenceof tillage and thus of physical perturbation would not dis-rupt fungal hyphae Finally the combination of no tillageand continuous cropping (NTCC) supported a less well-defined assemblage dominated by basal perturbation-resistant nematodes
Acknowledgements
This research was supported by California Bay DeltaAuthority (CBDA)-Ecosystem Restoration Program grant ERP-02-P36 by the California Department of Food andAgricultureKearney Foundation of Soil Science Projects2003011 and by the Kearney Foundation of Soil ScienceProject 2005210 We thank the LTRAS staff for fieldmanagement Many thanks to members of the Jackson andTemple lab groups for help with sampling and Dr S Goyalfor guidance with the HPLC
References
ADEDIRAN JA ADEGBITE AA AKINLOSOTU TAAGBAJE GO TAIWO LB OWOLADE OF amp
Vol 8(5) 2006 713
S Saacutenchez-Moreno et al
OLUWATOSIN GA (2005) Evaluation of fallow and covercrops for nematode suppression in three agroecologies ofsouth western Nigeria African Journal of Biotechnology 41034-1039
BERKELMANS R FERRIS H TENUTA M amp VAN
BRUGGEN AHC (2003) Effects of long-term crop man-agement on nematode trophic levels other than plant feedersdisappear after 1 year of disruptive soil management AppliedSoil Ecology 23 223-235
BONGERS T (1990) The maturity index an ecological mea-sure of environmental disturbance based on nematode speciescomposition Oecologia 83 14-19
BONGERS T amp BONGERS M (1998) Functional diversity ofnematodes Applied Soil Ecology 10 239-251
BOSSIO DA SCOW KM GUNAPALA N amp GRAHAMKJ (1998) Determinants soil microbial communities ef-fects of agricultural management season and soil type onphospholipids fatty acid profiles Microbial Ecology 36 1-12
BOUWMAN LA BLOEM J VAN DEN BOOGERT PHJFBREMER F HOENDERBOOM GHJ amp DE RUITER PC(1994) Short-term and long-term effects of bacterivorousnematodes and nematophagous fungi on carbon and nitrogenmineralization in microcosms Biology and Fertility of Soils17 249-256
BULLUCK III LR BARKER KR amp RISTAINO JB (2002)Influences of organic and synthetic soil fertility amendmentson nematode trophic groups and community dynamics undertomatoes Applied Soil Ecology 21 233-250
CADET P PATEacute E amp NrsquoDIAYE-FAYE N (2003) Nematodecommunity changes and survival rates under natural fallow inthe sudano sahelian area of Senegal Pedobiologia 47 149-160
CHAN KY (2001) An overview of some tillage impacts onearthworm population abundance and diversity ndash implicationsfor functioning in soils Soil and Tillage Research 57 179-191
DE MESEL I DERYCKE S MOENS T VAN DER GUCHTK VINCX M amp SWINGS J (2004) Top-down impactof bacteriovorous nematodes on the bacterial communitystructure a microcosm study Environmental Microbiology 6733-744
EKSCHMITT E STIERHOF T DAUBER J KREIMES Kamp WOLTERS V (2003) On the quality of soil biodiversityindicators abiotic parameters as predictor of soil faunalrichness at different spatial scales Agriculture Ecosystemsand Environment 98 273-283
ETTEMA CH (1998) Soil nematode diversity species coex-istence and ecosystem function Journal of Nematology 30159-169
FERRIS H VENETTE RC amp LAU SS (1997) Populationenergetics of bacterial-feeding nematodes Carbon and nitro-gen budgets Soil Biology and Biochemistry 29 1183-1194
FERRIS H BONGERS T amp DE GOEDE RGM (2001) Aframework for soil food web diagnostics extension of the
nematode faunal analysis concept Applied Soil Ecology 1813-29
FERRIS H VENETTE RC amp SCOW KM (2004) Soil man-agement to enhance bacteriovore and fungivore nematodepopulations and their nitrogen mineralization function Ap-plied Soil Ecology 25 19-35
FISCUS DA amp NEHER DA (2002) Distinguishing sensi-tivity of free-leaving soil nematode genera to physical andchemical disturbances Ecological Applications 12 565-575
FU S FERRIS H BROWN D amp PLANT R (2005) Doespositive feedback effect of nematodes on the biomass andactivity of their bacteria prey vary with nematode speciesand population size Soil Biology and Biochemistry 37 1979-1987
GYEDU-ABABIO TK FURTENBERG JP BAIRD D ampVANREUSEL A (1999) Nematodes as indicators of pollu-tion a case study from the Swartkops river system SouthAfrica Hydrobiologia 397 155-169
HAacuteNEL L (2003) Recovery of soil nematode populations fromcropping stress by natural secondary succession to meadowland Applied Soil Ecology 22 255-270
KLADIVCO EJ (2001) Tillage systems and soil ecology Soiland Tillage Research 61 61-76
KORTHALS GW VAN DE ENDE A VAN MEGEN HLEXMOND THM KAMMENGA JE amp BONGERS T(1996) Short-term effects of cadmium copper nickel andzinc on soil nematodes from different feeding and life-historystrategy groups Applied Soil Ecology 4 107-117
LENZ R amp EISENBEIS G (2000) Short-term effects ofdifferent tillage in a sustainable farming system on nematodecommunity structure Biology and Fertility of Soils 31 237-244
LIPHADZI KB AL-KHATIB K BENSCH C STAHLMANPW DILLE JA TODD T RICE CW HORAK MJamp HEAD G (2005) Soil microbial and nematode commu-nities as affected by glyphosate and tillage practices in aglyphosate-resistant cropping system Weed Science 53 536-545
MIKOLA J amp SETAumlLAuml H (1998a) No evidence of trophiccascades in an experimental microbial-based soil food webEcology 79 153-164
MIKOLA J amp SETAumlLAuml H (1998b) Relating species diversityto ecosystem functioning mechanistic backgrounds and ex-perimental approach with a decomposer food web Oikos 83180-194
MINOSHIMA H JACKSON LE CAVAGNARO TRSAacuteNCHEZ-MORENO S FERRIS H TEMPLE S ampMITCHELL J (2006) Soil food webs and carbon dynam-ics in response to conservation tillage in legume rotations inCalifornia Soil Science Society of America in press
MULDER C DE ZWART D VAN WIJNEN HJSCHOUTEN AJ amp BREURE AM (2003) Observa-tional and simulated evidence of ecological shifts withinthe soil nematode community of agroecosystems under
714 Nematology
Effects of soil management on soil food webs
conventional and organic farming Functional Ecology 17516-525
MULDER C SCHOUTEN AJ HUND-RINKE K ampBREURE AM (2005) The use of nematodes in ecologi-cal soil classification and assessment concepts Ecotoxicologyand Environmental Safety 62 278-289
NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
PORAZINSKA DL DUNCAN LW MCSORLEY R ampGRAHAM JH (1999) Nematode communities as indicatorsof status and processes of a soil ecosystems influenced byagricultural management practices Applied Soil Ecology 1369-86
POSTMA-BLAAUW MB DE VRIES FT DE GOEDERGM BLOEM J FABER JH amp BRUSSAARD L(2005) Within-trophic group interactions of bacterivorousnematode species and their effects on the bacterial commu-nity and nitrogen mineralization Oecologia 142 428-439
ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
SALOMON J ALPHEI J RUF A SCHAEFER M SCHEUS SCHNEIDER K SUumlHRIG A amp MARAUN M (2006)Transitory dynamic effects in the soil invertebrate communityin a temperate deciduous forest Effects of resource qualitySoil Biology and Biochemistry 38 209-221
SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
STATSOFT INC (1996) STATISTICA for Windows (ComputerProgram Manual) Tulsa OK USA
THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
YAMADA M (2001) Methods of control injury associatedwith continuous vegetable cropping in Japan ndash Crop rotationand several cultural practices Japan Agricultural ResearchQuarterly 35 39-45
YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
YEATES GW BONGERS T DE GOEDE RGM FRECK-MAN DW amp GEORGIEVA SS (1993) Feeding-habits insoil nematode families and genera ndash an outline for soil ecolo-gists Journal of Nematology 25 315-331
Vol 8(5) 2006 715
S Saacutenchez-Moreno et al
OLUWATOSIN GA (2005) Evaluation of fallow and covercrops for nematode suppression in three agroecologies ofsouth western Nigeria African Journal of Biotechnology 41034-1039
BERKELMANS R FERRIS H TENUTA M amp VAN
BRUGGEN AHC (2003) Effects of long-term crop man-agement on nematode trophic levels other than plant feedersdisappear after 1 year of disruptive soil management AppliedSoil Ecology 23 223-235
BONGERS T (1990) The maturity index an ecological mea-sure of environmental disturbance based on nematode speciescomposition Oecologia 83 14-19
BONGERS T amp BONGERS M (1998) Functional diversity ofnematodes Applied Soil Ecology 10 239-251
BOSSIO DA SCOW KM GUNAPALA N amp GRAHAMKJ (1998) Determinants soil microbial communities ef-fects of agricultural management season and soil type onphospholipids fatty acid profiles Microbial Ecology 36 1-12
BOUWMAN LA BLOEM J VAN DEN BOOGERT PHJFBREMER F HOENDERBOOM GHJ amp DE RUITER PC(1994) Short-term and long-term effects of bacterivorousnematodes and nematophagous fungi on carbon and nitrogenmineralization in microcosms Biology and Fertility of Soils17 249-256
BULLUCK III LR BARKER KR amp RISTAINO JB (2002)Influences of organic and synthetic soil fertility amendmentson nematode trophic groups and community dynamics undertomatoes Applied Soil Ecology 21 233-250
CADET P PATEacute E amp NrsquoDIAYE-FAYE N (2003) Nematodecommunity changes and survival rates under natural fallow inthe sudano sahelian area of Senegal Pedobiologia 47 149-160
CHAN KY (2001) An overview of some tillage impacts onearthworm population abundance and diversity ndash implicationsfor functioning in soils Soil and Tillage Research 57 179-191
DE MESEL I DERYCKE S MOENS T VAN DER GUCHTK VINCX M amp SWINGS J (2004) Top-down impactof bacteriovorous nematodes on the bacterial communitystructure a microcosm study Environmental Microbiology 6733-744
EKSCHMITT E STIERHOF T DAUBER J KREIMES Kamp WOLTERS V (2003) On the quality of soil biodiversityindicators abiotic parameters as predictor of soil faunalrichness at different spatial scales Agriculture Ecosystemsand Environment 98 273-283
ETTEMA CH (1998) Soil nematode diversity species coex-istence and ecosystem function Journal of Nematology 30159-169
FERRIS H VENETTE RC amp LAU SS (1997) Populationenergetics of bacterial-feeding nematodes Carbon and nitro-gen budgets Soil Biology and Biochemistry 29 1183-1194
FERRIS H BONGERS T amp DE GOEDE RGM (2001) Aframework for soil food web diagnostics extension of the
nematode faunal analysis concept Applied Soil Ecology 1813-29
FERRIS H VENETTE RC amp SCOW KM (2004) Soil man-agement to enhance bacteriovore and fungivore nematodepopulations and their nitrogen mineralization function Ap-plied Soil Ecology 25 19-35
FISCUS DA amp NEHER DA (2002) Distinguishing sensi-tivity of free-leaving soil nematode genera to physical andchemical disturbances Ecological Applications 12 565-575
FU S FERRIS H BROWN D amp PLANT R (2005) Doespositive feedback effect of nematodes on the biomass andactivity of their bacteria prey vary with nematode speciesand population size Soil Biology and Biochemistry 37 1979-1987
GYEDU-ABABIO TK FURTENBERG JP BAIRD D ampVANREUSEL A (1999) Nematodes as indicators of pollu-tion a case study from the Swartkops river system SouthAfrica Hydrobiologia 397 155-169
HAacuteNEL L (2003) Recovery of soil nematode populations fromcropping stress by natural secondary succession to meadowland Applied Soil Ecology 22 255-270
KLADIVCO EJ (2001) Tillage systems and soil ecology Soiland Tillage Research 61 61-76
KORTHALS GW VAN DE ENDE A VAN MEGEN HLEXMOND THM KAMMENGA JE amp BONGERS T(1996) Short-term effects of cadmium copper nickel andzinc on soil nematodes from different feeding and life-historystrategy groups Applied Soil Ecology 4 107-117
LENZ R amp EISENBEIS G (2000) Short-term effects ofdifferent tillage in a sustainable farming system on nematodecommunity structure Biology and Fertility of Soils 31 237-244
LIPHADZI KB AL-KHATIB K BENSCH C STAHLMANPW DILLE JA TODD T RICE CW HORAK MJamp HEAD G (2005) Soil microbial and nematode commu-nities as affected by glyphosate and tillage practices in aglyphosate-resistant cropping system Weed Science 53 536-545
MIKOLA J amp SETAumlLAuml H (1998a) No evidence of trophiccascades in an experimental microbial-based soil food webEcology 79 153-164
MIKOLA J amp SETAumlLAuml H (1998b) Relating species diversityto ecosystem functioning mechanistic backgrounds and ex-perimental approach with a decomposer food web Oikos 83180-194
MINOSHIMA H JACKSON LE CAVAGNARO TRSAacuteNCHEZ-MORENO S FERRIS H TEMPLE S ampMITCHELL J (2006) Soil food webs and carbon dynam-ics in response to conservation tillage in legume rotations inCalifornia Soil Science Society of America in press
MULDER C DE ZWART D VAN WIJNEN HJSCHOUTEN AJ amp BREURE AM (2003) Observa-tional and simulated evidence of ecological shifts withinthe soil nematode community of agroecosystems under
714 Nematology
Effects of soil management on soil food webs
conventional and organic farming Functional Ecology 17516-525
MULDER C SCHOUTEN AJ HUND-RINKE K ampBREURE AM (2005) The use of nematodes in ecologi-cal soil classification and assessment concepts Ecotoxicologyand Environmental Safety 62 278-289
NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
PORAZINSKA DL DUNCAN LW MCSORLEY R ampGRAHAM JH (1999) Nematode communities as indicatorsof status and processes of a soil ecosystems influenced byagricultural management practices Applied Soil Ecology 1369-86
POSTMA-BLAAUW MB DE VRIES FT DE GOEDERGM BLOEM J FABER JH amp BRUSSAARD L(2005) Within-trophic group interactions of bacterivorousnematode species and their effects on the bacterial commu-nity and nitrogen mineralization Oecologia 142 428-439
ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
SALOMON J ALPHEI J RUF A SCHAEFER M SCHEUS SCHNEIDER K SUumlHRIG A amp MARAUN M (2006)Transitory dynamic effects in the soil invertebrate communityin a temperate deciduous forest Effects of resource qualitySoil Biology and Biochemistry 38 209-221
SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
STATSOFT INC (1996) STATISTICA for Windows (ComputerProgram Manual) Tulsa OK USA
THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
YAMADA M (2001) Methods of control injury associatedwith continuous vegetable cropping in Japan ndash Crop rotationand several cultural practices Japan Agricultural ResearchQuarterly 35 39-45
YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
YEATES GW BONGERS T DE GOEDE RGM FRECK-MAN DW amp GEORGIEVA SS (1993) Feeding-habits insoil nematode families and genera ndash an outline for soil ecolo-gists Journal of Nematology 25 315-331
Vol 8(5) 2006 715
Effects of soil management on soil food webs
conventional and organic farming Functional Ecology 17516-525
MULDER C SCHOUTEN AJ HUND-RINKE K ampBREURE AM (2005) The use of nematodes in ecologi-cal soil classification and assessment concepts Ecotoxicologyand Environmental Safety 62 278-289
NAKAMOTO T YAMAGISHI J amp MIURA F (2006) Effectof reduced tillage on weeds and soil organisms in winterwheat and summer maize cropping on Humic Andosols inCentral Japan Soil and Tillage Research 85 94-106
NEHER D (2001) Role of nematodes in soil health and theiruse as indicators Journal of Nematology 33 161-168
PANKHURST CE STIRLING GR MAGAREY RCBLAIR BL HOLT JA BELL MJ amp GARSIDE AL(2005) Quantification of the effects of rotation breaks on soilbiological properties and their impact on yield decline in sug-arcane Soil Biology and Biochemistry 37 1121-1130
POLIS A SEARS ALW HUXEL GR STRONG DRamp MARON J (2000) When is a trophic cascade a trophiccascade Trends in Ecology and Evolution 15 473-475
POPOVICI I amp CIOBANU M (2000) Diversity and distribu-tion of nematode community in grassland from Romania inrelation to vegetation and soil characteristics Applied SoilEcology 14 27-36
PORAZINSKA DL DUNCAN LW MCSORLEY R ampGRAHAM JH (1999) Nematode communities as indicatorsof status and processes of a soil ecosystems influenced byagricultural management practices Applied Soil Ecology 1369-86
POSTMA-BLAAUW MB DE VRIES FT DE GOEDERGM BLOEM J FABER JH amp BRUSSAARD L(2005) Within-trophic group interactions of bacterivorousnematode species and their effects on the bacterial commu-nity and nitrogen mineralization Oecologia 142 428-439
ROBERTS PA MATTHEWS WC amp EHLERS JD (2005)Root-knot nematode resistant cowpea cover crops in tomatoproduction systems Agronomy Journal 97 1626-1635
SALOMON J ALPHEI J RUF A SCHAEFER M SCHEUS SCHNEIDER K SUumlHRIG A amp MARAUN M (2006)Transitory dynamic effects in the soil invertebrate communityin a temperate deciduous forest Effects of resource qualitySoil Biology and Biochemistry 38 209-221
SMILEY RW MERRIFIELD K PATTERSON LM WHIT-TAKER RG GOURLIE JA amp EASLEY SA (2004) Ne-matodes in dryland field crops in the semiarid Pacific North-west United States Journal of Nematology 36 54-68
STATSOFT INC (1996) STATISTICA for Windows (ComputerProgram Manual) Tulsa OK USA
THIAGALINGAM K DALGLIESH NP GOULD NS MC-COWN RL COGLE AL amp CHAPMAN AL (1996)Comparison of no-tillage and conventional tillage in the de-velopment of sustainable farming systems in the semi-aridtropics Australian Journal of Experimental Agriculture 36995-1002
URZELAI A HERNAacuteNDEZ AJ amp PASTOR J (2000) Bioticindices based on soil nematode communities for assessingsoil quality in terrestrial ecosystems The Science of TotalEnvironment 247 253-261
VILLENAVE C BONGERS T EKSCHMITT K FERNAN-DES P amp OLIVER R (2003) Changes in nematode commu-nities after manuring in millet fields in Senegal Nematology5 351-358
VILLENAVE C EKSCHMITT K NAZARET S amp BONGERST (2004) Interactions between nematodes and microbialcommunities in a tropical soil following manipulation of thesoil food web Soil Biology and Biochemistry 36 2033-2043
WANG KH MCSORLEY R amp GALLAGER RN (2004)Relationship of soil management history and nutrient statusto nematode community structure Nematropica 34 83-95
WARDLE DA (1995) Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices In Begon M amp Fitter AH (Eds)Advances in ecological research Vol 26 New York NYUSA Academic Press pp 105-185
WARDLE DA YEATES GW WATSON RN amp NICHOL-SON KS (1995) The detritus food web and the diversityof soil fauna as indicators of disturbance regimes in agro-ecosystems Plant and Soil 170 35-43
WARDLE DA YEATES GW BONNER KI NICHOL-SON KS amp WATSON RN (2001) Impacts of ground veg-etation management strategies in a kiwifruit orchard on thecomposition and functioning of the soil biota Soil Biologyand Biochemistry 33 893-905
WARDLE DA WILLIAMSON WM YEATES GW ampBONNER KI (2005) Trickle-down effects of abovegroundtrophic cascades on the soil food web Oikos 111 348-358
YAMADA M (2001) Methods of control injury associatedwith continuous vegetable cropping in Japan ndash Crop rotationand several cultural practices Japan Agricultural ResearchQuarterly 35 39-45
YEATES GW (2003) Nematodes as soil indicators functionaland biodiversity aspects Biology and Fertility of Soils 37199-210
YEATES GW BONGERS T DE GOEDE RGM FRECK-MAN DW amp GEORGIEVA SS (1993) Feeding-habits insoil nematode families and genera ndash an outline for soil ecolo-gists Journal of Nematology 25 315-331
Vol 8(5) 2006 715
