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

15 Pages·2005·0.44 MB·English

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. Luiza˜ob
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.:[phone];
requiredtoprocesssamplesbothincreasedramatically
fax:[phone].
E-mailaddress:[email protected](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 Cha˜o. 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
Cha˜o(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-invertebratecommu-
nity 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-typesavannaareasofAlterdoCha˜o.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 prob-
ability 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-typesavannaareasofAlterdoCha˜o.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 Cha˜o. 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 Cha˜o.