Assessment of Relationships between Earthworms and Soil Abiotic and Biotic Factors as a Tool in ...

14 Pages·2016·0.62 MB·English

sustainability
Article
Assessment of Relationships between Earthworms
and Soil Abiotic and Biotic Factors as a Tool in
Sustainable Agricultural
RadoslavaKanianska1,*,JanaJad’ud’ová1,JarmilaMakovníková2andMiriamKizeková3
1 FacultyofNaturalSciences,MatejBelUniversity,Tajovského40,BanskáBystrica97401,Slovakia;
[email protected]
2 NationalAgriculturalandFoodCentre—SoilScienceandConservationResearchInstituteBratislava,
RegionalStationBanskáBystrica,Mládežnícka36,BanskáBystrica97421,Slovakia;
[email protected]
3 NationalAgriculturalandFoodCentre—GrasslandandMountainAgricultureResearchInstitute,
Mládežnícka36,BanskáBystrica97421,Slovakia;[email protected]
* Correspondence:[email protected];Tel.:[phone]
AcademicEditor:MarcA.Rosen
Received:13June2016;Accepted:2September2016;Published:7September2016
Abstract: Earthworms are a major component of soil fauna communities. They influence soil
chemical, biological, and physical processes and vice versa, their abundance and diversity are
influencedbynaturalcharacteristicsorlandmanagementpractices. Thereisneedtoestablishtheir
characteristicsandrelations. Inthisstudyearthwormdensity(ED),bodybiomass(EB),anddiversity
inrelationtolanduse(arableland—AL,permanentgrasslands—PG),management,andselected
abiotic(soilchemical,physical,climaterelated)andbiotic(arthropoddensityandbiomass,ground
beetledensity,carabiddensity)indicatorswereanalysedatsevendifferentstudysitesinSlovakia.
Onaverage,thedensityofearthwormswasnearlytwiceashighinPGcomparedtoAL.Among
five soil types used as arable land, Fluvisols created the most suitable conditions for earthworm
abundanceandbiomass. WerecordedasignificantcorrelationbetweenED,EBandsoilmoisture
in arable land. In permanent grasslands, the main climate related factor was soil temperature.
Relationshipsbetweenearthwormsandsomechemicalproperties(pH,availablenutrients)were
observedonlyinarableland. Ourfindingsindicatetrophicinteractionbetweenearthwormsand
carabidsinorganicallymanagedarableland. Comprehensiveassessmentofobservedrelationships
canhelpinearthwormmanagementtoachievesustainableagriculturalsystems.
Keywords: earthworm; agro-ecosystem; sustainability; climate; soil type; soil moisture;
soil temperature;arthropod;groundbeetle;carabid
1. Introduction
Soil macro-invertebrates play a key role in soil organic matter transformations and nutrient
dynamicsatdifferentspatialandtemporalscalesthroughperturbationandtheproductionofbiogenic
structuresfortheimprovementofsoilfertilityandlandproductivity[1,2]. Assuch,theyinfluence
soilchemical,biological,andphysicalprocesses[3]orcontributetobiologicalcontrol[4],foodweb
dynamicsandsoilprocesses[5,6]. Amongnumerousmacro-invertebratesinthesoil,earthwormsare
themostimportantcomponentsofsoilbiotaintermsofsoilformationandmaintenanceofsoilstructure
andfertility[7]. Duetoearthworms’activityinsoiltheyareclassifiedas“ecosystemengineers”,which
meansthattheyaffecttheirenvironment,eitherbioticorabiotic. Ecosystemengineersarekeystone
speciesthatmodifytheirhabitatsostronglythatitinturnaffectsotherorganisms. Christensenand
Mather[8]showedthatearthwormnumberandbiomassreflectbothnaturalsoilparameters,e.g.,sand
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content,andagriculturalpractices. Kerneckeretal.[9]confirmedtheeffectofsoilmoisture,vegetation
diversity,andsoilnutrientconcentrationsonearthwormspeciescompositions.
Therearemanystudiesindifferentpartsoftheworldwhichhaveassessedearthwormabundance
and functions in the soils [10–16]. Focus has been given to integrate earthworms into agriculture
managementinordertoincreasethecropyield[17]. However,culturalpracticesarewidelyrecognized
to affect earthworms in agricultural fields [18]. Tillage, crop type and pesticide inputs have been
demonstrated to affect earthworms in agroecosystems. Earthworms can serve as a tool reflecting
theenvironmentalimpactoftillageoperations,soilpollution,differentagriculturalinput,trampling,
industrial plant pollution, etc. [19]. Several studies have shown that earthworm abundance and
diversityarereducedinagriculturalfields,comparedtouncroppedsoils[4]. Significantlossofsoil
faunalbiodiversityorspeciesrichnesshasbeenfoundtoaccompanyconventionalagriculturalsystems
basedonintensivecultivation,highfertilizerinputsandcropmonoculture.
In terrestrial systems the majority of ecosystem services arise from soil functions that are
dependent to a greater or lesser extent on interactions between organisms, organic and mineral
fractionsofsoil[20]. Earthwormscomeintointeractionwithothersoilorganismsdirectlyorindirectly.
So,toinvestigatethepotentialoftheearthwormstointegrateintoagriculturemanagement,knowledge
on different physical, chemical, biological and management factors that affect the distribution
and abundance of earthworm population is important, which will help to identify the ecological
appropriatenessoftheearthwormsinordertosupplementtheirexistingpopulationandquantitythe
impactofearthwormsonagriculturalland[21]. Incorporatingthefunctionalrolesofearthworms
in agro-ecosystem management is key to sustainable agriculture. Earthworms have a potential to
contribute to the management of soil fertility for plant growth, enhanced farming efficiency and
agriculturalsustainability. Forthistoberealised,itisimportanttounderstandtherolestheyplayin
drivingsoilbasedprocesses,theirbiologyandecology[22].
The linkages between earthworm activity, biotic and abiotic factors, climate change and land
management practices are numerous, interrelated, and in many cases shape ecosystem service
provision. Here,wepresentasurveyofearthwormspeciesindifferentlymanagedarablesystemsand
permanentgrasslandsofSlovakiawiththefollowingobjectives;(1)torecorddifferentspeciespresent
invariousagroecosystems;(2)toevaluatevariationsofearthwormdensity,biomassproductivity,and
diversityinrelationtomanagement,abioticandbioticfactors;and(3)toevaluatetrophicinteractions
betweenearthwormsandarthropodsthatcanbeutilisedtoenhanceagriculturalsustainability.
2. MaterialsandMethods
2.1. StudyArea
Slovakia is a highly diversified country in respect to its natural environment. It is largely
located in the mountainous territory of the western Carpathian arch, which forms the boundary
betweenimportantphysicalandbio-geographiczonesandseveralmainEuropeanwatersheds. Only
a small part of Eastern Slovakia belongs to the eastern Carpathian region, and the southwestern
parttothePannonianbasin. Themountainregionscovermorethan55%ofthetotallandterritory.
Theclimateistemperatebutisinfluencedlocallybyelevationandtypeofrelief. Communitiesvary
fromthermophilousinthesouthernpartsofthecountry,tomountainousinthehigheraltitudes[23].
Sevenstudysiteswithtwodifferentlanduses(arableland—AL,andpermanentgrasslands—PG)
locatedindifferentnaturalconditionswereselected. OnlytheVOstudysitesituatedatDanubian
Uplandwiththemostproductivesoiltype(BlackChernozem)isusedonlyasarableland(Figure1,
Tables1and2).
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Study Geographical Soil Altitude
SSitteu dySite LocaGtieoLonog craatpiohnical SoSiol iTlyTpypee TeSTxoteuilxreture Altitu(dme)( m) LaLnadnd MMaannaaggeemmeenntt
AL-121 AL-intensive farming
NV NVEasternE SalsotevrankS UlopvalaknUdp land HuHmuimc RiceRgeogsooslo (lF(Fluluvviissooll)) ClaCyleayyey AL-121 AL-intensivefarming
PPGG-1-12323 PGPG-c-acatttltele ppaassttuurree
VO Danubian Upland Black CheBrlnacokzeCmhe r(Cnohzeermnozem) Loamy AL-137 AL-intensive farming
VO DanubianUpland Loamy AL-137 AL-intensivefarming
(Chernozem) AL-157 AL-intensive farming
DV Krupina Plain Humic Regosol (Fluvisol) Sandy-loam
APLG-1-15755 PAGL-a-ilnlutevnisailv mefeaarmdoinwg
DV KrupinaPlain HumicRegosol(Fluvisol) Sandy-loam
AL-Regosol (Regosol) Sandy PAGL-1-15557 ALP-Gin-atellnusviivalem faeramdoinwg
MJ Borská Lowland
PG-HuAmLi-cR Regeogsooslo(Rl e(Fgolusovli)sol) Sandy PG-160 PG-meadow
Sandy AL-157 AL-intensivefarming
MJ BorskáLowland PG-HumicRegosol AL-360 AL-extensive farming
KE Slovak Karst Eutric Cam(bFilsuovli s(oCl)ambisol) SaLnodaymy PG-160 PG-meadow
PG-344 PG-cattle pasture
KE SlovakKarst EutricCambisol(Cambisol) Loamy AALL-3-56095 ALA-Le-xetxetnenssivivee ffaarrmmiinngg
TA Kremnica Mountain Dystric Cambisol (Cambisol) Loamy PG-344 PG-cattlepasture
PG-597 PG-sheep pasture
TA KremnicaMountain DystricCambisol(Cambisol) Loamy AALL-5-99550 AALL--oerxgteannsiicv efaframrminingg
LT Low Tatras Regosol (Rendzina) Loamy PG-597 PG-sheeppasture
PG-931 PG-meadow
AL-950 AL-organicfarming
AbLbTreviations: NLVo,w NTaatcrainsa Ves; VO,R Vegoodsoelr(Radenyd;z DinaV), DvornLíkoyam; My J, Moravský Ján; KE, Kečovo; TA,
PG-931 PG-meadow
Tajov; LT, Liptovská Teplička; AL, arable land; PG, permanent grasslands.
Abbreviations:NV,NacinaVes;VO,Voderady;DV,Dvorníky;MJ,MoravskýJán;KE,Kecˇovo;TA,Tajov;LT,
LiptovskáTeplicˇka;AL,arableland;PG,permanentgrasslands.
Table 2. Climatic characteristics from the nearest meteorological stations.
Table2.Climaticcharacteristicsfromthenearestmeteorologicalstations.
Long-Term Two Months Average Long-Term Two Months
Study Meteorological
Average Air Air Temperature Average Rainfall before
Site Station Long-Term TwoMonthsAverage Long-Term TwoMonths
Study Meteorological Temperature (°C) before Sampling (°C) Rainfall (mm) Sampling (mm)
AverageAir AirTemperature Average Rainfallbefore
SiteNV MSticahtiaolnovce Tempera8t.u9 re(◦C) beforeSa4m.3p ling(◦C) Rain5f5a9l l(mm) Sam28p ling(mm)
VO Kráľová pri Senci 9.5 4.1 560 57
NVDV MiDchuadloinvccee 88..97 34..53 60565 9 67 28
VO Král’ovápriSenci 9.5 4.1 560 57
MJ Moravský Ján 9.2 4.1 525 53
DV Dudince 8.7 3.5 606 67
KE Rožňava 8.6 3.4 620 33
MJ MoravskýJán 9.2 4.1 525 53
TA Banská Bystrica 8.1 7.2 795 106
KE Rožnˇava 8.6 3.4 620 33
LT Poprad 6.2 4.7 950 41
TA BanskáBystrica 8.1 7.2 795 106
ALTbbreviationPso: pNraVd, Nacina Ves; V6O.2, Voderady; DV, Dv4o.7rníky; MJ, Moravs9k50ý Ján; KE, Kečov4o1; TA,
TaAjobvb;r eLvTia, tLioinpst:oNvsVk,áN TaceipnaličVkeas;. VO,Voderady;DV,Dvorníky;MJ,MoravskýJán;KE,Kecˇovo;TA,Tajov;LT,
LiptovskáTeplicˇka.
2.2. Methods
2.2. Methods
At each study site the biotic (earthworm density—ED, earthworm biomass—EB, earthworm
diverAsittye—acEhDsIt,u deyarsthitweothrme b isopteicci(eesa, rtahrwthorormpodde ndseintys—ityE—DA, Dea,r tahrwthorrompobdi obmioamssa—ssE—B,AeBa,r thgrwoournmd
dbeiveetlres idtye—nsEityD—I,GeBarDth, wanodr mcarsapbeidci edse,nasirttyh—roCpDod) adnedn asbitiyo—ticA pDa,raamrtehtreorsp o(sdoilb tioemmpasesr—atuArBe—, gSrTo,u snodil
bmeoeitsleturdee—nsSiMty—, aGndB Dpe,naentdratciaorna breidsisdtaenncseit—y—PRC) Dw)earen dmeaabsiuortiecd pfoarr atmweot elarnsd( suosiel cteamtepgoerraietsu r(ea—rabSlTe,
slaonildm—oAisLt uarned— pSeMrm,aannedntp gernaestsrlaatniodns—rePsGis)t awnicteh— thPeR s)itwe sepreecmifieca lsaunrde dmfaonratgwemoelnant.d use categories
(arabBleefloarned —theA Leaarnthdwpoerrmma ncoenlltecgtriaosns laanndds —traPpGs) winistthaltlhaetiosinte, smpeeacisfiucrelamnednmt aonf atgheem seonitl. physical
parameters was done in the same places where earthworms were collected. Soil temperature, soil
moisture and penetration resistance were measured at seven points on each site at the arable land
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Before the earthworm collection and traps installation, measurement of the soil physical
parameterswasdoneinthesameplaceswhereearthwormswerecollected. Soiltemperature, soil
moistureandpenetrationresistanceweremeasuredatsevenpointsoneachsiteatthearablelandand
permanentgrasslands.Soiltemperature(ST)wasmeasuredin◦Cat0.05(ST05)and0.20(ST20)mdepth
byinsertionofathermometerin◦C.Soilmoisturelevel(SM)wasmeasuredinsoilmoisturevolume
percentageat0.05(SM05)and0.20(SM20)mdepthusingasoilmoisturesensor(ThetaProbe,typeML2x:
Eijkelkamp Agrisearch Equipment, Giesbeek, The Netherlands, 2013) in the soil moisture volume
percentage. Penetrationresistance(PR)wasmeasuredwithanelectronicpenetrometer(Penetrologger,
6987EM:EijkelkampAgrisearchEquipment,Giesbeek,TheNetherlands,2013)withaconediameter
of1cm2anda60◦ topanglecone. ConeresistancewasrecordedinMPa.
Oneachsite1kgofsoilsamplesforchemicalanalysiswerecollectedfromfourpointsplacedat
theapicesofa10-msidesquare. Soilsampleswereairdried,homogenized,sievedthoungh2mm
sievesandanalysedforsoilpHinKCl,totaloxidizableorganiccarbon(TOC)accordingtoTjurin’s
method(amodificationofNikitin)[24],totalnitrogen(N)accordingtoamodifiedKjeldahlmethodin
t
accordancewiththeSlovakstandardizedmethod(STNISO11261),andavailablenutrients(P,K,Mg)
accordingtoMehlichIII[25]. Themeanvalueswereusedassoilchemicalstatuscharacteristics.
Earthwormsweresampledinsevenstudysites,insevenarablelandandsixgrasslands(atVO
study site the land is not used as permanent grasslands). Sampling was done in the spring 2015
(March–April) when earthworm populations are the most active. At each site, earthworms were
sampledbydiggingofsevenpitsof35×35cm2tothedepthof20cmplacedinalinewith3mdistance
betweenthepits. Soilfrompitwasreplacedonplasticbagandhandsorted. The earthwormswere
countedandcollected.Deeper-dwellingearthwormswereexpelledby1.5Lof0.2%formalin.Formalin
was applied directly to the holes. After a few minutes earthworms were collected. The collected
samples of earthworms were transported in glass cups with sufficient amount of soil in portable
fridge to the laboratory. The next day, the collected earthworms were washed, weighed, and
the sexual maturity and body colour were noted. The earthworm density and biomass from soil
monoliths were recalculated per square meter. Earthworms were sacrificed, fixed in 4% formalin
andmatureindividualsidentifiedbytheZajoncEarthwormkey[26]usingabinocularmicroscope.
Shannon-Wienerindex(H(cid:48))analysiswasperformedtodetermineameasureofestimateddiversity
withineachstudysite.
Soilarthropodsincludinggroundbeetlesandcarabidsweresampledinthesameplaceswhere
earthworms were collected. Seven plastic pitfall traps of 1.5 L volume were placed flush with
the surface. The traps were filled with 200 mL 4% formalin solution. After one month the traps
were collected. The captured individuals were counted, weighed, identified and preserved in
formalinsolution.
CorrelationanalysiswasconductedusingtheSpearman’sRankcorrelationcoefficientstoidentify
relationshipamongearthwormsandselectedsoilabioticandbioticfactors. Differencesbetweentwo
differentlandusesystems(AL,PG)weretestedbyapairedsamplestest. Thestatisticalanalysiswas
conductedusingthePASWStatisticssoftwareversion18.0(SPSSInc.,Chicago,IL,USA,2016).
3. ResultsandDiscussion
3.1. EarthwormBiomass,DensityandDiversityinDifferentlyManagedAgroecosystems
Intotal,1091earthwormsweresampledrepresentinganoverallbiomassof609.8g. Averagefresh
bodybiomassoftheearthwormsper1m2 rangedfrom0to66.4g·m−2 and28.2to134.5g·m−2 in
arablelandandpermanentgrasslands,respectively(Table3).
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Table3.Basicstatisticalcharacteristicsofearthwormfreshbiomassatsevenstudysitesunderdifferent
landusein2015(g·m−2).
AL PG
Study
Site Min Max Mean±SD Median Min Max Mean±SD Median
NV 0.0 101.6 40.8±31.10 32.6 64.8 235.6 134.5±57.49 132.7
VO 0.0 93.3 28.2±30.26 23.2 - - - -
DV 13.3 143.5 66.4±49.76 46.8 84.9 194.0 122.0±39.11 129.4
MJ 0.0 0.0 0.0 0.0 15.2 171.0 84.4±64.54 78.0
KE 42.7 90.4 63.3±17.82 58.3 7.3 188.5 67.8±63.42 51.4
TA 21.6 39.5 27.4±6.25 25.1 19.2 69.1 40.8±19.00 37.5
LT 0.0 21.39 7.23±8.35 2.12 8.7 49.8 28.2±16.35 28.8
Abbreviations: NV,NacinaVes; VO,Voderady; DV,Dvorníky; MJ,MoravskýJán; KE,Kecˇovo; TA,Tajov;
LT,LiptovskáTeplicˇka;AL,arableland;PG,permanentgrasslands.
Themeasuredmassvaluesindicatethefactthatearthwormsbelongtothelargestsoilmacrofauna
species and they are a major component of soil fauna communities in most ecosystems [27,28].
In temperate zones earthworm biomass often exceeds the biomass of all other soil biota having
majorimpactsonothersoilbiotaandsoilconditions[29].
Thedensityofearthwormsrangedfrom0to226.2ind·m−2andfrom74.6to277.6ind·m−2inAL
andPG,respectively(Table4).
Table4.Basicstatisticalcharacteristicsofearthwormdensityat7studysitesunderdifferentlanduse
in2015(ind·m−2).
AL PG
Study
Site Min Max Mean±SD Median Min Max Mean±SD Median
NV 0.0 57.1 29.2±17.54 24.5 114.3 261.2 197.1±53.20 220.4
VO 0.0 122.4 45.5±38.25 40.8 - - - -
DV 32.7 114.3 53.6±27.43 49.0 228.6 383.7 277.6±54.15 253.1
MJ 0.0 0.0 0.0 0.0 16.3 179.6 100.3±59.37 98.0
KE 146.9 351.0 226.2±69.54 195.9 32.7 146.9 84.0±48.23 65.3
TA 32.7 81.6 56.0±21.82 40.8 40.8 179.6 108.5±49.37 89.8
LT 0.0 57.14 20.99±18.77 24.49 16.3 163.3 74.6±50.86 65.3
Abbreviations: NV,NacinaVes; VO,Voderady; DV,Dvorníky; MJ,MoravskýJán; KE,Kecˇovo; TA,Tajov;
LT,LiptovskáTeplicˇka;AL,arableland;PG,permanentgrasslands.
Themaximumvalueof277.6individualsperm2wasmeasuredinpermanentgrasslandsattheDV
siteinFluvisol. Themajorityofindividualswerejuveniles(228.57ind·m−2ofjuveniles;47.72ind·m−2
ofmatures). Onaverage,thedensityofearthwormsperm2 wasnearlytwiceashighinpermanent
grasslands(120.3ind·m−2)comparedtoarableland(61.6ind·m−2).
AttheKEsitewemeasuredthesecondhighestdensityofindividualsperm2(226.2ind·m−2)in
extensivelymanagedarableland. AsattheDVsitejuvenilesdominatedthesamples(205.25ind·m−2
of juveniles; 21.00 ind·m−2 of matures). The high earthworm density at the KE site is probably a
consequenceofongoingerosionprocessesthataremoreintenseinarablelandthaninpermanent
grasslandswithpermanentvegetationcover. Thesamplingwasdoneonthebottomoftheslopewith
accumulatedfinematerialswithsuitablecontentoforganicmatter,nitrogenandothernutrientsthat
generategoodlivingconditionsforearthworms. ThefindingsfollowedsimilarpatternsasKanianska
etal. foundin2014[30].
Mean biomass of earthworms was also more than twice as high in permanent grasslands
(68.3 g·m−2)comparedtoarableland(33.3g·m−2).Thedifferencesbetweenarablelandandpermanent
grasslandsanalysedbyapairedsamplestestconfirmedsignificantdifferencesbetweentheearthworm
density and biomass in these two land uses. Results confirmed the opinion that the distribution
and biomass of earthworms in the soil depends on land use and management practices. Several
authors[31–33]foundearthwormstobemoreabundantandpopulationstohavegreaterbiomass
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underlong-termpasturethanunderlong-termcropping. Inaddition,inpermanentgrasslandswith
managedgrazing,positiveeffectsofcattleandsheepslurrymanureonearthwormpopulationswere
recordedinpermanentgrasslandsattheNVandtheTAsitessimilartostudiesofdeGoedeetal.[34],
Murchie et al. [35], and Pommeresche and Loes [36]. Significant loss of soil faunal abundance in
arablelandsisconnectedwithintensivecultivation[37],highfertilizerinputs,cropmonoculture,and
machinetrafficinarableland[38]. Inourstudythenumberofanecicearthwormswerealsoreduced
inintensivelymanagedstudysites.
Atotalof12specieswereidentifiedofwhich9werepresentinarablelandand11inpermanent
grasslands(Tables5and6). Thepercentageofjuvenileswithincommunitywasonlyslightlyhigherin
arableland(80%)thaninpermanentgrasslands(72.4%).
Table5.SummaryofthenumbersofearthwormsofeachspeciesandShannon-Wienerindexatseven
studysitesinarableland(ind·m−2).
NV VO DV MJ KE TA LT Total
Aporrectodeacaliginosa 7.00 5.83 1.17 0.00 11.70 0.00 2.30 27.99
Aporrectodearosea 3.50 1.17 1.17 0.00 0.00 0.00 2.33 8.16
Eiseniellatetraedra 0.00 1.17 0.00 0.00 1.17 0.00 0.00 2.33
Octolasioncyaneum 0.00 0.00 0.00 0.00 0.00 16.32 0.00 16.32
Octolasionlacteum 0.00 0.00 0.00 0.00 1.17 0.00 1.17 2.34
Sumofmatureendogeicspecies 10.50 8.17 2.34 0.00 14.04 16.32 5.80 57.17
%ofmatureendogeicspecies 64.30 22.26 70.01 0.00 66.86 77.79 99.49 66.23
Dendrobaenaoctaedra 0.00 1.17 0.00 0.00 7.00 0.00 0.00 8.17
Dendrodrilusrubidus 0.00 0.00 0.00 0.00 00.00 4.66 0.00 4.66
Lumbricusrubellus 0.00 2.33 1.17 0.00 0.00 0.00 0.00 3.50
Sumofmatureepigeicspecies 0.00 3.50 1.17 0.00 7.00 4.66 0.00 16.33
%ofmatureepigeicspecies 0.00 29.99 11.13 0.00 33.33 22.21 0.00 18.92
Lumbricusterrestris 5.83 0.00 7.00 0.00 0.00 0.00 0.00 12.83
Sumofmatureanecicspecies 5.83 0.00 7.00 0.00 0.00 0.00 0.00 12.83
%ofmatureanecicspecies 35.70 0.00 66.60 0.00 0.00 0.00 0.00 14.86
Sumofmaturespecies 16.33 11.67 10.51 0.00 21.00 20.98 5.83 86.30
Sumofjuveniles 12.83 33.82 43.15 0.00 205.25 34.99 15.16 345.20
Totalsum 29.16 45.49 53.65 0.00 226.25 55.97 20.99 431.50
H(cid:48) 1.50 1.90 1.36 0.00 1.41 0.79 1.52 2,72
Abbreviations:H(cid:48),Shannon-Wienerindex;NV,NacinaVes;VO,Voderady;DV,Dvorníky;MJ,MoravskýJán;
KE,Kecˇovo;TA,Tajov;LT,LiptovskáTeplicˇka.
Table 6. Summary of the numbers of earthworms of each species and Shannon-Wiener index at
sixstudysitesinpermanentgrasslands(ind·m−2).
NV DV MJ KE TA LT Total
Allolobophorachlorotica 3.50 1.17 0.00 0.00 0.00 0.00 4.66
Aporrectodeacaliginosa 39.65 30.32 48.98 13.99 23.32 3.50 159.77
Aporectodearosea 5.83 7.00 0.00 0.00 3.50 8.16 24.49
Eiseniellatetraedra 1.17 0.00 1.17 0.00 0.00 0.00 2.34
Octolasioncyaneum 0.00 0.00 0.00 0.00 1.17 4.66 5.83
Octolasionlacteum 0.00 0.00 0.00 0.00 0.00 2.33 2.33
Sumofmatureendogeicspecies 50.15 38.49 50.15 13.99 27.99 18.65 199.42
%ofmatureendogeicspecies 82.69 80.49 87.74 70.59 100.00 99.95 85.92
Dendrobaenaoctaedra 1.17 1.17 1.17 1.17 0.00 0.00 4.67
Lumbricuscastaneus 0.00 0.00 2.33 0.00 0.00 0.00 2.33
Lumbricusrubellus 0.00 2.33 1.17 0.00 0.00 0.00 3.50
Sumofmatureepigeicspecies 1.17 3.50 4.67 1.17 0.00 0.00 10.51
%ofmatureepigeicspecies 1.93 7.32 8.17 5.90 0.00 0.00 4.53
Aporrectodealonga 0.00 0.00 1.17 0.00 0.00 0.00 1.17
Lumbricusterrestris 9.33 5.83 1.17 4.66 0.00 0.00 20.99
Sumofmatureanecicspecies 9.33 5.83 1.17 4.66 0.00 0.00 20.99
%ofmatureanecicspecies 15.38 12.19 4.09 23.51 0.00 0.00 9.55
Sumofmaturespecies 60.65 47.82 57.16 19.82 27.99 18.66 232.08
Sumofjuveniles 136.44 228.57 43.15 64.14 80.47 55.98 608.75
Totalsum 197.09 276.39 100.31 83.96 108.45 74.64 840.83
H(cid:48) 1.04 1.24 0.85 1.08 0.80 1.85 1.42
Abbreviations: H(cid:48),Shannon-Wienerindex;NV,NacinaVes;DV,Dvorníky;MJ,MoravskýJán;KE,Kecˇovo;
TA,Tajov;LT,LiptovskáTeplicˇka.
Sustainability2016,8,906 7of14
Only one species, Aporrectodea caliginosa occur in abundance at all seven study sites and
was the most numerous species in both different land use sites. In permanent grasslands,
A. caliginosa represented 68.8% of identified specimens in the dataset, and 32.4% in arable land.
AporrectodearoseaandLumbricusterrestriswerefoundatfourofsevenstudysites. Octolasioncyaneum
and Octolasion lacteum were found abundant in arable land. Other species were found irregularly.
At the species level, our results are in line with the observations done of Zajonc [26,39] in
agro-climaticzonesofSlovakiainthe1970sand1980s. Themostabundantspeciesinourresearch,
Aporrectodeacaliginosa,belongstothequitecommonearthwormspeciesinEurope. Theassessment
of earthworm field studies from six different European countries revealed that endogeic species
Aporrectodea caliginosa, Aporrectodea rosea and Allolobophora chlorotica are the dominant ecological
group[40]. AporrectodeacaliginosawasconfirmedasthesecondmostnumerousspeciesinaBritish
earthwormdataset[41].
The overall effect of earthworms on soil processes varies with their ecological category
andspecies.Weidentifiedsixendogeic(Allolobophorachlorotica,Aporrectodeacaliginosa,Aporrectodearosea,
Eiseniella tetraedra, Octolasion cyaneum, and Octolasion lacteum), four epigeic (Dendrobaena octaedra,
Dendrodrilus rubidus, and Lumbricus castaneus, and Lumbricus rubellus), and two anecic
(Aporrectodea longa, Lumbricus terrestris) species. Endogeic species dominated in both land
usecategories. HigherendogeicspeciesabundancewasobservedinPG(85.9%)thaninAL(66.2%).
Epigeicspeciesrepresented4.5%and18.9%inpermanentgrasslandsandarableland,respectively.
Theanecicspeciesrepresented9.5%and14.9%inpermanentgrasslandsandarableland,respectively.
Thedistributionofthedifferentecologicalcategoriesofearthwormsinarablelandandpermanent
grasslandsshowedapreferenceofendogeicspecies,assoildwellerswithhorizontalburrows. These
wormsrarelycometothesurfaceincontrasttotheepigeicspeciesthatliveinthelitterandhumus
layersorcansometimespenetratealittledeeperintoloosemineralsoil(particularlyLumbricusrubellus).
Epigeicspeciesaresusceptibletosoilcultivation,sinceitdestroysthesuperficialsoillayer. Epigeic
speciesareassociatedwithsurfaceorganicmatterandmaybepresentinagriculturalsettingswhere
farming practices provide concentrations of organic materials e.g., animal faeces or crop residues.
Trueepigeicspeciesareoftenrareinnaturalsettings. Ingeneral,theyaremuchmoreabundantin
non-arablehabitatsthaninploughedones[42,43]. Sucheffectwereobservedinintensivelymanaged
arable land at the NV, the DV, the MJ sites where the epigeic group of earthworms was absent.
In addition, the numbers of endogeic species were higher in permanent grasslands comparing to
arableland. Similarly,thedeep-burrowingearthworms(LumbricusterrestrisandAporrectodealonga),
whichcollectfoodfromthesoilsurface,isadverselyaffectedbyheavysoilcultivationthatdestroysits
burrowsystemandreducesfoodsources[44]. Overall,Aporrectodealongawasnotfoundinarableland
ThehighestearthwormdiversitywasfoundattheVOsite(H(cid:48) =1.90)amongarablelandstudy
sites,andattheLT(H(cid:48)=1.85)amongpermanentgrasslandsstudysites(Tables5and6).Althoughmany
authorsarguethatpermanentgrasslandshavethegreatestspeciesdiversityofearthworms[45,46]we
confirmedthestatementinonlythreestudysites(MJ,TA,LT).
3.2. EarthwormsinRelationtoSoilTypeandSoilChemicalProperties
Earthwormabundanceanddiversityisaffectednotonlybymanagementpracticesbutisalso
influenced by abiotic and biotic factors. Soil types have an impact on soil biota. We found no
earthworms at the MJ study site in Regosol used as arable land situated in a region with low
precipitation and high temperature. Regosol used as arable land had unfavourable soil chemical
andphysicalproperties. Itstextureissandy,andcoarsesandcanbeanegativefactorforearthworms
eitherbecauseoftheabrasiveactionofsandgrainsthatdamagesearthwormskinorbecausethissoil
retainslesswater[47].
Generally,theabundanceofspeciesreflectstheirpreferencetositespecificconditions. O.lacteum
preferssoilswhicharerichincalcium[39]. ThereforeO.lacteumwasfoundinRendzina,shallowsoil
developedonlimestonerockattheLTsite. E.tetraedraassemi-aquaticspecies[48]withaffinityfor
Sustainability2016,8,906 8of14
moistconditions[49],wasfoundmoreabundantinFluvisol. Inourresearchweobservedthehigher
earthwormabundanceandbiomassinFluvisols,soiltypesdevelopedinalluvialzones.
Sevenstudysitesdifferinsoilchemicalproperties(Tables7and8). Inarableland,soilreactionat
theVOandLTisneutral,attheDVweaklyacidic,attheNVandKEacidic,andattheTAstrongly
acidic. Inpermanentgrasslands,soilreactionattheNV,MJandLTisneutral,attheKEweaklyacidic,
attheDVstrongacidic,andattheTAextremelyacidic. Contentoftotalorganiccarbonismedium,
high,veryhigh,andonlyattheMJisitverylow. Contentofavailablephosphorousisverylowand
lowatallstudysites. Incontrast,contentofavailablemagnesiumismedium,highandveryhighatall
studysiteswiththeexceptionoftheMJ.Contentofavailablepotassiumvaries,andlowcontentwas
recordedattheNVinAL,MJ,andTAinPG.
Table7.Soilchemicalparametersat7studysitesinarableland.
pHKCl TOC(g·kg−1) Nt(g·kg−1) P(mg·kg−1) K(mg·kg−1) Mg(mg·kg−1)
NV 5.51 16.67 2.51 10.16 245.59 672.27
VO 7.18 15.89 1.99 18.74 256.53 762.78
DV 6.04 13.54 1.61 48.35 310.84 318.49
MJ 4.58 7.43 0.96 65.77 132.16 39.32
KE 5.46 13.09 1.58 4.84 221.93 184.84
TA 4.84 15.45 1.62 33.56 221.90 127.36
LT 6.70 34.00 3.05 38.23 199.36 949.12
Abbreviations: NV,NacinaVes; VO,Voderady; DV,Dvorníky; MJ,MoravskýJán; KE,Kecˇovo; TA,Tajov;
LT,LiptovskáTeplicˇka;TOC,totalorganiccarbon;Nt,totalnitrogen;P,availablephosphorus;K,available
potassium;Mg,availablemagnesium.
Table8.Soilchemicalparametersat6studysitesinpermanentgrasslands.
pHKCl TOC(g·kg−1) Nt(g·kg−1) P(mg·kg−1) K(mg·kg−1) Mg(mg·kg−1)
NV 7.18 23.18 2.78 14.52 293.56 721.78
DV 5.08 13.88 1.91 3.02 140.20 466.68
MJ 6.75 4.80 1.02 31.42 82.33 113.11
KE 5.89 28.20 3.13 22.83 349.30 260.85
TA 4.19 42.30 4.14 0.52 136.22 631.80
LT 6.94 51.30 5.16 3.82 300.33 1233.15
Abbreviations: NV,NacinaVes; DV,Dvorníky; MJ,MoravskýJán; KE,Kecˇovo; TA,Tajov; LT,Liptovská
Teplicˇka;TOC,totalorganiccarbon;Nt,totalnitrogen;P,availablephosphorus;K,availablepotassium;Mg,
availablemagnesium.
Inpermanentgrasslands,therewasnocorrelationbetweenearthwormcharacteristics(earthworm
density,biomass,anddiversity)andsoilchemicalparameters(Table9). Inarableland,wefounda
positivecorrelationbetweenearthwormbiomassandavailablepotassium. Theavailablenutrients
are supportive not only for plants but also for soil edaphon biomass. In contrast, nutrients and
their availability are influenced by soil fauna. Zhu et al. [50] found that earthworms can activate
andtransformKintoeffectiveKthatismorereadilytakenupbyplantsthroughfeeding,digestion,
absorption,andexcretion. EarthwormdiversitywaspositivelycorrelatedwithMgandpHinarable
land(Table9).
Sustainability2016,8,906 9of14
Table9.ResultsofaSpearman’scorrelationanalysisforearthwormdensity,biomass,diversityand
selectedsoil,climaticandgeographicparameters(n=7forAL,n=6forPG).
AL PG
ED EB H(cid:48) ED EB EH(cid:48)
pH −0.036 0.286 0.893** −0.257 0.257 −0.200
TOC −0.214 −0.071 0.750 −0.543 −0.771 −0.029
Nt −0.214 −0.071 0.750 −0.543 −0.771 −0.029
P −0.571 −0.464 −0.500 −0.371 0.257 0.371
K 0.464 0.857* 0.393 −0.429 −0.200 −0.429
Mg −0.179 0.143 0.929** −0.086 −0.257 −0.486
**Correlationissignificantatthe0.01level;*Correlationissignificantatthe0.05level;Abbreviations: ED,
earthwormdensity;EB,earthwormbiomass;H(cid:48),Shannon-Wienerindex;TOC,totalorganiccarbon;Nt,total
nitrogen;P,availablephosphorus;K,availablepotassium;Mg,availablemagnesium;AL,arableland;PG,
permanentgrasslands.
3.3. EarthwormsinRelationtoClimateRelatedandPhysicalSoilParameters
Observationofrelationshipsbetweenbioticandclimaterelatedsoilparametersareveryimportant
becauserapidclimatechangesmakeitunlikelythatearthwormcommunitiesandtheirecosystem
serviceswillsurviveinthecurrentform,becausetheenvironmentalfiltersmaychangefasterthan
wormscanrespond[51].
The development of the present ecosystems in the postglacial period (Holocene) depended
on significant changes in climate, on the distance of refuges in which organisms could survive
unfavourableconditionsoftheglacialperiod,andonthenatureanddevelopmentofsoils. Glacial
periodsintheCarpathianscausedthelocalextinctionofmanylivingforms.Warminginthepost-glacial
period,about10,000yearsago,createdconditionsthatfacilitatedmigrationofindividualspeciesfrom
their refuges (dominantly in southern Europe), where they were protected during glacial periods.
Aftertheneoliticrevolution,humansocietybegantoinfluencemorenoticeablythedevelopmentof
naturalecosystemsinthelowerwarmeraltitudesofCentralEurope. Duringtheformationperiodof
neoliticagriculture,theCarpathianswerealmostcompletelycoveredbyforests. Onlyhigh-montane
andalpinerockylocalitieswerewithoutforestcover—i.e.,rockywalls,avalancheslopes,andnarrow
beltsofsomeriverbanks[52].
Anthropogenicchangesrelevanttoearthwormcommunitiesincludehabitatalteration,invasive
species,andclimatechange. Disturbanceintensityandfrequencyareimportantvariablesforboth
extinctionofendemicsandcolonizationbyinvasivespecies[53]. Climatechangeeffectsonearthworm
communitieshavenotbeencloselyexploredwithexperimentalprocedures. Distributionaldatain
temperatezonesindicateastronginfluenceofglaciationhistoryonmoderndistributions,andavery
slowreboundfromrefugiatodeglaciatedland,whereinvasivespeciesnowdominate[54]. Underthe
conservativeestimatesofclimatechange,thefutureofearthwormecosystemservicesmaydependon
invasivespecies,andtopographicallysimpleregions. Otherwise,medium-termevolutionarychange
maybetheonlyresponsemechanismavailabletoearthworms[55].
Inrelationtoclimate,climaticfactorsreflectedinsoilmoistureandtemperatureareconsideredto
betheprimaryfactorslimitingsurvivalofearthworms[56,57]. Soiltemperatureandmoisturevaried
amongthestudysitesindifferentsoildepthsinarablelandandpermanentgrasslands(Table10).
Inarableland, earthwormdensityandbiomasswerepositivelycorrelatedwithsoilmoisture.
Inpermanentgrasslandswithsignificantlyhighermoisturecontentvalues(Table10),temperature
becamealimitingfactorsaffectingearthwormdensityandbiomass,whichisreflectedinsignificant
positivecorrelation(Table11).
Sustainability2016,8,906 10of14
Table10. Meansoiltemperatureandsoilmoistureatsevenstudysitesunderdifferentlandusein
2015(◦C,%).
SoilTemperature(◦C) SoilMoisture(%)
Study
AL PG AL PG
Site
5cm 20cm 5cm 20cm 5cm 20cm 5cm 20cm
NV 10.4 5.2 7.7 5.2 10.4 27.0 23.0 22.9
VO 9.1 6.2 - - 21.1 20.6 - -
DV 8.9 7.9 7.9 7.7 39.0 31.9 47.6 29.9
MJ 7.4 5.6 7.9 5.2 12.9 13.3 34.9 35.3
KE 6.0 4.1 7.2 5.1 22.0 19.7 35.3 18.6
TA 5.0 6.9 6.9 6.6 12.4 30.7 34.7 33.0
LT 4.6 4.3 4.3 4.4 22.7 - 40.4 16.4
Abbreviations:NV,NacinaVes;VO,Voderady;DV,Dvorníky;MJ,MoravskýJán;KE,Kecˇovo;TA,Tajov;LT,
LiptovskáTeplicˇka;AL,arableland;PG,permanentgrasslands.
Table11.Spearman’sRankcorrelationcoefficients(n=49forAL,n=42forPG)forearthwormdensity,
biomassandselectedabioticandbioticparameters.
AL PG
ED EB ED EB
ST05 −0.118 0.185 0.371* 0.457**
ST20 −0.055 0.034 0.481** 0.309*
SM05 0.309* 0.242 0.107 −0.113
SM20 0.387** 0.528** 0.250 0.225
PR80 −0.137 −0.307* 0.133 0.072
** Correlation is significant at the 0.01 level; * Correlation is significant at the 0.05 level; Abbreviations:
ED,earthwormdensity;EB,earthwormbiomass;ST05,soiltemperaturein5cmdepth;ST20,soiltemperature
in20cmdepth;SM05,soilmoisturein5cmdepth;SM20,soilmoisturein20cmdepth;PR80,penetration
resistancein80cmdepth;AL,arableland;PG,permanentgrasslands.
Anegativecorrelationratewasmeasuredbetweenpenetrationresistanceandearthwormbiomass
inarablelandconfirmingthenegativeeffectofsoilcompactiononearthworms. Theresultsareinline
withotherstudiesthatfoundareductioninearthwormpopulationsasaresultofsoilcompactionin
arableland[58,59].
3.4. EarthwormsinRelationtoArthropods
We observed relationships between earthworms, arthropods, ground beetles and carabids
(phylumArthropoda,orderColeoptera,familyCarabidae). Atotalof3849arthropodindividualswere
trappedrepresentinganoverallbiomassof302.3g. Thenumbersofarthropods,groundbeetlesand
carabidsvariedbetweenstudysiteswithdifferentlandmanagementpractices(Table12).
On average, the number of arthropods was roughly twice as high in permanent grasslands
comparedtointensivelymanagedarableland(NV,DV,andMJ)includingextensivelymanagedarable
landattheKE.OrderColeopterabelongedtothedominantordersatallstudysites.
ThehighestnumberofcarabidswascountedattheLTstudysiteinorganicallymanagedarable
land. Carabidrecruitmentisenhancedbyproperorganicfertilizationandgreenmanuring[60]applied
attheLTstudysite. ThesecondhighestnumberwasrecordedagaininarablelandattheTA,study
site with extensive land use management, located in mountain area surrounded by pastures and
forests. Theresultssuggestthatlanduseandmanagementdeterminethearthropods’assemblages.
Regardingtotheeffectofmanagementonsoilarthropodstherearedifferentresearchresults. Many
studiesreportedthatextensiveororganicmanagementhaspositiveeffectsonbiodiversity[61],but
these effects differed between species groups and spatial scales [62]. Attwood et al. [63] observed
significantlyhigherarthropodrichnessinareasoflessintensivelanduse. Therearealsoauthorswho