Impact of different land management on soil spiders (Arachnida: Araneae) in two Amazonian areas of Brazil and Colombia

2011·5.4 MB·English

by  Nancy F Lo-Man-Hung

2011.TheJournalofArachnology39:296-302
Impact ofdifferent land management on soil spiders (Arachnidai Araneae)
in two Amazonian areas ofBrazil and Colombia
NancyF.Lo-Man-Hung' RaphaelMarichal' DavidF.Candiani',LeonardoS.Carvalho^RafaelP.IndicattP,Alexandre
B.Bonaldo',DarioH.R.Cobo^AlexanderFeijooM.^,StephanieTselouiko-,CatarinaPraxedes',GeorgeBrown®,Elena
Velasquez^,ThibaudDecaens^JohanOszwald'^, MarluciaMartins' andPatrickLavelle-’: 'Museu Paraense Emilio
Goeldi, CoordenagaodeZoologia, Belem, Para, Brazil. E-mail: [email protected]; -Universite Pierreet Marie
Curieand IRD, UMR BIOEMCO 211, Centre IRD Hede France, Bondy, France; '’Universidade Federaldo Piaui,
CampusAmilcarFerreiraSobral, Floriano, Piaui, Brazil;'‘Instituto Butantan, LaboratoriodeArtropodes, SaoPaulo,
Sao Paulo, Brazil; ®UniversidadTecnologica de Pereira, Pereira, Colombia;®Embrapa Florestas, Colombo, Parana,
Brazil; ’Centro InternacionaldeAgriculturaTropical (CIAT), Unidad Suelos, Cali, Colombia; ^Universitede Rouen,
UFRSciencesetTechniques,MontSaintAignan,France;“^UniversitedeRennesLaboratoryofGeographyandRemote
SensingCOSTEL, UMR CNRS LETG6554, France
Abstract. Theglobaldemandfordifferentland-usepracticecommoditiesintheAmazoniaisgrowing,andthisregionis
increasinglyaffectedbytheimpactsoflandmanagement.Theaimofthisstudywastoevaluatetheinfluenceofland-use
intensificationonsoilspiderassemblagesfromsixdifferentland-usesystemsinColombiaandBrazil.Thesystemswere
fallowsaftercropsandpastures,forest,crops,pasturesandplantations.Spiderspeciesrichnessanddensitydecreasedwith
increasing farming management intensity. A principal component analysis (PCA) showed forests and fallows were
separated from systems with stronger anthropogenic soil disturbance. The relationships often spider guilds differed
significantlybetweenland-uses,suggestingthattheycanbeareliableparameterforstudiesofecologicalindicators.
Keywords: Macroecology,agroecosystems,land-use,guilds,ecologicalindicators
Soilisoneofthemostdiversehabitatsonearth(Gilleretal. 2006). Furthermore, arthropod diversity may be higher in
1997; Wolters 2001; Decaens et al. 2006). Unfortunately, the cultivated areas than in non-cultivated areas (e.g., secondary
soildiversityinAmazoniaisthreatenedbythegrowingglobal forest), suggesting that arthropods are good candidates for
demand foragricultural commodities produced in this region biodiversity correlates (see Duelli & Obrist 1998). Arachnids
and also by increasing deforestation (Laurance et al. 2002). represent approximately 2% ofthe described species world-
Additionally, climatechangecan resultindroughtand forest wide (Adis 2002) and are conspicuous components of
fires(Lauranceetal.2002).ChangeinsoiluseinAmazoniais agricultural landscapes (Samu et al. 1999). Given their
currently intense, and the conversion of native forest to prominence, several authors have studied the effect and
agriculturalpracticesorpastureisthemaindisturbanceeffect relative importance of local environmental factors on
impactingtheremainingnativeforests(Fearnside2005,2006). arachnids (mostly spiders) in agroecosystems. Studies of
Thesocialandeconomicimportanceofthiskindofagriculture spiders deal with the potential use of these animals for
iswell recognized (Alexandratos 1995), but itsenvironmental limiting arthropod pests through predation (Greenstone &
impactisnotsatisfactorilyknown.Usuallythereisaconsensus Sunderland 1999; Hodge 1999; Marc et al. 1999; Riechert
among researchers as to the negative effects of habitat 1999; Sunderland 1999; Maloney et al. 2003; Nyffeler &
modification (e.g., deforestation by ranchersand farmers) on Sunderland 2003; Harwood et al. 2004), competition and
dLiavuerrsaintcyeoeftnaalt.iv2e00p0l;anPterannedra&niMmaalltsp2e0c0i3e;sSinoaArmesa-zFoinlihoae(te.ga.l., ignutielrdactsitornusctu(rMears(hGailblso&n eRtypsalt.ra1919929;9;UWetizseetetaall.. 11999999)),,
2006). Understanding changes that directly influence these agrobiont species (Samu & Szinetar 2002; Pekar & Haddad
processes is important for local people, whose livelihoods 2005; Thorbek &Topping2005; De Meester& Bonte2010),
depend on agriculture practices or pasture areas. In fact, anddiversityanddistribution(Duelli&Obrist 1998;Samuet
duentdeerrmsitnainndgintghethceoemcpoolsoigtiicoalncoofmpsolielximtaycrooffathuensaeaissscerumcbilaalgetso aslp.ide1r9s99;areSeyufsuelfiunlaa2s010p)o.tenAtlilaltheecsoelogsitcuadliesindsihcoatwoerds tahnadt
(Franklinetal. 2005; Decaensetal. 2006; Lavelleetal. 2006; natural enemies ofpests, since the composition and species
aaDrnetdcharseounpsstoadis2n)0a1bh0ia)l.viteySbe(evMeenarraplcroeoptroagsla.endi1sa99sm9sb;ioWoiifnldltiehcteat2o0sr0osi1l;ofLfsaaouwinleasquea(tel.igat.ly., dcriiocsmhtpnuoerssbisatnicioenn dlaeinvfedflesr,tehnetresgpliaaotnnidaallmapanondpaugtleeatmmipeoonnrtsalaosrfceaalssepsiddoeefrpeasnpdgeicvioeenns
200A5r)t.hropods are the most diverse group of animals, study. However, little information is available on theeffects
inhabiting most habitats on Earth (Hawksworth & Bull ofdifferent forest management regimes on the composition
ofarachnidassemblages(e.g., Downieetal. 1999; Rypstraet
"’Currentaddress: PontificiaUniversidadeCatolicado RioGrande al. 1999;Jeanneretetal. 2003). Inaddition, inAmazoniathe
doSul,MuseudeCienciaseTecnologia,LaboratoriodeAracnologia, consequences of different land management techniques on
PortoAlegre,RioGrandedoSul,Brazil. this group are rarely studied.
296
LO-MAN-HUNGETAL.—IMPACTOFLANDUSEONSOILSPIDERS 297
COLOMBIA
Caqueta
3landscapewindows 3landscapewindows
n
1 Palmares Macaranduba 1 Traditional ’21>,%o a<>“O Agroforestry
3subwindows /I
/ i \ / J 1 / 1 \ / 11 0\ ) / i \
1
—
Figure 1. Siteselection,showingsamplingdesignforeachstudyarea(modifiedfromLavelleetal.2010).Areanamesmatchthoseidentified
inthetext(studyareaandsiteselection).
The purpose of this study was to assess the impacts of WGS84 for Traditional: -2316945.11 / 10179721.63; Agro-
I landscape management on spider distribution patterns by sylvopastoral: -2335962.87 / 10176406.04; Agroforestry:
i sampling two contrasting regions in a large-scale soil —2351790.15 / 10163206.21. Six land-use systems were iden-
ecosystem project. It was also to evaluate the relationships tified after field confirmation: forest (F; preserved or ratio-
betweenspiderbiodiversityparametersinprimaryforestsand nally exploited forests); fallows after crop (FAC; secondary
I inawiderange ofderivedsystems oflandmanagement. We forest developed in abandoned crops dominated by native
tested the hypotheses that spider species richness increases grasses, vegetables and weeds); fallows after pasture (FAP;
with decreasingmanagement impact, and that overall spider secondaryforestsdevelopedinabandonedpasturesdominated
: aresssteomrbaltaigoensefafreectssuiitnabdliestausrbreedlialbalnedseccoalpoegsic(aPlerinnedrica&torMsalotf Bbryachheirabrsiaasnsdp.,shirnuvbasd);edpabsytu“rbeasba(tPjaus”t,; aanreaAsmadzoomniinaantedpalbmy
2003). tree; Arecaceae: Orbygnia sp. or other trees); crops (Cr;
METHODS shiftingcultivation ofcassava (manioc), rice ormaizecrops)
— andplantations(PI;cocoa, rubbertree, agroforestrysystems)
Study area and site selection. The experiment was estab- (seeMarichaletal. 2010,Table 1).Averageannualrainfallin
lishedintwoAmazonianareaswithdifferentplantcoverage, the Brazilian sites is 1775.5 mm per annum (p.a.) in Pacaja,
onerelativelyrecentlycolonized(10-15yrago)inthestateof 1881.4 mm/p.a. in Macaranduba, and 2452.6 mm/p.a. in
Para, northeastern Brazil andanothercolonized60yragoin Palmares,withameanannualtemperatureof28.3°C. Inthe
the Department of Caqueta, southwestern Colombia. Both Colombiansitestheaverageannualrainfallis4676.0mm/p.a.,
I study areas were separated into three landscapes (windows) withameanannualtemperatureof27.8°C.
—
, with different deforestation ages and/or different land Spidersampling. SpidersweresampledbetweenApriland
I managementstructure. June2008,duringthedryseason.Thesamplingmethodology
Each window was formed by three replicate groups (sub- usedtocollectsoilandlitterspiderswasbasedontheTropical
windows) containing 17 farms. Three farms were selected in SoilBiologyandFertilityProgram(TSBF)method(Anderson
eachsub-window, andeachselected farmwasdivided infive and Ingram 1993), which consists ofdiggingonecentral soil
samplingpoints (sites) located 200 m apartalonga diagonal monolith (25cm long, 25 cmwideand 20cmdeep)and two
transect(Fig. I).Wesampled54farmsand270sites(135sites additionalmonolithswith25 X 25 X 30cmdug5meastand
ineachcountry). west, respectively, from the central monolith on each ofthe
The landscape mosaic for all areas was analyzed using 270sites.Atotalof810monolithswastakenandhandsorted.
satellite images - coordinates of the windows in UTM Thus,onesampledunitwascomposedofthreemonoliths.The
i projection, zone 22S, WGS84 for Macaranduba: 682382.74/ macrofaunawashand-sortedinthefield,andthespiderswere
9469861.49; Pacaja; 494874.75 / 9586676.06; Palmares: stored in 80% alcohol. In the laboratory, the spiders were
627813.87 / 9351874.23, in UTM projection, zone 18N, counted, and the adults were sorted to morphospecies and
I
298 THEJOURNALOFARACHNOLOGY
o o identified. The spiders were classified by assemblage guilds
UH and to provide trustworthy for the results, all the analyses
were based only on adults (i.e., individuals susceptible to
(H^3 o o o correctidentification).Thevoucherspecimensaredepositedin
U the collection of Museu Paraense Emilio Goeldi in Belem,
o o o o o ParSap,idBerrazgiulil(dA.eBs.tabBloinsahlmdeont,.—curWateorf)o.llowedtheclassicdefini-
tionofguildsbyRoot(1967).Ourdesignationofspiderguilds
o o o o was based on ecological characteristics obtained during
numbers. fieldwork, observation, biology, taxonomy and additional
literature reviewed (i.e., Coddington et al. 1996; Uetz et al.
by o o 1999; Hofer&Br—escovit2001; Diasetal. 2010).
Data analysis. Monte-Carlo test simulations were calcu-
latedtoassessthesignificantdifferencesofspiderinteractions
followed o o oo o with land use. A Principal Component Analysis (PCA) was
performed to verify differences in the composition ofspider
letters o o o O guildsamongland-usesystems.ThePCAwascarriedoutona
as U< matrix composed of 270 sites and 10 spider guilds. We
& assigned spiders to ecological categories rather than species,
labeled <o2 o o o ^ vbaelcuaeusseinmothsettsapbelceiseswowuelrde rianrvealiadnadteathgerePatCnAumanbaelrysiosf.zTehreo
< datawere subjected to natural logarithmictransformationIn
< o o in (x + 1) to reduce the influence of common species and
Sub-windows u differencesintotalsiteabundanceindeterminingcommunity
patterns(seeKeene 1995).Statisticalanalyseswereconducted
using R version 2.12 (R Development Core Team 2009),
packageade4(Chesseletal.2004;Dray&Dufour2007;Dray
areas.
in o etal. 2007).
RESULTS
sampling in in o A total of 1906 individuals, including 178 individuals in
Palmares, 344 in Magaranduba, 143 in Pacaja, 459 in
Colombia Traditional, 340 in Agrosylvopastoral, and 442 in Agrofor-
estry was collected. The adults corresponded to 206 individ-
ualsand 101 morphospeciesbelongingto25families. Median
and o CN o r^i lspoewceiresvarliucehsneosbssewravsed1.i5ncsrpoepcsi,espaisntufraelsloawsndapnldanftoarteisotsn,sw(0i.t4h,
Brazil 0.2,and0.1,respectively:Fig. 2a);averagedensitiesofspiders
in m (N variedfrom 1.1 iedividuals/m"inplantationsto7individuals/
in forest, with intermediate values in crops and fallows
observed (Fig. 2b). The results ofthe analysis ofthe ten spiderguilds
VO ^ o (Table2)collectedoneachland-usesystemweresubjectedto
PCA. The correlation circle built with the first two factors
systems r- o o wrieptrhes1e2n.t4ed%:28s.e2e%Foifg.th2e).totFaalcvtaorrian1cese(pFaIrwaittehd1t5h.e9%laanndd-uFs2e
systemsfallowaftercrops(FAC), fallowafterpasture(FAP)
Land-use andforest(F)fromcrops(Cr),pasture(Past)andplantation
(PI). Monte-Carlo test (P < 0.01) simulations exhibited
1.— significant differences in the spider assemblage relationships
with the land-use systems. The simultaneous comparison of
Table ^M”3t-.S10-.-.0c^-(Soss'"oaS-coo 3Sh I^.•ga^^SID'^ioCIIuo^"Xyoag) soSc (tnFFhoAiecgPt.cuor3ran)ranesldlhagotriFwooenudhncatdivrhecahltuenstathtenerrdopsnofg(iancNttrGoseHrlli)aaot,lciaomgtnresahdopiufpnoasdrritwswhiieentaghvleafrnrtdshormu(eseGtehWseg)uFPiAlaCdCnsA,d:
groundrunners(GR).
DISCUSSION
Theresultssuggestthatspiderspeciesrichnessanddensity
decreased with regular disturbance and/or high levels of
grazing (Fig. 2). This pattern can be partly explained by
LO-MAN-HUNGETAL.~IMPACTOFLANDUSEONSOILSPIDERS 299
Crops Fallowaftercrops Fallowafterpastures Forests Pastures Plantations
(a) Landuse
(b)
Landuse
—
Figure 2. Totalspidersrichness(a)anddensity(b)underdifferenttypesoflanduse.Theboxplotsshowthelowerquartile,themedianand
the upper quartile, with whiskers extending to the most extreme data point unless outliers (more than 1.5 times the interquartile range)
arepresent.
—
Table 2. GuildclassificationdefinedofthespiderssampledbyTropicalSoilBiologyandFertilityProgrammethod(seeDiasetal.2010).
Totalnumberofmorphospeciesforfamily/generaoneachguild(n = 10)isinbrackets.
Guild IncludedTaxa
Aerialhunters(AH) Anyphaenidae(1)-Corinnidae(1):(1) Trachelas-Oxyopidae(1);(1)O.xyopes
Diurnalaerialambushers(DAA) Thomisidae(3):(1)Bucranium,(I)Misiimenops
Diurnalspacewebweavers(DSWW) Linyphiidae(8):(1)Meioneta-Pholcidae(2):(1)Mesabolivar,(1)Melagonia-Theridiidae(10):(1)
Chrysso,(2)Dipoena,(2)Theridion,(1) Thwaitesia
Groundrunners(GR) Corinnidae(7):(1)Castianeira,(1)Corinna,(2)Creugas,(1)Mazax,(1)Mynnecotypiis,(1)Orthohida
Groundweavers(GW) Dip-lGunriadpaheos(1i)d:a(e1)(3D);ip(l1u)rAapo-pyHlalhunsi,i(d2a)eZi(2m)i:r(o2m)uNse-ohLayhcnoisaidae(1)-Prodidomidae(1):(1)Lygromma
Nocturnalaerialambushers(NAA) Ctenidae(1):(1)Acanthocienus-Sparassidae(1):(1)Olios
Nocturnalgroundambushers(NGA) Idiopidae(2):(1)Neocleniza-Theraphosidae(1)
Nocturnalgroundhunters(NGH) Cyrtaucheniidae(2)-Oonopidae(18):(1)Brignolia,(1)Coxapopha,(3)Neoxyphiniis,(1)Xyccarph-
Palpimanidae(4):(1)Fernandezma,(3)Otiothops-Salticidae(12)-Tetrablemmidae(1):(1)
Tetrablemma
Nocturnalspaceweb-weavers(NSW) Ochyroceratidae(1)
Orbweavers(OW) Araneidae(13):(3)Alpaida,(3)Mangora,(2)Micrathena,(1)Spilasma,(1) Wagnerkma-
Symphytognathidae(1):(1)Symphytognatha-Theridiosomatidae(3)
300 THEJOURNALOFARACHNOLOGY
ecological effects at the vegetation level that are strongly
dependentonboththeintensityofformerarablemanagement
and the initial conditions of grassland succession (Van der
Putten et al. 2000). Several studies predicted that spider
densityanddiversitywouldbedisproportionallyimpactedby
reduction in plant species richness and habitat complexity
(Gibsonetal. 1992;Rypstraetal. 1999;Jeanneretetal.2003;
Perner&Malt2003;Haddadetal.2009).However,Jeanneret
et al. (2003) suggested that the most importantlocal habitat
factorsarethosedirectlyinfluencedbymanagementpractices.
Itiswellknownthatspiderscanexhibitshortreactiontimesto
changesinlanduse(Jeanneretetal.2003;Perner&Malt2003)
and subsequently to changes in microclimate (Nyffeler &
Sunderland2003; Perner&Malt2003), soil-moisture(Perner
& Malt 2003), litter cover, litter depth and twig cover
(Oxbrough et al. 2005). Since the establishment of crops,
pastures and plantations makes a significant impact on soil
properties, we expected that the soil spiders would be more
significantly affected than what was observed. In fact, most
similar studies showed that spider species richness decreased
duetosoilmanagementintensity(Downieetal. 1999;Perner
&Malt2003).Furthermore,theincreaseinspiderdiversityon
disturbedareasisoftenconstrained,evenwhennaturalabiotic
conditions seem to be restored (e.g., on secondaryforestsee
Lo-Man-Hungetal. 2008).
Our PCA results separated the land-use systems offorest
and fallows (F, FAC, FAP) from thosewith high anthropo-
genicsoildisturbance(Fig. 3).ThePCAalsoshowedthatthe
identification of ecological categories was sufficient to
separatethesixsystemsstudied,andtoindicatewhichspider
guildsweremostassociatedwithforestsystems.Spiderguilds
are widely used in environmental management and impact
assessment (e.g., Perner & Malt 2003) because of the
assumption that the factor affecting a resource in the
environment will also impact the whole spider guild (Sever-
inghaus 1981; Simberloff& Dayan 1991). In our study the
three guilds (GR, GW, NGH) associated with forest and
fallows (F, FAC, FAP) are characterized by spiders that
search actively for prey (i.e., Corinnidae, Cyrtaucheniidae,
Gnaphosidae,Lycosidae,Oonopidae,Palpimanidae,Prodido-
midae, SalticidaeandTetrablemmidae)oraresedentaryweb-
weavers (Dipluridae, Hahniidae) (Hofer & Brescovit 2001;
Dias et al. 2010; also see Table2). Potentially, these three
guilds (GR, GW,NGH)favorcrypticandcomplexhabitats;
in this study theywere significantly represented in theforest
and fallows. Also, these guilds seem to be negatively
influencedbyhumanimpactsonlandmanagement,although
thelycosidsareusuallyobservedingrasslandhabitats(Jocque
&Alderweireldt2005).Theseresultssuggestthatspiderguilds
can be considered a useful tool for ecological studies, as
predictedbyotherauthors(e.g.,Gibsonetal. 1992;Uetzetal.
— 1999; Jeanneret et al. 2003). Such information can help to
Figure 3. Principal component analysis (PCA) performed on identifytheirvalueinland-useareasandevaluatetheirrolein
sDpSidWerW:guidlidusrn(aAlH:spaaecreialwehbuntweerasv,erDsA,AG:R:diugrnraolunaderiwaelavaemrbsu,shGerWs:, pest management (e.g., Maloney et al. 2003; Nyffeler &
nocturnal ambushers, NAA: nocturnal aerial ambushers, NGA:
nocturnal ground ambushers, NGH: nocturnal space web-weavers,
NSW:nocturnalspaceweb-weavers,OW:orbweavers)forlanduse ofsoil land-usesystems. Thedots representthesites andthecolor
(F:forests,FAC:fallowsaftercrops,FAP:fallowsafterpastures,PI: degradedindicatesland-usesystemsasdarkertolighterasfollows:jet
plantations.Past:pastures,Cr:crops),(a)Correlationcircleofspider black,black,darkgray,gray,lightgray,verylightgrayforPast,F,
guilddensityforsoilland-usesystems,(b)Factorialmapsandeffect FAC,Cr,FAP,PI,respectively.
LO-MAN-HUNGETAL.—IMPACTOFLANDUSEONSOILSPIDERS 301
Sunderland 2003). Our study suggests that spider guilds can Fearnside,P.M.2005.DeforestationinBrazilianAmazonia:history,
strongly and quickly respond to changes in environmental rates,andconsequences.ConservationBiology 19:680-688.
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at2o0n0d5p,reec2vo0es0ny7tstaaennmdthJsreoorcpvqoiucgeeesn,eitcaaslc.th2hai0ns0g5ei)ss.tIihtneaelmscaooishnyisgthflaeicmgthoftrusnctcuhtreiroennneitenldyg drIKaemntvpoieawoclnltoaeslpdemgeoenfntorinpAaemCrnaoavzndisoirengorimnvama:ietnnitLoatanhlteiansneRAdromvleiDecreeisvcoeafl.oofpPTmprs.eatnda1tin5t.d8ii-on(n1gDa7.l1A.f.oIrEencPsotoHlsouegamyiscaa&nla
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