Applied Soil Ecology 71 (2013) 72 80

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Applied Soil Ecology

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Patricia L Stra Universidade 0 Lavrb Instituto Tecnc Universidade 9012-

a r t i c

Article history:Received 6 SepReceived in reAccepted 16 M

Keywords:Land useSpecies richnessGlomeromycotaSpore abundanceCommunity structureMycorrhiza

ommlant

changss. Soal sp

were recovered from both systems, with 83% of them pertaining to Acaulosporaceae and Glomeraceae.Only 12 species were shared between systems and spore abundance of the majority of fungal species didnot differ between pasture and forest. Spore abundance was signicantly higher in pasture compared toforest but both systems did not differ on mean species richness, Shannon diversity and Pielou equitability.Species abundance distribution depicted by species rank log abundance plots was not statistically differ-ent between both systems. We concluded that conversion of pristine tropical forest to pasture inuences

1. Introdu

Arbuscuare an impcosystems symbiosis wferentiate inout their abity nutrienNutrients aplant growimproves sparticles byand Rillig, 2AMF and thlow fertilitysurvival an

CorresponRegional de BlTel.: +55 47 33

E-mail add

0929-1393/$ http://dx.doi.othe taxonomic composition of AMF communities while not affecting species richness and abundancedistribution.

2013 Elsevier B.V. All rights reserved.

ction

lar mycorrhizal fungi (AMF Phylum Glomeromycota)ortant component of soil biota in natural and agroe-where they establish the arbuscular endomycorrhizalith plant roots. In this association, AMF grow and dif-to typical structures inside the root cortex and spreadsorptive hyphae into the bulk soil to uptake low mobil-ts like phosphorus and zinc (Smith and Read, 2008).re then transferred to their host resulting in improvedth rates and nutrition; external mycelium of AMF alsooil aggregation through physical entanglement of soil

hyphae and production of glomalin-like protein (Purin007; Gillespie et al., 2011). These functions render thee symbiosis particularly important in highly weathered

tropical soils, where mycorrhizal association impactsd growth of tropical woody species (Siqueira and

ding author at: Departamento de Cincias Naturais, Universidadeumenau, Cx.P. 1507, 89012-900 Blumenau, SC, Brazil,21 0272/55 47 321 0470; fax: +55 47 3321 0232.ress: sturmer@furb.br (S.L. Strmer).

Saggin-Jnior, 2001) and also inuences plant succession andrecovery of degraded areas (Scabora et al., 2010).

Switches in land use exert a differential effect upon AMF, caus-ing changes in fungal community structure by altering distributionand dominance of species. Causal effects for these changes arealterations to soil chemical properties (Siqueira et al., 1989), soilmanagement (Jansa et al., 2002), and plant community (Oehl et al.,2003). Considering that different AMF species and fungal isolateswithin species have differential effects on plant growth and nutri-tion, changes on fungal communities caused by switches in land usecan impact host establishment and development (Dodd et al., 1990)and plant diversity and ecosystem productivity (Van der Heijdenet al., 1998).

In the tropics, conversion of areas of native tropical forest topasture and agricultural crops is one of the main switches in landuse system and represent a casual factor in forest degradation(Aguiar et al., 2005; Siqueira et al., 1989). The impacts of chang-ing from a high diversity woody-species dominated forest systemto a low diversity graminoid-species dominated pasture upon AMFcommunities have been evaluated in tropical countries of CentralAmerica. In Nicaragua and Costa Rica, Picone (2000) found roughlythe same AMF species richness in forest and pasture but sporeabundance of most species was higher in the former than in the

see front matter 2013 Elsevier B.V. All rights reserved.rg/10.1016/j.apsoil.2013.05.010 of tropical Amazon forest to pasture afsition but not species abundance and dhizal fungal community

opes Leala, Jos Oswaldo Siqueiraa,b, Sidney Luiz Federal de Lavras (UFLA), Departamento de Cincias do Solo (DCS), Cx.P. 37, 37200-00olgico Vale, BrazilRegional de Blumenau (FURB), Departamento de Cincias Naturais (DCN), Cx.P. 1507, 8

l e i n f o

tember 2012vised form 15 May 2013ay 2013

a b s t r a c t

Arbuscular mycorrhizal fungi (AMF) cfactors including soil attributes and pof tropical Amazon forest to pasture munity species abundance and richne(n = 11) and pasture (n = 13) and fung/ locate /apsoi l

ts taxonomicrsity of arbuscular

merc,

as, MG Brazil

900 Blumenau, SC, Brazil

unity composition and species richness are affected by severalhost. In this paper we tested the hypothesis that conversiones taxonomic composition of AMF community but not com-il samples were obtained in 300 m 300 m plots from forestores extracted, counted and identied. A total of 36 species

P.L. Leal et al. / Applied Soil Ecology 71 (2013) 72 80 73

latter. Both systems also contained similar AMF communities andshared the most frequent species. Johnson and Wedin (1997) foundno differences on total spore number, mean species richness andSimpsons diversity index when comparing grassland sites domi-nated by thtropical drycommunitiethe most abtwo sites ofdetected 29respectivelyHowever, sosame numb(2009) comafter slash-and observesimilar betwsimilar betwin Sorenson

The Amaglobal biodihas caused ture and bedeforestatiohuman comthe slash-anforestry syset al., 2006)zon forest i(Leal et al.,Amazon regthat averagpasture, resboth system

This stution and Su(CSM-BGBDimplementagram and benchmarkBrazilian stwhere the lforest at distems, orchacommunitiepare severaAmazon forcorollary ofwe tested thchanges theabundance

2. Materia

2.1. Study a

The benstant (421

located in tthe Amazonwith precipmean annuto Kppen Pasture siteareas of Ben

was located in the rural community of Guanabara, which is a ter-ritory occupied by Ticuna cultures. Cambissolos (Inceptsols) arethe dominant soils in both areas (Coelho et al., 2005).

The Pasture area is covered by imperial grass (Axonopusius), rass s orishmeanchentatstatios hasuruar, Ria sp

eae, nace

mpli

s (3 were

of thumbstureollec

Marcmpll samed asnd awithsamp

andclude

traytory

two

il che

che andompand , soil orusy (66wedgeabed bectrichroe alsion e

ore e

aliquract man0% aith turedal retnd oe exotic grass Hyparrhenia rufa (Ness) Stapf. adjacent to forest in Costa Rica. The study also showed that AMFs were similar between both systems that also sharedundant species. In Mexico, Gavito et al. (2008) sampled

each primary forest, secondary forest and pasture and and 18 AMF species in a pasture and primary forest,, with only 10 species being shared between systems.me of the sites of primary and secondary forest had theer of species of those found in pasture. Fernndez et al.pared the AMF community in a pasture site establishedand-burn with adjacent tropical dry forest in Mexicod that AMF species richness and spore numbers wereeen both systems. AMF community composition waseen pasture and forest, sharing 13 species and resulting

similarity above 80%.zon forest is considered one of the main hotspots ofversity. Despite this status, anthropogenic disturbancedeforestation of pristine forest to be used for agricul-ef cattle ranching, both accounting for more than 90% ofn in the 1980s (Amelung and Diehl, 1992). Traditionalmunities also convert pristine Amazon Forest throughd-burn practice to distinct land use like orchards, agro-tems, and crop elds for subsistence (Mendonc a-Santos. However, impacts generated by turning pristine Ama-nto distinct land use systems on AMF are still scarce

2009; Strmer and Siqueira, 2011). In a study in theion of Colombia, Pena-Venegas et al. (2007) observed

e species richness was 4.5 and 4.6 in pristine forest andpectively, and a total of 18 AMF species were found ins.dy is part of a broader project entitled Conserva-stainable Management of Below-Ground Biodiversity), co-funded by the Global Environment Facility withtion support of the United Nations Environment Pro-

developed in seven tropical countries. In Brazil, the area of this project was in the western portion of theate of Amazon, in the border with Peru and Colombia,andscape is a mosaic of pristine forest and secondarytinct stages of regeneration adjacent to agroforestry sys-rds and small crop areas created by traditional humans (Fidalgo et al., 2005). In this paper, we aimed to com-l attributes of AMF communities occurring in pristineest and a pasture area used for cattle ranching. As a

previous studies comparing tropical forest and pasture,e hypothesis that converting pristine forest to pasture

composition of AMF communities but not AMF speciesand richness.

l and methods

rea

chmark area is in the municipality of Benjamin Con-and 426 S, 6936 and 701 W, 65 m above sea level),he Alto Solimes river region at the western portion of

state, Brazil. Mean annual precipitation is 2562 mm,itation concentrated between December and April, andal temperature is 25.7 C. Climate is Af type according(tropical humid and superhumid with no dry season).

(PS) was located in private land in the surroundingjamin Constant town while pristine Amazon Forest (FO)

scoparbahiagsite waestablicattle rrepresdeforespecieconia jconcoloGeonomArecacHelico

2.2. Sa

Gridpointsnormsgrids nand Pawere c1015each safor soicollectpoint apoint, 12 subdepth)not inplasticlabora(one to

2.3. So

Soil(1997)each cdried BrieyphosphtometrK folloexchanextracttion spwith d(%). Wthe cat

2.4. Sp

An to ext(Gerdetion (2lled wwas poMateridish abrachiaria grass (Brachiaria brizantha, B. humidicola),(Paspalum notatum), and several invasive plants. Theginally covered by terra rme forest, cleared in 1945 fornt of sugarcane and converted to pasture in 1970 foring. The Forest area is typical pristine terra rme forestive of the western Brazilian Amazon forest and neithern nor selective logging has occurred. A total of 599 plant

been registered with the most abundant being Heli-na, Heterostemon ellipticus, Pariana radiciora, Cecropianorea racemosa, Iriartea deltoidea, Ischnosiplon sp. and. Families with high densities were Fabaceae, Araceae,Myriticaceae, Cecropiaceae, Moraceae, Poaceae, andae (Nogueira et al., 2007).

ng design

00 m 300 m) containing geo-referenced sampling established in several land use systems to follow thee CSM-BGDB project (Huising et al., 2008). For this study,er 1 and 6 covered by Forest (n = 11 sampling points)

(n = 13 sampling points) were selected and all samplested during the rainy season in a eld campaign duringh 2004 and detailed in Strmer and Siqueira (2011). Ine point a wooden stick was placed as a center referencepling. Each sample was composed of 12 subsamples

follow: four subsamples collected 3 m from the centernother eight subsamples collected 6 m from the center

four in cardinal directions and four between them. Allles were collected with a soil core sampler (020 cm

pooled into a plastic bag. Forest litter was scraped andd in the soil sample. Soil was then homogenized ins, conditioned in new plastic bags, transported to theinside thermic boxes and kept at 4 C until processing

months after sampling).

mical characteristics

mical analysis were performed according to EMBRAPA described in Moreira et al. (2009). A sub-sample fromosite sample was removed from the plastic bag, airpassed through a 2 mm mesh sieve before analysis.pH was measured in a soil:water suspension (1:2.5) and

extracted by Mehlich 1 and analyzed by spectropho-0 nm). Mehlich 1 was also used to extract exchangeable

by photometry. KCl 1 mol L1 was used to extractle Al, Ca and Mg. Available Zn, Fe, Mn and Cu werey Mehlich 1 and further determined by atomic absorp-ometry. Organic carbon was determined by oxidationmate and the value used to calculate organic matter

o calculated after analysis above the sum of bases andxchange capacity (CEC).

xtraction and species identication

ot of 100 cm3 of soil from each sample was usedAMF spores following the method of wet sievingn and Nicolson, 1963) and sucrose gradient centrifuga-nd 60%). Briey, soil sample was placed in a 2 L bucket,ap water and swirled using a glass rod. Soil suspension

onto two nested sieves with 710 and 45 m opening.ained in the 710 m sieve was conditioned in large Petribserved under dissecting microscope for large spores

74 P.L. Leal et al. / Applied Soil Ecology 71 (2013) 72 80

and sporocarps. Material from the 45 m sieve was poured intoFalcon tubes containing the sucrose gradient and centrifuged for2000 rpm for 1 min. The supernatant was dispensed over the 45 msieve, washed under tap water and placed on Petri dish. Sporeswere obserdissecting min permanemixed with

Taxonomafter sporecharacteristciated withdissecting descriptionat West Virand Plant Psity, Polandused to assi

2.5. AMF co

Differenareas were Number of surement ofor each spFrequency est was calpresent oveage. AMF spspecies perShannon diative sporethe Pielou PAST (PAleoSpore abunrank-log ab(Magurran,

2.6. Survey

We survspecies richVenegas etet al., 2008GuadarramAfrica (Wilet al., 2003identied sGlomeraceacota was anwas compawhere C = thity to 1 = coto both stustudy, and late similarnumber of identied: Snchez (19

2.7. Statisti

Total spto analysis ferences in

Table 1Mean values of soil parameters in pasture (PS) and forest (FO). Within rows, meansfollowed by different letters indicate that values are signicantly different (P 0.05).N = number of samples.

tribut

dm3) dm3

olc dmolc d

olc dmg dm

dm3

g dm

g dm

f base exchic mat

s richay an

< 0.0in eag (x for sat Pred pare

s ranhe K

and

ltivarnshipe r

sponeity nt. Axis, pelatioMultncy o

ults

pH st (4tly hantltly btal odentecovf the species (83%) pertained to the families Acaulospo-

(Acaulospora) and Glomeraceae (Glomus and Rhizophagus).nera Gigaspora, Diversispora, Archaeospora, and Ambisporaepresented by only one species each while four species wereed in the genus Scutellospora (Table 2). Species richness ofsporaceae was higher in pasture compared to forest whiles of Glomeraceae and Gigasporaceae were in higher numberst.elve species were shared between pasture and forest:spora foveata Trappe & Janos, Acaulospora gedanensis cf,spora spinosa Walker & Trappe, Acaulospora tuberculata Janospe, Acaulospora walkeri Kramadibrata & Hedger, Glomusiforme Blaszkowski, Glomus 04, Glomus 15, Scutellospora

da (Nicolson & Schenck) Walker & Sanders, Archaeosporaved, collected and separated by morphotypes under aicroscope (Zeiss Stemi-2000). Spores were mounted

nt slides in polyvinyllactoglycerol (PVLG) and PVLG Melzers reagent.ic composition of AMF community was assessed

s were identied through the analysis of spore wallics observed under a microscope (Zeiss, Axiostar) asso-

spore color, size, and shape observed under themicroscope. Comparison with both original species

protocols and description of reference isolates (INVAMginia University, USA, http://www.invam.caf.wvu.edu)athology Department homepage at Agriculture Univer-

(http://www.agro.ar.szczecin.pl/jblaszkowski/) wasgn morphotypes into species.

mmunity analysis

ces in AMF communities between pasture and forestinvestigated by using a suite of community descriptors.spores was counted for each species and used as a mea-f species abundance. Summing the number of sporesecies in a sample yielded the total number of spores.of occurrence of AMF species within pasture and for-culated as the number of samples that a species wasr the total number of samples and expressed as percent-ecies richness (S) was determined by counting fungal

soil sample. Spore number was used to calculate theversity index (H = ipi(log pi), where pi is the rel-

abundance of ith species considering all species) andevenness (J) according to Magurran (2004) using thentological STatistics) software (Hammer et al., 2001).dance of each species was used to generate speciesundance plot to depict species abundance distribution

2004).

ed publications

eyed twelve publications that have information on AMFness occurring in tropical forest in the Americas (Pena-

al., 2007; Picone, 2000; Lovelock et al., 2003; Gavito; Aguilar-Fernandez et al., 2009; Violi et al., 2008;a and lvarez-Snchez, 1999; Mangan et al., 2004),son et al., 1992; Mason et al., 1992), and Asia (Zhao). For each study, the number of identied and non-pecies pertaining to Gigasporaceae, Acaulosporaceae,e sensu lato and other families in the Glomeromy-alyzed. AMF community composition between studiesred using Srensen coefcient of similarity: C = 2w/a + b,e coefcient of similarity (ranging from 0 = no similar-mplete similarity), w = the number of species commondies being compared, a = the number of species in oneb = the number of species of the other study. To calcu-ity index the following studies were not included as thenon-identied species was higher than the number ofPena-Venegas et al. (2007), Guadarrama and lvarez-99), and Mangan et al. (2004).

cal analysis

ore abundance data was log(x + 1) transformed priorto meet normality and homogeneity of variance. Dif-

soil chemical properties, total spore abundance and

Soil at

pH P (mg K (mgCa (cmMg (cmAl (cmZn (mFe (mgMn (mCu (mSum oCationOrgan

specieone-wtest (Plected was loforest t test compato comspecieusing tANOVA1995).

Murelatioties. Wthe reerogengradieDCA ainfer rerties. freque

3. Res

Soilto forenicansignicnican

A towere iwere rMost oraceaeThe gewere ridentiAcaulospeciein fore

TwAcauloAcaulo& Trapcorymbpellucies Pasture (N = 13) Forest (N = 11)

5.21 0.04 a 4.46 0.03 b 2.8 0.21 b 4.1 0.18 a) 40.3 3.5 b 58.7 3.7 a

3) 2.23 0.20 b 3.63 0.42 am3) 1.43 0.20 a 1.94 0.13 a3) 2.75 0.25 b 5.14 0.37 a

3) 7.7 1.78 a 5.85 1.48 a) 471.76 80.0 a 194.5 17.4 b3) 40.47 9.4 a 61.79 6.9 a

3) 2.15 0.33 a 1.22 0.09 bs (cmolc dm3) 3.79 0.36 b 5.71 0.41 aange capacity (cmolc dm3) 6.55 0.46 b 10.85 0.41 ater (dag kg1) 1.58 0.06 a 1.55 0.08 a

ness between pasture and forest were tested using aalysis of variance (ANOVA) following Tukey post hoc5) and treating the number of sampling points col-ch area as replicates. Spore abundance of each species+ 1) transformed and differences among pasture andpecies spore abundance were tested using a Students

< 0.05. Shannon diversity and Pielou evenness wereusing a t test according to the statistical procedures

diversity indices in PAST (Hammer et al., 2001). Thek-abundance plots were compared between systemsolmogorovSmirnov two-sample test (Tokeshi, 1993).

post hoc tests were performed in JMP (SAS Institute,

iate analyses were applied using PCORD 6.0 to infers between AMF spore abundance and soil proper-st used detrended correspondence analysis (DCA) tose variable data (spore abundance) to estimate het-in species abundance throughout the length of thefter conrming the length of the gradient on the rstrincipal component analysis (PCA) was carried out tonships between AMF spore abundance and soil prop-ivariate analyses were applied to AMF species that hadf occurrence higher than 10%.

was signicantly higher in pasture (5.21) compared.46) (Table 1). Values of P, K, Ca, and Al were sig-igher in forest and those of Fe and Cu levels werey higher in pasture. Organic matter did not differ sig-etween both systems (Table 1).f 36 species were recovered from both systems and 25ied to the species level (Table 2). Twenty two speciesered from pasture and 25 were found under forest.

P.L. Leal et al. / Applied Soil Ecology 71 (2013) 72 80 75

Table 2Spore abundance (in 100 cm3 soil) of AMF species found in soils of pasture (PS) and forest (FO) in Brazilian western Amazon region. Data are means standard error.

AMF species PS FO Signicance a

Family AcaulosporaceaeAcaulospora 14.Acaulospora Acaulospora 1.5 Acaulospora 2.2 Acaulospora 31 a Acaulospora 1.7 Acaulospora Acaulospora 0.1Acaulospora Acaulospora 0.1Acaulospora 0.6Acaulospora 29.Acaulospora 0.3Family GlomGlomus austrGlomus corym 0.3Glomus glomGlomus lacteGlomus tortuRhizophagus 0.4Rhizophagus 1.0Glomus 01 Glomus 02 Glomus 04 0.8Glomus 08 Glomus 09 2.0Glomus 12 Glomus 15Glomus 16

Family GigaGigaspora 01ScutellosporaScutellosporaScutellosporaScutellospora

Family DiveDiversispora

Family ArchArchaeospora

Family AmbAmbispora a

a Species with

trappei (Ampora appenexclusivelyrespectivelywas not sAcaulospora& Morton,Ambispora ature while and A. scroforest (Tabl

Only eigthan 30% ofgedanensis, colombianaspecies recmellea were

Spore ab779 in pastsignicantlyaging 255 arichness pespecies richcolombiana (Spain & Schenck) Kaonongbua, Bever & Morton 47.7delicata Walker, Pfeiffer & Trappe elegans cf 4.0 foveata Trappe & Janos 4.9 gedanensis cf 83 laevis Gerd. & Trappe 2.0 mellea cf. rehmii Sieverding & Toro 0.15scrobiculata Trappe spinosa Walker & Trappe 0.23tuberculata Janos & Trappe 0.76walkeri Kramadibrata & Hedger 42.701 0.53

eraceaeale cf. biforme Blaszkowski 0.30

erulatum Sieverding um cf. osum Schenck & Smith

clarus (Nicolson & Schenck) Walker & Schussler 1.00 intraradices (Schenck & Smith) Walker & Schussler 1.38

0.84 2.07

52.15 304.07 2.9

sporaceae

biornata Spain, Sieverding & Toro 0.07 0.0 pellucida (Nicolson & Schenck) Walker & Sanders 0.07 0.0 scutata Walker & Diederichs 01

rsisporaceae spurca cf. 3.31 2.0aeosporaceae

trappei (Ames & Linderman) Morton & Redecker 0.53 0.5isporaceaeppendicula (Spain, Sieverding & Schenck) Walker 3.31 1.5

signicantly higher number of spores in pasture or forest are indicated by PS and FO, res

es & Linderman) Morton & Redecker, and Ambis-dicula (Spain, Sieverding & Schenck) Walker. Species

found in pasture and forest numbered 11 and 14, (Table 2). Spore abundance of most AMF speciesignicantly different between pasture and forest.

colombiana (Spain & Schenck) Kaonongbua, Bever A. elegans cf, A. gedanensis cf., Glomus 15, andppendicula were signicantly more abundant in pas-A. delicata Walker, Pfeiffer & Trappe, A. mellea cf.,

biculata Trappe were signicantly more abundant ine 2).ht AMF species in each system were detected in more

the samples and among those only three (Glomus 15, A.and A. foveata) were shared between systems (Fig. 1). A., A. gedanensis cf., and Glomus 15 were the most frequentovered in pasture while Glomus 15, A. delicata, and A.

the most frequent species in forest.undance per sample (100 cm3 soil) ranged from 25 toure and from 11 to 139 in forest. Spore abundance was

different between pasture and forest (P < 0.05) aver-nd 58 spores/100 cm3 soil, respectively (Fig. 2). Speciesr sample ranged from 35 to 10 in both systems. Meanness was not signicant differences between pasture

(7.0) and fonot signic

Species depicted folog of sporesteep initiathe initial scf., Glomus 1resulted froA. mellea. Kture and foon the patte

From thaxis was comethod yieand 2.49, rethe variabildiagram (Fitially in a hmellea, A. spabundant a

Studies found that 9 PS30.7 11.7 FO PS1.2 0.6 ns11 6 b PS ns3.5 1.5 FO

ns1.54 1.01 FO

6 0.63 0.36 ns2 0.72 0.48 ns1 1.1 0.70 ns3 ns

0.09 0.09 ns0 1.45 0.69 ns

0.36 0.24 ns0.27 0.27 ns0.27 0.27 ns

8 ns1 ns

0.63 0.63 ns0.18 0.18 ns

4 1.45 1.45 ns0.27 0.19 ns

7 ns0.09 0.09 ns.01 2.00 0.57 PS3 ns

0.27 0.19 ns7 ns7 0.09 0.09 ns

0.09 0.09 ns0.27 0.19 ns

0 ns

3 0.45 0.24 ns

3 0.09 0.09 PSpectively. ns, not signicant.

rest (6.1). Shannon diversity and Pielous evenness wereantly different between both systems (Fig. 2).abundance distribution for AMF community was

r pasture and forest by ranking AMF species against the abundance (Fig. 3). For both systems, the curves had al slope suggesting a log normal distribution. For pasture,teep slope was due to high abundance of A. gedanensis5, A. colombiana, and A. mellea. In forest the steep slopem high sporulation by A. delicata, A. gedanensis cf., andolomogorov-Smirnov two sample test comparing pas-rest (D0.01, 22, 25 = 250) yielded no statistical differencesrn of species abundance distribution between systems.e DCA analyses, the length of the gradient of the rstmputed to be 3.22. PCA used as the linear ordinationlded eigenvalues of the rst and second axes of 3.63spectively. The rst two axes of PCA explained 38.3% ofity in species abundance data. The resulting ordinationg. 4) indicates that most species sporulated preferen-igher soil pH. Acaulospora scrobiculata, A. tuberculata, A.inosa, A. delicata and Glomus corymbiforme were moret relatively higher Ca and CEC.surveying AMF species richness in tropical forestmycorrhizal communities are dominated by species of

76 P.L. Leal et al. / Applied Soil Ecology 71 (2013) 72 80

20 40 60 80 0 100

Acaulospora colombiana

Acaulospora gedanensis

Glomus15

Acaulospora foveata

Acaulospora elegans

Ambispora leptoticha

Rhizophagus clarus

Diversispora spurca cf

G

Acaulospora delicata

Acaulospora mellea

Acaulospora foveata

Acaulospora scrobiculata

Acaulospora spinosa

Glomus corymbiforme

Acaulospora gedanensis

Pasture

Forest

Fig. 1. Frequein pasture andbetween syste

Acaulosportern was theof species iTotal numbto 14) beinget al. (1992areas of trostudies detAmazon tro

forest (Lovelock et al., 2003) than to any other forest site (Table 4).Communities of AMF in tropical forest in distinct continents arehighly dissimilar as only 11% of the comparisons yielded a similaritycoefcient 0.50 (Table 4).

4. Discussion

We provided data to support the working hypothesis that con-version of pristine Amazon forest to managed pasture provokeschanges to AMF species composition while not affecting speciesabundance distribution and species richness. We acknowledgethat our results are from eld-collected spores and that someAMF species could not be represented in our study if they werenot sporulating at the sampling time. Previous results from trapcultures (Leal et al., 2009) revealed only two additional species(Gigaspora margarita, Entrophospora infrequens) in trap culturesestablished with distinct hosts, suggesting that most of AMFcommunity composition is represented in this study. Forest siterepresented a climax area of tropical Amazon forest subject only tonatural succession process while the pasture area was submitted tothe slash-and-burn practice to remove native vegetation followingcropping with sugarcane and nally, establishment of grass speciesfor pasture since approximately 42 years ago. Despite the high dis-turbance imposed by changes in plant species and soil conditionswhen converting forest to pasture, species abundance distribution,species richness and diversity indices were not affected negatively.

ncy ed byical silienld noure aiversusly

num

Table 3Number of spe

Continent/st

AsiaZhao et al. (2

AfricaWilson et alMason et al.

Central AmePicone (2000Johnson andLovelock et aGavito et al.Aguilar-FernVioli et al. (2Guadarrama

(1999) [MMangan et a

South AmerPena-VenegThis study [Blomus15

200 40 60 80 100

Frequency (%)

ncy of occurrence (%) of the most commonly recovered AMF species forest. Bars not lled evidence the most frequent species sharedms.

Resiliedetectin tropthis reit shouin pasthigh dprevio

The

aceae or Glomeraceae (Table 3). Exception to this pat-

study of Violi et al. (2008) in Mexico where the numbern Gigasporaceae was the same of that in Glomeraceae.er of species per study varied widely, the lowest (12

found in plantations of Terminalia in Africa by Wilson) and Mason et al. (1992) and the largest (37) in threepical forest in Mexico by Violi et al. (2008). Most ofected 15 to 26 AMF species. The AMF community inpical forest was more similar to Costa Ricas tropical

est and pastropical soiand Picone forest and precovered 1Aguilar-Fernumber betsion. Violi eto 21 in a

cies of arbuscular mycorrhizal fungi by family in tropical forest around the world. Numbe

udies Country Number ofsamples

Gigasporaceae

003) [CH] China 118 2

. (1992) [CI] Cote dIvoire 2 (1992) [CM] Cameroon 282 2

rica) [NC] Costa Rica/Nicaragua 57 4 (1)

Wedin (1997) [CR1] Costa Rica 10 3 l. (2003) [CR2] Costa Rica 97 2 (2)

(2008)[MX1] Mexico 90 3 (1) ndez et al. (2009) [MX2] Mexico 3 (1) 008) [MX3] Mexico 54 8 (2)

and lvarez-SnchezX4]

Mexico 60 1(1)

l. (2004) [PN] Panama 144 1

icaas et al. (2007) [CO] Colombia 90 1 (1) R] Brazil 11 2 (2) of AMF community in tropical soils has been already Picone (2000) in Central America when studying AMFforests and pastures. From an ecological point of view,cy is a positive attribute of mycorrhizal community ast be a limitation for plant natural succession to occurreas (Picone, 2000) and contributes to maintenance ofity of AMF in distinct land use in Amazonian soils asreported (Strmer and Siqueira, 2011).ber of AMF species recovered from pristine Amazon for-ture land is similar to the one found in other studies inls comparing these systems. Johnson and Wedin (1997)(2000) found 24 and 25 species, respectively, in tropicalasture in Central America. In Mexico, Gavito et al. (2008)8 AMF species in pasture and 29 species in Forest, whilenandez et al. (2009) found minor differences in speciesween forests and pasture sites after one year of conver-t al. (2008) found 25 species in mature forest compareddjacent pasture. In the Amazon region of Colombia,

r in parenthesis represents non-identied species within each family.

Acaulosporaceae Glomeraceae Otherfamilies

Total speciesrichness/study

9 15 0 26

4 5 1 125 6 1 14

8 (1) 5 (4) 3 265(5) 6(4) 1 246 (3) 2 (2) 0 174 (3) 7 (9) 2 292 (2) 5 (2) 0 1510 (4) 6 (4) 3 372(1) 2(9) 0 16

5 1(9) 0 15

3(1) 2(9) 1 188 5 (6) 2 25

P.L. Leal et al. / Applied Soil Ecology 71 (2013) 72 80 77

0

2

4

6

8

Pasture Forest

2

0.6

0.7

a

0

50

100

150

200

250

300

350

Pasture Forest

b

aa

a a aa

Me

an

AM

F s

po

res (

in 1

00

ml so

il)

Me

an

sp

ecie

s r

ich

ne

ss

x (

H)

(J)

A) B)

C) D)

Fig. 2. Compa soil)Pielous evenn ntly d

Pena-Venegspecies (18combined wtant insighrelationshipa low planthe alpha dnumber in cal regions communitiecontaining

Composbetween Amat the famiaceae werespecies reco

her svergr

Table 4Coefcient of s

CR1 MX1 MX2 CR2 CH MX3 CI CM BR

NC, Picone (20Violi et al. (2000

0.5

1

1.5

Pasture Forest

0

0.1

0.2

0.3

0.4

0.5

Sh

an

no

n d

ive

rsity in

de

Pie

lou

s e

ve

nn

ess

rison of pasture and forest areas according to (a) mean of AMF spores (in 100 cm3

ess. Within each graph, bars with different letters indicate that values are signica

as et al. (2007) also found the same number of AMF) when comparing forest and pasture areas. Our results

in anotland eith others found in tropical forest soils provide impor-t into the debate on plant versus fungal diversity, as the conversion of a high plant diversity forest tot diversity pasture area had no signicant effect oniversity of AMF species. Moreover, similar AMF speciestropical forest areas occurring in distinct geographi-supports the principle of convergence, i.e. independents from similar habitats in different parts of the world

similar number of species (Schluter and Ricklefs, 1993).ition of mycorrhizal fungal community is also shared

azon forest and other American tropical forest sitesly level. In this study, Acaulosporaceae and Glomer-

the most speciose families accounting for 19 out of 25vered in forest sites. Both families were also dominant

Lovelock ettropical for(Gavito et montane cl

Similar ture also hindices. Mehigher thantine forest aAmazon foLovelock eta mean speest areas anin Costa Ric

imilarity of arbuscular mycorrhizal fungal community in tropical forest.

NC CR1 MX1 MX2 CR2

0.460.28 0.190.17 0.32 0.460.38 0.24 0.23 0.100.52 0.44 0.38 0.27 0.380.38 0.23 0.23 0.16 0.27 0.44 0.22 0.21 0.36 0.45 0.53 0.27 0.20 0.25 0.42 0.32 0.19 0.30 0.07 0.52

00); CR1, Johnson & Wedin (1997); MX1, Gavito et al. (2008); MX2, Aguilar-Fernndez e8); CI, Wilson et al. (1992); CM, Mason et al. (1992); BR, this study.Pasture Forest

, (b) mean species richness, (c) Shannons index of diversity, and (d)ifferent (P < 0.05).

ite of Amazon forest (Pena-Venegas et al., 2007), in low-een forest in Nicaragua and Costa Rica (Picone, 2000; al., 2003) and Panama (Mangan et al., 2004), and dryest in Costa Rica (Johnson and Wedin, 1997) and Mexicoal., 2008; Aguilar-Fernandez et al., 2009) and tropicaloud forest in Mexico (Violi et al., 2008).to other studies, conversion of Amazon forest to pas-ad no effect on mean species richness and diversityan species richness found in this study (6.1 to 7.0) was

that found by Pena-Venegas et al. (2007) studying pris-nd pastures within the same geographic region of the

rest and values found in Costa Rica tropical forest by al. (2003). However, Johnson and Wedin (1997) foundcies richness of ca. 13 when comparing dry tropical for-d pasture land dominated by the grass Hyparrhenia rufaa. Diversity indices were also not signicantly different

CH MX3 CI CM

0.410.47 0.250.50 0.34 0.530.23 0.27 0.34 0.25

t al. (2009); CR2, Lovelock et al. (2003); CH, Zhao et al. (2003); MX3,

78 P.L. Leal et al. / Applied Soil Ecology 71 (2013) 72 80

1

10

100

1000

10000

1

Pasture

Species rank

Lo

g s

po

re a

bu

nd

an

ce

1000

100

10000Forest

10

Fig. 3. Rank/log abundance distribution of AMF species in pasture and forest.

between forest and pasture in studies conducted by Picone (2000)and Johnson and Wedin (1997).

We depicted and compared AMF species abundance distributionin both systems by plotting species rank against the log of sporeabundance. Species abundance distributions (SADs) summarize a

community by combining information on species richness andabundance (Dumbrell et al., 2009). In our study, both systemstended to follow a log normal distribution and SADs were notsignicantly different between pasture and forest. This providesevidence that extreme differences of plant communities regardingplant species life form, plant physiology, plant diversity and above-ground productivity are not impacting the commonness and rarityof AMF species. Both systems shared few AMF species that werevery abundant and the majority of AMF species that were less abun-dant, a universal pattern of SADs observed for plant and animalsbut seldom examined in microbial communities (Dumbrell et al.,2009). This pattern has been detected for AMF communities fromseveral Brazilian ecosystems by Strmer and Siqueira (2006) basedon spore abundance data and for 32 data sets from distinct habi-tats by Dumbrell et al. (2009) based on molecular techniques. Intropical forest of Costa Rica, Lovelock et al. (2003) found an over-whelming dominance of Acaulospora mellea and A. morrowiae thattogether accounted for 98% of the spores. In this study, four speciesaccounted for 88% of the spores in pasture and three species wereresponsible for 57% of the sporulation in forest, demonstrating thatonly few species sporulate profusely within the AMF communitiesstudied. Among the most abundant species found in both systems,sporulation of Glomus 15, A. colombiana and A. gedanensis was inu-enced by soil pH while sporulation of A. mellea and A. delicate wereassociated with Ca and CEC. Soil pH is well known to inuencespore abundance and occurrence of AMF species (Siqueira et al.,1989), but we do not have a reasonable explanation for the roleof Ca and CEC to inuence AMF sporulation, although Ca and pH

AdelAscr

Ael e

Awal

Gcor

Gl15

Aml e

1

3

Fig. 4. DiagramA. elegans; AcoDiversispora spAmel

Aspi

Atub

Ca

CECAxis

2Ag

DspuArt p

-3 -1

-3

-1

Axis 1

of a PCA of arbuscular mycorrhizal fungal abundance with soil pH, Ca, and cation exchal, A. colombiana; Afov, A. foveata; Aged, A. gedanensis cf; Atub, A. tuberculata; Amel, A. urca; Gcor, Glomus corymbiforme; Gl15, Glomus 15; Rcla, Rhizophagus clarus; Amle, Ambied AfovAcol

Rcla

1 3

pH

nge capacity in pasture and forest. (Awal, Acaulospora walkerii; Aele,mellea; Aspi, A. spinosa; Ascr, A. scrobiculata; Adel, A.delicata; Dspu,spora leptoticha; Artp, Archaeospora trappei.)

P.L. Leal et al. / Applied Soil Ecology 71 (2013) 72 80 79

are often found to covary. Nevertheless, these results show howlimited is our knowledge about the inuence of soil factors on AMFsporulation.

Differences between Amazon forest and pasture lands werefound in thiwere four-fP = 0.05, t = 2who detectcompared tin pasture tto multiplydecumbens that grasslamature forerhizal colonforest and 2012). Althferences onthese ndinbe related ticantly high

Qualitatwas the mamong the ethree were most frequethe second eight most quency in bwere also dnensis was of Acaulospture while tAcaulosporaone of the mempty spormus 15 founand one of t

Compariin distinct pof distributemerged fro(a) Numbercommunitiein this ecosfrom these is within thplant in trodata. Consistudies andilarity indexof tropical from the 70culated simA. mellea, A.pellucida we

In concluresilience west to a maresiliency isspecies as fproduction based on thnot distinctsition and tin forest are

forests elsewhere, suggesting convergence of AMF diversity in trop-ical forest.

Acknowledgments

thangicoumbe7/200Procndile Maentsia, K

Tropith cnd imnt Pra (Use o

thors ackn

Ma revutio

nces

.P., C Serra.), Maa AtlnFern

consi of a g, T., DImpac, M.Ao do us etadadoM.R., F, Moreation icpionvolv., Aria

esiculaystemducedll, A.J.y and orrhizA, 199neiroez, M.equentropicE.C.C.,ing, J.BiosBiversiimentM.E., Ptnez-al comystemann, Jacted 244., A.Wegier,orrhizhem. 4ama, Pi spororrhizs study regarding the mean number of AMF spores thatold higher in pasture compared to forest (paired t test,.07). Similar results were found by Siqueira et al. (1989)

ed low sporulation of AMF in the savanna-like Cerradoo agrosystems. We can attribute the high sporulationo the fact that grass species are generally good hosts

AMF. Carneiro et al. (1995) observed that Brachiariaincreased up to 400% sporulation of AMF. It is knownd species have more abundant ne-root system than ast and this correlates positively with arbuscular mycor-ization and sporulation across the Pantanal, AtlanticAraucaria forest ecosystems in Brazil (Zangaro et al.,ough no root traits were measured in our study, dif-

spore abundance between pasture and forest supportgs. Moreover, lower sporulation levels in forest mighto the higher P soil found in this system that was signif-er than in pasture.ive difference in the composition of AMF communityain component to set apart forest and pasture. First,ight most frequent species found in both systems, onlyshared between pasture and forest. Glomus 15 was thent in forest and third on pasture, A. gedanensis cf. was

most frequent in pasture but ranked the last among thefrequent in forest while A. foveata ranked fourth in fre-oth systems. Second, the most abundant AMF speciesistinct between pasture and forest and only A. geda-shared as one of the abundant species. Third, numberora species was slightly higher than Glomus in pas-he opposite occurred in forest. Picone (2000) reported

foveata and a Glomus small brown (90130 m) asost common species producing a large number of dead

es in forest and pasture sites. The latter is similar to Glo-d herein, a species producing brown rod-shaped sporeshe most common species in our study.son of community from the same ecosystem occurringarts of the world is a rst step to establish a pattern

ion of AMF species, genera and families. Two patternsm comparisons of AMF communities in tropical forest:

of AMF species per study ranges widely, and (b) AMFs are dominated by Acaulosporaceae and Glomeraceae

ystem. Indeed, the average number of species recordedspore-based surveys was 21 species per study and ite range of the number of AMF species found per hostpical forest by pik et al. (2010) based on moleculardering that the sampling size was dissimilar between

the sampling intensity affects the outcome of the sim-, it is clear that AMF communities from different sites

forest around the world are highly dissimilar. In fact, AMF species identied in the ten studies used to cal-ilarity index, Sclerocystis clavispora, Acaulospora foveata,

scrobiculata, A. spinosa, A. tuberculata, and Scutellosporare the only species found in at least six studies.sion, we demonstrated that AMF community has a highhen experiencing a change from tropical Amazon for-naged pasture land. One possible mechanism for this

the shifting of the most abundant and most frequentorest is converted to pasture, following by large sporeof the entire fungal community. This explanation ise fact that most of AMF communitys descriptors were

between forest and pasture, except taxonomic compo-otal number of spores. Number of AMF species founda in this study was similar to others found for tropical

WeTecnolcess n30266PNPD, of the tainabimplemIndoneby theCIAT wGEF), aronmeMoreirare thothe auis alsodebt toEnglishcontrib

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Aguiar, Ae da(EdsMat

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Coelho, D.V.servMunDese

Dodd, J.Cof vecosintro

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GuadarrfungMyck Conselho Nacional de Desenvolvimento Cientco e (CNPq), Brazil, for research grants to J.O. Siqueira (Pro-r 304781/2006-1) and S.L. Strmer (Process number9-1). PLL thanks CAPES for an assistantship (Programess number 0113085). This publication presents partngs of the international project Conservation and Sus-nagement of Below-Ground Biodiversity (CSM-BGBD),ed in seven countries Brazil, Cte dIvoire, India,enya, Mexico, and Uganda. This project is coordinatedical Soil Biology and Fertility Institute of CIAT (TSBF-o-nancing from the Global Environmental Facility plementation support from the United Nations Envi-

ogram (UNEP), and coordinated in Brazil by Dr. F.M.S.FLA, Lavras, MG). Views expressed in this publicationf their authors and do not necessarily reect those of organization, the UNEP and the GEF. Carlos R. Grippaowledged for contribution to soil sampling. We are inrta Helena Crio de Caetano and Greici Buzzi for theiew and two anonymous reviewers for their valuablen to this paper.

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Switch of tropical Amazon forest to pasture affects taxonomic composition but not species abundance and diversity of arbus...1 Introduction2 Material and methods2.1 Study area2.2 Sampling design2.3 Soil chemical characteristics2.4 Spore extraction and species identification2.5 AMF community analysis2.6 Surveyed publications2.7 Statistical analysis

3 Results4 DiscussionAcknowledgmentsReferences