AppliedSoilEcology29(2005)259–273 www.elsevier.com/locate/apsoil Relative effects of biotic and abiotic factors on the composition of soil invertebrate communities in an Amazonian savanna E. Franklina,*, W.E. Magnussonb, F.J. Luizaõb aNationalInstituteforAmazonResearch(INPA),DepartmentofEntomology(CPEN),CP478,69011-970Manaus,AM,Brazil bDepartmentofEcology(CPEC),CP478,69011-970Manaus,AM,Brazil Received13July2003;accepted13December2004 Abstract Usingordinationstechniques,weinvestigatedtheeffectsofdifferenttypesofplantcoverontherelationshipbetweensoil structureandinvertebratecommunitiesinanAmazoniansavanna.Vegetationislandswerechosenwherefourselectedshrubs specieswerepresentonsandyandclayeysoils.Foreachsampleunderaselectedshrubwithintheclump,anothersamplewas taken in thegrass-tuft and extracted in Berlese-Tullgren. Classifying at higher taxonomic levels, we detected 27 zoological categories.Themeannumberofindividualswasgenerallyhigheronshrubs.AcariandCollembolawerethedominantgroups. Non-Oribatid mites dominated in the savanna, in contrary with what occurs in most Amazonian ecosystems, where the dominanceofOribatidaisalwayshigherthanothersAcari.Theleveloftaxonomicresolutionutilizedwassufficienttoshowthe maindifferencesofthespatialvariationincommunitystructure.Wedetectedeffectsofsoiltype,vegetationstructureandplant specieidentityonthecompositionofthecommunities.Themesofaunahaveamosaicdistributioninthesavannadependenton thesoil-foodwebstructureofthevegetation.Shrubsandgrass-tuftgeneratedifferentecosystems.Therefore,studieswithbetter taxonomicresolution will benecessary toassess the magnitudeoftheeffect of bioticandabiotic factors. #2005Elsevier B.V.Allrights reserved. Keywords: Amazoniansavanna;Soilinvertebrate;Habitatspecificity;Edaphicfactors;Vegetationstructure 1. Introduction theirassemblageintheprofile(Barrosetal.,2004).It is to be expected that soils of different structure and In Amazonia, edaphic organisms such as inverte- vegetational cover will harbor different communities brates,roots,andmicrofloraplayanimportant,ifnot ofsoilinvertebrates(Abbottetal.,1979;Majer,1989). predominant,roleinsoilstructuralorganization,both However, it is time consuming and expensive to by forming and destroying aggregates and altering identify these invertebrates to specie level. The proportionof‘morphospecies’thatcannotbeassigned tonamed species and the number of ‘scientist-hours’ * Correspondingauthor.Tel.:+55926433196; requiredtoprocesssamplesbothincreasedramatically fax:+55926431838. E-mailaddress:beth@inpa.gov.br(E.Franklin). for smaller-bodied taxa (Lawton et al., 1998), that 0929-1393/$–seefrontmatter#2005ElsevierB.V.Allrightsreserved. doi:10.1016/j.apsoil.2004.12.004 260 E.Franklinetal./AppliedSoilEcology29(2005)259–273 composethemajorityofthesoilmesofaunagroups.In structure,waterrelationshipandnutrientretentionand a complex and poorly studied region, such as availability (Brady, 1989). Two types of soil occur Amazonia, even groups that are widely used in within the savanna at Alter do Chaõ. The most environmental studies (e.g. Oligochaeta, ants and commonisaloosesandysoil,withyellowishsurface termites) are far from being taxonomically well that becomes darker with depth. However, nearby a known. lesssandyanddarkersoilcanbefoundamoreclayey The concept of taxonomic sufficiency (TS; Ellis, and compact soil. However, the vegetation cover is 1985),involvestheidentificationoforganismsonlyto broadlysimilarandmanyshrubspeciesoccuronboth aleveloftaxonomicresolutionsufficienttosatisfythe types of soil. It is not clear to what extent the objective of a study (Pik et al., 1999; Terlizzi et al., vegetationcovercanmodifytheeffectsofthemineral 2003). Unfortunately, taxonomic sufficiency for fraction of the soil on invertebrate communities. detecting habitat-related changes in invertebrate We initially investigate the effects of vegetation communities in Amazonia is unknown. Most studies type (shrubs or grass-tuft) and soil type (clayey and have used classification at the levelof class, order or sandy)onthestructureoftheinvertebratecommunity. family (e.g.: Adis et al., 1987; Adis, 1988; Oliveira We then test for differences among species of shrubs and Franklin, 1993; Vohland and Schroth, 1999; fortheireffectsonmesofaunacommunitiesunderthe Franklin et al., 2001). Within pure taxonomic levels, shrubs and in the surrounding grass-tuft matrix. For zoologicalcomponentscanbeseparatedaccordingto biological reasons, and consideration of previous stage of development (adult/immature) or the main studies, it is unlikely that any of the hypotheses we feedinghabitoftheindividuals(Mooreetal.,1988).In present here are false. That is, soil type, vegetation Amazonian ecosystems, several studies have used structure, and vegetation species composition almost functional zoological groups (e.g. Franklin et al., certainly affect the invertebrate community to some 2001;Ho¨feretal.,2001;Barrosetal.,2002,2004)to extent. However, the relative magnitude of these investigate factors affecting the distribution of soil effectsisunclearanditisnotknowntowhatextentthe invertebrates.InWesternAmazonia,thereisevidence bioticfactorscancompensateforvariationinmineral that soil macrofauna classified at higher taxonomic soil structure. Management of savanna areas usually level, and using principal components analysis, can implies management of vegetation structure and show effects of land-use (Barros et al., 2002). composition, but it is unclear whether management Weusedthenaturalvariationinsoilandplantcover practicesdesignedtomaintaintheconservationvalue inanAmazoniansavannatoinvestigatetheeffectsof of the vegetation would be of equal benefit to the different types of plant cover on the relationship invertebratecommunity(Sandersonetal.,1995).Ifthe between mineral soil structure and invertebrate taxonomic resolution used in most studies in community composition. We also investigated Amazonia is not sufficient to detect natural variation whether soil invertebrates at the savanna show insoilinvertebrate’scommunities,itisunlikelytobe consistent pattern in distribution when analyzed at adequate to detect subtle effects caused by human highlevelsoftaxonomicsufficiency.TheAmazonian- interventions. type savannas (Huber, 1982) of northern Brazil have Weusedordinationtechniquestolocatezoological lowfloristicdiversity(Miranda,1993,1995)andmost categoriesinmultivariatespacebasedonsimilaritiesin of them are burned frequently at the end of the dry their occupation of sites. If organisms in different season(September–October).Thisaffectsthefloristic categoriesdonotdifferinspatialdistribution,theywill diversity and composition of the ecosystem, because be poor indicators of spatial variation in community grasses and shrubs form functional groups that differ structure.Weidentifiedtheinvertebratesintaxonomi- in their responses to external factors such as fire callevelsofclass,sub-class,order,sub-orderorfamily, (Ginoux et al., 1996; Jeltsch et al., 1998). These and then in zoological categories, according to their groups also differ in their effects on soil structures, main feeding habit and/or stage of development. We principallybecauseofdifferencesininputsoforganic divided the zoological categories in two groups: all- matter. Soil percent material may also affect vegeta- invertebrate community and non-mite, non-collembo- tionstructure.Sandyandclayeysoilsdiffersharplyin laninvertebratecommunity.Wehypothesizedthat:(1) E.Franklinetal./AppliedSoilEcology29(2005)259–273 261 thesoiltypeaffectsthemesofaunacommunities;(2)the detectedundershrubs(2.5(cid:2)0.2,n=3)inrelationto mesofauna communities under shrubs are different grass-tuft (1.6(cid:2)0.7, n=5). These difference were fromthoseundergrass-tuft;(3)thespeciesoftheshrub significant at 5% two sample t-test (p=0.003 and affects the invertebrate communities, and this effect p=0.042, respectively). Under loose sandy soil, the could override differences due to mineral soil; (4) claypercentageundershrubs(6.2(cid:2)1.7,n=4)didnot taxonomicresolutioninhigherzoologicalcategoriesis differ from the value obtained under grass-tuft sufficienttodetectchangesinsoilinvertebratesdueto (4.3(cid:2)1.2, n=4). No difference was detected naturalvariationinsoilandvegetationstructure. comparing the value for C concentration (1.9(cid:2)0.6, n=4undershrubs;1.8(cid:2)0.4,n=4undergrass-tuft). Thesamplesweretakenbetween28and30August 2. Methods 1996,duringthedryseason.Ateachsavannasite,on sandy and clayey soils, we chose those vegetation The study was carried out in two savanna sites, islands where four shrubs species [Myrcia sylvatica separated from each other by 1km, one with sandy (Meyer)DC,Miconiaalbicans(Sw.)Triana,Manihot soilandtheotherwithclayeysoil,situatedontheright caerulenscens Pohl subsp. Paraensis (Mueller von marginoftheTapajo´sriver,nearthevillageofAlterdo Argau) Rogers & App and Chomelia ribesioides Chaõ(28310Sand558000W),inthestateofPara´.The Benth. Ex M. Arg.] were present. Twelve shrubs on climate is Ami (tropical wet) in the Ko¨ppen each soil type were sampled, giving three repetitions classification, with a well-defined dry season, mean for each shrub species on each soil, totalizing 24 annual rainfall of 1950mm, with 75% of the rain samples under shrubs. For each sample under a falling between December and June. The dry season selected shrub within the clump, another samplewas extends from June to December. The mean annual taken outside the clump, in the grass-tuft matrix, temperature is 27.78C and the mean monthly totalizing 24 samples under grass-tuft. Samples were temperature varies less than 1.58C from the annual taken using a 49cm2 metal corer, introduced to a mean (Miranda, 1993). depthof5cmintothesoil.Thesampledareacovered Thevegetation inthe areas surveyedisdominated at each shrub and each grass-tuft was 0.0025m2. byanherbaceousstratumcomposedprincipallyofthe In the same day as collection, the samples were tufts forming grasses Paspalum carinatum and prepared for extraction with Berlese-Tullgren extrac- Trachypogon plumosus, interspersed with patches of tor, in a local laboratory. We used 1% formaldehyde trees and shrubs. Regular semi-annual burning can solution as a collector liquid. The samples were drastically reduce the area covered by the common extracted during 6–7 days, during which time the shrub speciesofthegenera MiconiaandMyrcia,and temperatureoftheextractorwasraisedslowlyfrom28 theareamadeavailablebythelossoftheshrubsmay to 458C. be occupied mainly by the grass P. carinatum Weidentifiedtheinvertebratesintaxonomiclevels (SanaiottiandMagnusson,1995).Thestatureoftrees of class, sub-class, order, sub-order or family. Our is short, and many have tortuous trunks, thick cortex method was not efficient at catching Nematoda, and leathery leaves. Trees do not form a continuous Enchytraeidae (microfauna) and invertebrates larger canopy and, in the area we studied, the vegetation is than2mm(macrofauna),andthesewerenotincluded groupedintowell-definedclumps,consistingoftrees, inanalyses.Withintaxonomiclevels,weclassifiedthe shrubs or herbs. Tracts of grass, dominated by P. individuals in zoological groups, according to their carinatum mixed with sedges and other herbaceous mainfeedinghabitand/orstageofdevelopment(adult/ plants, occur between clumps of shrubs (Miranda, immature). Acari was separated into zoological 1993). groups of Oribatida (80–85% detritivorous species), Soil characteristics differed sharply under shrubs and Acari Non-Oribatida, the majority being pre- andgrasstuftsintheclayeybutnotintheloosesandy dators. Diptera, Coleoptera, Homoptera, Hemiptera soil.Underclayeysoil,theclaycontentundershrubs and Thysanoptera were separated into adults and (17.7(cid:2)2.1, n=3) was higher than under grass-tuft immatures,becauseofthegreatdifferencesinfeeding (5.9(cid:2)1.4, n=5). A higher C concentration was habits. Hymenoptera were separated into ants and 262 E.Franklinetal./AppliedSoilEcology29(2005)259–273 other groups. Twenty-seven faunal community vari- samples under shrubs and grasses together, and then ables (zoological categories) were found. separatelytoinvestigatetheeffectsofshrubtype.We Weusedordinationtosummarizethemajorpattern used MANOVA totestfor the effects of (1) soil type in the data. Ordinations were undertaken in the non- (clayeyor sandy), (2) structure of thevegetation (the metric hybrid multidimensional scaling (SSH-MDS) environmentundershrubsclumps,orundergrass-tuft) module of the PATN Program (Belbin, 1992). The and (3) shrub species (M. sylvatica, M. albicans, M. apriori decision was made to use two dimensions caerulescens and C. ribesioides). It is probable that (SSH1 and SSH2), to capture the major gradients. anychangewillhavesomeeffectonsomeinvertebrate Minorpatternsmayexistinotherdimensions,butthey species. We investigated only the effects of the aredifficulttointerpret(Gauch,1982),andwedidnot independent variables on the major patterns of the have sufficient repetitions to justify such analysis. community, that is, those captured by the two Theordinationswereundertakenforquantitativeand dimensions of the ordination. forqualitative(presence/absence)data.Thequantitative dataweretransformedbydividingtaxonomicgroupsby the sum of squares to balance the contribution ofrare 3. Results and common taxa. Data in sites were divided by site totalstogivethesameweighttoeachsite.Wemadethe 3.1. The invertebrate fauna of the savannas ordinationsfortwogroupings:all-invertebratecommunity and, the non-mite, non-collembolan invertebrate Twenty-sevenzoological categories were detected community. The ordinations based on qualitative data in both savannas. Chilopoda, adults Homoptera, and (presence/absence) give more weight to uncommon Phalangida were not found in the savanna on clayey species, as common species tended to occur in most soil. Immatures and adults Diptera, immatures sites, and therefore contributed little to qualitative Lepidoptera, Pauropoda, Symphyla, and immatures differences among sites. The Bray Curtis Association Thysanopterawerenotfoundinthesavannaonsandy Indexwasusedtoindicatethedissimilaritybetweenthe soil. The mean number of individuals was generally samples. When used on presence/absence data, this higher on shrubs (28.3–240.3 individuals) than on association is called the Sorensen index. Ordination grass-tufts (9.0–106.3 individuals). with MDS and the Bray Curtis distance is generally The highest invertebrate density was detected effectiveatdetectingecologicalgradients(Kenckeland underM.sylvaticashrubs,causedbythehighdensity Orloci,1986;Minchin,1987).TheMDSaxesarelinear of Acari Oribatida, resulting from a great dominance andapproximatelyorthogonalandthereforeconformto of Rostrozetes foveolatus Sellnick, 1925, in both soil the principal assumptions of multivariate analysis of types. Acari Oribatida, Acari Non-Oribatida and variance(AndersonandLegendre,1999). Collembolaweredominantinallofthesitessampled, Ameasureof‘stress’andr2statisticwascalculated. representing more than 60% in relation to the total Stressisamismatchbetweentherankorderofdistances invertebratefauna.Inthesavanna,greatestdominance in the data, and the rank order of distances in the ofAcariNon-Oribatidawascharacteristicofthegrass ordination(thehigherthevalue,closeraretheimplied cover and of the schrubs, with exception of C. ultrametric-distancesfromthedendrogramtotheinput ribesioides on the clayey and sandy soil, and M. association measure). The r2 statistic is descriptive of silvatica on sandy soil. Collembola was more theproportionofthevarianceintheoriginaldistances dominant in the savanna on clayey soil capturedbytheordinationandisgenerallycomparable (Appendix A; Table 1). For simple comparison, the among analyses, though it may slightlyunderestimate results for a primaryforest were included in Table 1. theeffectivenessoftheMDS,whichdoesnotrequirea linear relationship between the input and output 3.2. All-invertebrate community—soil, shrub species distances. and vegetation structure Ordinations summarize the major pattern in the data and may not capture patterns in subgroups well. Multivariate multiple regression for quantitative Therefore, we conducted ordinations of sites for dataindicatednostatisticallysignificanteffectofsoil E.Franklinetal./AppliedSoilEcology29(2005)259–273 263 Table1 RelativedominanceofAcariOribatida,AcariNon-Oribatida,Collembola,andnon-mite,non-collembolaninvertebratesinrelationtothetotal catchinthesoilandlitterlayersofaprimaryforestandAmazonian-typesavannaareasofAlterdoChaõ.Para´.Brazil Acari Collembola Non-mite,non-collembolan invertebrates Oribatida Non-Oribatida Primaryforest(clayeysoil) 58 20 2.4 19.6 Savanna(clayeysoil) M.sylvatica S 26 63 3 8 G 27 61 0.3 11.7 M.albicans S 27 43 9 21 G 35 53 0 12 M.caerulenscens S 30 49 3 18 G 32 55 0.5 12.5 C.ribesioides S 45 44 1 10 G 14 82 0 4 Savanna(sandysoil) M.sylvatica S 55 14 16 15 G 23 33 6 38 M.albicans S 30 51 10 9 G 17 59 0 24 M.caerulenscens S 29 34 15 22 G 17 69 2 12 C.ribesioides S 44 35 10 11 G 18 65 5 12 S=shrub;G=grass-tuft. (Pillai trace=0.059; P=0.312) or shrub species vegetation (Fig. 2). One group consists of generalists, (Pillai trace=0.211; P=0.178). However, commu- such as Acari Non-Oribatida, Acari Oribatida and nity was affected by the structure of the vegetation immatures Homoptera, which occurred under both (MANOVA; Pillai trace=0.422; P=0.000). The shrubs and grass-tuft. Some small groups, such as variationwasprincipallyontheMDSaxis1(ANOVA, PsocopteraandimmaturesDipteragroupedtothelower P<0.001). The all-invertebrate community under leftofFig.2,occurredmainlyundergrass-tuft.Taxain shrubswasdistinctfromthatinthegrass-tuft matrix. theupperrightofFig.2,suchasAraneae,Coleoptera The ordination (stress: 0.238, r2=0.856) showed the immatures, Diplura, Pseudoscorpionida, Collembola, separation of the samples into shrub and grass-tuft adults Coleoptera, Isopoda and Protura, occurred communities (Fig. 1A). mainly under shrubs. Other taxa were rare and no Multivariate multiple regression for qualitative associationwithvegetationcovercanbeinferred. dataindicatednostatisticallysignificanteffectofsoil (Pillai trace=0.934; P=0.275) or shrub species 3.3. All-invertebrate community under shrubs—soil (Pillai trace=0.160; P=0.354). However, the com- and shrub species munitywasaffectedbythestructureofthevegetation (MANOVA; Pillai trace=0.355; P=0.000). The Multivariate multiple regression for quantitative variation was principally on axis 2 (ANOVA, data indicated no statistically significant effect of P<0.000). The ordination (Fig. 1B; stress: 0.267, shrub specie (Pillai trace=0.294; P=0.386). How- r2=0.783) indicated significant separation of the ever, the community was affected by the soil type samples into shrub and grass-tuft communities. (MANOVA; Pillai trace=0.296; P=0.043). The Plots of relative frequency of the zoological variationwasprincipallyontheMDSaxis1(ANOVA, categories of invertebrates against the sampling sites P<0.015).Theordination(stress:0.214;r2=0.888) (24 under shrubs and 24 under grass-tuft) reflect showsclearseparationofthesamplesfromclayeyand different groups according to the structure of the sandy soils (Fig. 3). 264 E.Franklinetal./AppliedSoilEcology29(2005)259–273 Fig.2. Upperpanelindicateswhetherthesamplewastakenunder shrubs (solid bars) or under grass tufts (open bars). Gray bars indicatetherelativefrequencyofeachzoologicalcategorywithin Fig.1. Ordinationintwodimensionsbyhybridmultidimensional all-invertebratecommunity.Sitesareorderedbytheirpositionon scaling(SSH)ofthetotalinvertebratecommunitycollectedunder axis1ofanMDSordination(seetext). shrubandgrassfor(A)quantitativedata,and(B)qualitativedata. S=shrub,G=grasstufts. group, in the upper right, such as Isoptera, For qualitative data, the invertebrate composition Collembola, adults and immatures Coleoptera, and under shrubswas notsignificantly affectedby shrub Isoptera, were more frequent on sandy soil. Other specie (MANOVA; Pillai trace=0.233; P=0.551) taxawere rare and no association with soil type can or soil type (MANOVA; Pillai trace=0.250; be inferred. P=0.075).However,forthesoil,thelowprobability ofthenullhypothesisandasignificantdifferenceon axis2(ANOVA,P<0.028)inindividualanalysesof each axis indicate a possible type II error (the probability of accepting the null hypothesis when it is false). Plots of relative frequency of the zoological categories of invertebrates against the soil type (12 samples under clay soil and 12 under sandy soil) indicate different responses among taxa to soil type(Fig.4).Onegroupconsistsofgeneralistssuch as Acari Non-Oribatida, Acari Oribatida and Diplura, which occurred on both clayey and sandy soil. A second group including Pseudoscorp- Fig.3. Ordinationintwodimensionsbyhybridmultidimensional ionida and Psocoptera, joined in the lower left of scaling(SSH)ofall-invertebratecommunitycollectedundershrubs Fig. 4, were more frequent on clayey soil. The third forquantitativedata.C=clayeysoil,S=sandysoil. E.Franklinetal./AppliedSoilEcology29(2005)259–273 265 Fig.5. Ordinationintwodimensionsbyhybridmultidimensional scaling(SSH)ofthenon-mite,non-collembolaninvertebratescol- lectedundershrubsandgrasstuftsforqualitativedata.S=shrub, G=grass-tuft. andasignificantdifferenceonMDSaxis2(ANOVA, P<0.021) in individual analyses of axes indicates a possible type II error. The community was also not Fig. 4. Upper panel indicates whether the sample was taken on statisticallysignificantlyaffectedbytheplantspecies clayeysoil(solidbars)orsandysoil(openbars).Graybarsindicate (MANOVA; Pillai trace=0.257; P=0.142) but the therelativefrequencyofeachzoologicalcategorywithinall-inver- significant differences on MDS axis 2 (ANOVA, tebratecommunity.Sitesareorderedbytheirpositiononaxis1ofan P<0.042) in individual analyses of each axis also MDSordination(seetext). indicatesapossibletypeIIerror.Thecommunitywas not affected by the soil (MANOVA; Pillai 3.4. All-invertebrate community under grass-tuft— trace=0.081; P=0.247). soil type and shrub species Forqualitativedata,thecommunitywasnotaffected bythesoil(MANOVA;Pillaitrace=0.117;P=0.128) Multivariate multiple regression for quantitative or by shrub species (MANOVA; Pillai trace=0.180; dataindicatednostatisticallysignificanteffectofshrub P=0.359). However, an effect of the vegetation specie(Pillaitrace=0.299;P=0.374)andsoil(Pillai structurewasdetected(MANOVA;Pillaitrace=0.211; trace=0.183; P=0.163). However, for soil type the P=0.020). The variation was principally on axis 2 variationontheMDSaxis2(ANOVA,P<0.058)was (ANOVA, P<0.005). The ordination axes explained veryclosetotheestablishedsignificancelimit. muchofthevariationintheoriginaldata(stress:0.284, For qualitative data, the ordination was not r2=0.6) and shows samples collected under shrubs significantly related to soil (MANOVA; Pillai differentfromthosecollectedundergrass-tuft(Fig.5). trace=0.115; P=0.332) or shrub species (MAN- Plots of relative frequency of the zoological OVA; Pillai trace=0.267; P=0.456). categories of invertebrates along the MDS axis 1 reflecttheirtendencytooccurundershruborgrass-tuft 3.5. Non-mite, non-collembolan invertebrate (Fig. 6). Psocoptera and Homoptera immatures community—soil, vegetation structure and shrub occurred under both shrub and grass-tuft. Grouped species inthelowerleftofFig.6,suchasIsoptera,immatures ColeopteraandadultsHemiptera,weremorefrequent Forquantitativedata,theordinationofallsamples undershrubs.Thethirdgroup,intheupperright,such (24 under shrubs and 24 under grass-tuft) was not as Pseudoscorpionida, Diplura, adults Coleoptera, statistically significantly affected by the vegetation Protura, and Araneae were more frequent on sandy structure(MANOVA;Pillaitrace=0.149;P=0.070). soil. Other taxa were rare and no association with However, the low probability of the null hypothesis vegetation cover can be inferred. 266 E.Franklinetal./AppliedSoilEcology29(2005)259–273 Fig.7. Ordinationintwodimensionsbyhybridmultidimensional scaling (SSH) of the non-mite, non-collembolan invertebrate sampledundershrubsforqualitativedata.C=clayeysoil;S=sandy soil. Diplura, adults Homoptera, Isopoda and adults Coleoptera, that occurred mostly on sandy soils. Fig.6. Upperpanelindicateswhetherthesamplewastakenunder Another group, such as Psocoptera and Pseudoscor- shrubs(solidbars)orgrass-tuft(openbars).Graybarsindicatethe pionida, were more frequent on clayey soils. Other relativefrequencyofeachzoologicalcategorywithinthenon-mite, taxawererareandnoassociationwithsoiltypecanbe non-collembolan invertebrates community. Sites are ordered by inferred. theirpositiononaxis2ofanMDSordination(seetext). 3.6. Non-mite, non-collembolan invertebrate community under shrubs—soil and shrub species Multivariate multiple regression for quantitative dataindicatednostatisticallysignificanteffectofsoil (Pillai trace=0.173; P=0.198). The ordination (stress: 0.230; r2=0.679) was also not significantly affected by the shrub specie (MANOVA; Pillai trace=0.540; P=0.064). However, the low probability for the overall null hypothesis and the significant difference on MDS axis 2 (ANOVA, P<0.039) in individual analyses of each axis indicates a possible type II error. Multivariate multiple regression for qualitative data indicated no significant effect of shrubs (Pillai trace=0.466; P=0.122). However, there was a significant effect of the soil (MANOVA; Pillai trace=0.339; P=0.030). The variation (ANOVA, P<0.013) was principally on MDS axis 1 (Fig. 7). Plots of relative frequency of the zoological Fig. 8. Upper panel indicates whether the sample was taken on clayeysoil(solidbars)orsandysoil(openbars).Graybarsindicate categoriesofinvertebratesagainstthesoiltypereflect therelativefrequencyofeachzoologicalcategorywithinthenon- their preferences for the type of soil (Fig. 8). In the mite,non-collembolancommunity.Sitesareorderedbytheirposi- upper right of Fig. 8 are grouped those taxa, such as tiononaxis1ofanMDSordination(seetext). E.Franklinetal./AppliedSoilEcology29(2005)259–273 267 3.7. Non-mite, non-collembolan invertebrate predators, were dominant in relation to the total of community under grass-tuft—soil and shrub species Acari.Ourresultsarecomparabletothoseobservedin otherenvironmentswithharshecologicalconditions.In The ordinations of the community sampled under African(Zaire)forestsandsavannastheOribatidmites grass-tuft(24samples)werenotaffectedbyanyofthe represent 49.4% and 26% of the arthropods, respec- factors analyzed (soil and species of shrub). For tively.AreversegradientisobservedinActinedidathat quantitativedata,theordinationwasnotsignificantly represents 21.5% and 44.1%, respectively, in the two related to soil (MANOVA; Pillai trace=0.242; typesofvegetation(Notietal.,1996).InChileansteppe P=0.144) or shrub species (MANOVA; Pillai soil under xerophyllous associations, Trombidiforme trace=0.428; P=0.262). (Non-Oribatid mite) is more abundant than the The ordination based on qualitative data was not Oribatida(DiCastri, 1963). Inthe Chihuahuandesert significantly related to soil (MANOVA; Pillai (USA),AcariweredominatedbytheProstigmatawith trace=0.157; P=0.302) or shrub species (MAN- the Oribatida making up a smaller percentage of the OVA; Pillai trace=0.201; P=0.760). assemblage. The dominance of Prostigmatids seems to be related to the harshness of the environment (Santos et al., 1978). In burned savannas in Africa 4. Discussion (Ivory Cost), the relative abundance of decomposers (principallyOribatidaandCollembola)islowerinthe 4.1. Density and diversity of the zoological groups unshadedsoilthatisimpoverishedoflitterandorganic matter due to fire and the density of predatory and The zoological diversity in the savanna areas was phytophagous microarthropods is relatively higher lower compared to an adjacent forest, where we (Athias,1976). registered32zoologicalcategories(Franklin,E.;data For better understanding of the following discus- not published). The higher concentration of Acari sion,theordinationsofthecommunitiesaresummar- Oribatida,speciallyR.foveolatus,andNon-Oribatida ized bellow (Table 2). causedthedifferencebetweenthetotalsampledunder shrubs of Mycia silvativa. In Venezuela (South 4.2. The effect of the soil on the invertebrate America),areductionofthediversityandabundance communities of soil invertebrates from the forest to savanna was detected (Rapoport, 1970). In Amazonia some Analyzing the samples taken under shrubs and evidence that the vegetation structure had a strong grass-tuft,andonbothsoiltypes,thesoildidnothave influence on animals through modification of micro- a detectable influence on the soil invertebrates. climate was already detected. In Central Amazonia, However, removing the effectof the structure ofthe the conversion of forest into policulture reduced the vegetation and analyzing the samples taken only diversity, the density and the biomass of meso- and under shrubs, the effect of the soil type was strong, macrofauna(Ho¨feretal.,2001).InwesternAmazonia, anditwasdetectedintheall-invertebratecommunity a reduction of the macro-invertebrate diversity and for quantitative data. There was a similar trend for biomass of pasture in relation to forest was demon- qualitative data. We also detected the effect for the strated (Barros et al., 2004). non-mite, non-collembolan invertebrate for the In our study, the dominance pattern of Acari in qualitative data, with a strong trend also for the relationtothetotalcatchissimilartoreportsforother quantitative data. The all-invertebrate community, forestenvironmentsinCentralAmazonialikeflooded composed by less numerically dominant groups, forestof‘‘va´rzea’’and‘‘igapo´’’,primaryandsecondary mostlylargerthan2mm,ismoremobileandoccurs forest and ‘‘campinarana’’ (Franklin et al., 1997). inhigherdensitiesinthevegetationlayer.Theshrubs Therefore, in most of Amazonian ecosystems the in the savanna provide a deeper litter layer that dominanceofOribatida(46–88%)isgreaterthanother enhances water retention as well as moderating soil mite groups (Franklin et al., 1997). However, in the temperatures. Both factors can favor growth of savannasoils,theNon-Oribatida,mostlycomposedof mesofauna populations. According to Kieft et al. 268 E.Franklinetal./AppliedSoilEcology29(2005)259–273 Table2 Quantitativeandqualitativesignificantresultsoftheordinationsbetweentheinvertebratesandstructureofthevegetation(shrubs,grass-tuft),soil type(sandy,clayey),plantspecies(M.sylvatica,Micorniaalbicans,M.caerulenscens,C.ribesioides),andplantspecies+structureofthe vegetationinAmazonian-typesavannaareasofAlterdoChaõ.Para´.Brazil Structure Soil Plant Plant+structure Shrubs+grass-tuft Allinvertebratescommunity Quantitative–qualitative Non-mite,non-collembolan Quantitative(?)–qualitative invertebratecommunity Shrubs Allinvertebratescommunity – Quantitative–qualitative(?) – Non-mite,non-collembolan – Quantitative(?)–Qualitative – invertebratecommunity Grass-tuft Allinvertebratescommunity – – Non-mite,non-collembolan – – invertebratecommunity ?=possibletypeIIerror;–=notcompared. (1998), plant communities of large portions of the webstructureofthevegetation(shrubsandgrass-tuft). southwestern United States have changed from In this case, shrubs and grass-tuft appear to generate grassland to desert scrubland and studies have different ecosystems inthe savanna areas ofAlter do demonstrated that soil nutrient resources become Chaõ. This is likely because of the enhanced habitat spatially more heterogeneous and are redistributed heterogeneity inside the shrub patches, with a more into islands of fertility with the shift in vegetation. diverseplantcommunity,andawiderrangeofniches. Within adjacent grassland and creosote bush sites, Also, the shrubs in the vegetation islands provide the soils under plants at both sites had greater total lower temperature and higher soil humidity. These and available nutrient resources, with higher con- results agree with those of Athias (1976), who centrationundercreosotebushthanundergrass-tuft. concluded that the temperature, soil humidity and Underthemoreexposedgrass-tuftcover,wherethe the amount of litter of the herbaceous plants were plant diversity was drastically lower, only the important for the invertebrate composition in burnt community composed of non-mite, non-collembolan savannas in the Ivory Coast. In Zaire (Africa), the invertebrate demonstrated a probable difference in communitiesofOribatidaspeciesareorganizedalong relation to the soil type. Here, we failed to find any asuccessionalgradient,startingfromthedenseforest relationship of soil type with the all-invertebrate (‘‘muhulu’’) passing through woodland (‘‘miombo’’) community. These results probably reflect the more tothesavanna,providingevidencethatthevegetation adverse conditions of the habitat in the sandy soil, structure had a strong influence on animals through more exposed to abiotic factors, and lower plant modificationofmicroclimate(Notietal.,1996).Pozo diversitythatisassociatedwithaloworganiccontent (1986) found similar patterns for collembolan in the soil caused by the thin litter layer. populations. However, in savanna at High Katanga (Congo, Africa) there was no major difference 4.3. Differences between the invertebrate between the oribatid mites fauna taken at the base communities underclumps of shrubs and grass-tuft ofgrass-tuftorbetweenthem,asthesoiliscompletely coveredbyalayeroflitterthatallowsfaunaexchanges The effect of the structure of the vegetation was betweenthetwohabitats(Notietal.,2003),providing evident,affectingtheall-invertebratecommunityand a‘‘corridor’’thatprobablyhasattenuatedthenegative thenon-miteandnon-collembolancommunity.These effects of fragmentation (Rantalainen et al., 2004), results showed that the mesofauna have a mosaic that is not the case of the savannas areas in Alter do distributioninthesavannadependentonthesoil-food Chaõ.

Relative effects of biotic and abiotic factors on the composition of soil invertebrate communities in

Similar Relative effects of biotic and abiotic factors on the composition of soil invertebrate communities in