Applied Soil Ecology 71 (2013) 7280

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Applied Soil Ecology

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Switch of tropical Amazon forest to pasture affects taxonomic composition but not species abundance and diversity of arbuscular mycorrhizal fungal community
Patricia Lopes Leal a , Jos Oswaldo Siqueira a,b , Sidney Luiz Strmer c,
a

Universidade Federal de Lavras (UFLA), Departamento de Cincias do Solo (DCS), Cx.P. 37, 37200-000 Lavras, MG Brazil Instituto Tecnolgico Vale, Brazil c Universidade Regional de Blumenau (FURB), Departamento de Cincias Naturais (DCN), Cx.P. 1507, 89012-900 Blumenau, SC, Brazil
b

a r t i c l e

i n f o

a b s t r a c t
Arbuscular mycorrhizal fungi (AMF) community composition and species richness are affected by several factors including soil attributes and plant host. In this paper we tested the hypothesis that conversion of tropical Amazon forest to pasture changes taxonomic composition of AMF community but not community species abundance and richness. Soil samples were obtained in 300 m 300 m plots from forest (n = 11) and pasture (n = 13) and fungal spores extracted, counted and identied. A total of 36 species 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 did not differ between pasture and forest. Spore abundance was signicantly higher in pasture compared to forest 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 different between both systems. We concluded that conversion of pristine tropical forest to pasture inuences the taxonomic composition of AMF communities while not affecting species richness and abundance distribution. 2013 Elsevier B.V. All rights reserved.

Article history: Received 6 September 2012 Received in revised form 15 May 2013 Accepted 16 May 2013 Keywords: Land use Species richness Glomeromycota Spore abundance Community structure Mycorrhiza

1. Introduction Arbuscular mycorrhizal fungi (AMF Phylum Glomeromycota) are an important component of soil biota in natural and agroecosystems where they establish the arbuscular endomycorrhizal symbiosis with plant roots. In this association, AMF grow and differentiate into typical structures inside the root cortex and spread out their absorptive hyphae into the bulk soil to uptake low mobility nutrients like phosphorus and zinc (Smith and Read, 2008). Nutrients are then transferred to their host resulting in improved plant growth rates and nutrition; external mycelium of AMF also improves soil aggregation through physical entanglement of soil particles by hyphae and production of glomalin-like protein (Purin and Rillig, 2007; Gillespie et al., 2011). These functions render the AMF and the symbiosis particularly important in highly weathered low fertility tropical soils, where mycorrhizal association impacts survival and growth of tropical woody species (Siqueira and

Corresponding author at: Departamento de Cincias Naturais, Universidade Regional de Blumenau, Cx.P. 1507, 89012-900 Blumenau, SC, Brazil, Tel.: +55 47 3321 0272/55 47 321 0470; fax: +55 47 3321 0232. E-mail address: sturmer@furb.br (S.L. Strmer). 0929-1393/$ see front matter 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.apsoil.2013.05.010

Saggin-Jnior, 2001) and also inuences plant succession and recovery of degraded areas (Scabora et al., 2010). Switches in land use exert a differential effect upon AMF, causing changes in fungal community structure by altering distribution and dominance of species. Causal effects for these changes are alterations to soil chemical properties (Siqueira et al., 1989), soil management (Jansa et al., 2002), and plant community (Oehl et al., 2003). Considering that different AMF species and fungal isolates within species have differential effects on plant growth and nutrition, changes on fungal communities caused by switches in land use can impact host establishment and development (Dodd et al., 1990) and plant diversity and ecosystem productivity (Van der Heijden et al., 1998). In the tropics, conversion of areas of native tropical forest to pasture and agricultural crops is one of the main switches in land use system and represent a casual factor in forest degradation (Aguiar et al., 2005; Siqueira et al., 1989). The impacts of changing from a high diversity woody-species dominated forest system to a low diversity graminoid-species dominated pasture upon AMF communities have been evaluated in tropical countries of Central America. In Nicaragua and Costa Rica, Picone (2000) found roughly the same AMF species richness in forest and pasture but spore abundance of most species was higher in the former than in the

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latter. Both systems also contained similar AMF communities and shared the most frequent species. Johnson and Wedin (1997) found no differences on total spore number, mean species richness and Simpsons diversity index when comparing grassland sites dominated by the exotic grass Hyparrhenia rufa (Ness) Stapf. adjacent to tropical dry forest in Costa Rica. The study also showed that AMF communities were similar between both systems that also shared the most abundant species. In Mexico, Gavito et al. (2008) sampled two sites of each primary forest, secondary forest and pasture and detected 29 and 18 AMF species in a pasture and primary forest, respectively, with only 10 species being shared between systems. However, some of the sites of primary and secondary forest had the same number of species of those found in pasture. Fernndez et al. (2009) compared the AMF community in a pasture site established after slash-and-burn with adjacent tropical dry forest in Mexico and observed that AMF species richness and spore numbers were similar between both systems. AMF community composition was similar between pasture and forest, sharing 13 species and resulting in Sorenson similarity above 80%. The Amazon forest is considered one of the main hotspots of global biodiversity. Despite this status, anthropogenic disturbance has caused deforestation of pristine forest to be used for agriculture and beef cattle ranching, both accounting for more than 90% of deforestation in the 1980s (Amelung and Diehl, 1992). Traditional human communities also convert pristine Amazon Forest through the slash-and-burn practice to distinct land use like orchards, agroforestry systems, and crop elds for subsistence (Mendonc a-Santos et al., 2006). However, impacts generated by turning pristine Amazon forest into distinct land use systems on AMF are still scarce (Leal et al., 2009; Strmer and Siqueira, 2011). In a study in the et al. (2007) observed Amazon region of Colombia, Pena-Venegas that average species richness was 4.5 and 4.6 in pristine forest and pasture, respectively, and a total of 18 AMF species were found in both systems. This study is part of a broader project entitled Conservation and Sustainable Management of Below-Ground Biodiversity (CSM-BGBD), co-funded by the Global Environment Facility with implementation support of the United Nations Environment Program and developed in seven tropical countries. In Brazil, the benchmark area of this project was in the western portion of the Brazilian state of Amazon, in the border with Peru and Colombia, where the landscape is a mosaic of pristine forest and secondary forest at distinct stages of regeneration adjacent to agroforestry systems, orchards and small crop areas created by traditional human communities (Fidalgo et al., 2005). In this paper, we aimed to compare several attributes of AMF communities occurring in pristine Amazon forest and a pasture area used for cattle ranching. As a corollary of previous studies comparing tropical forest and pasture, we tested the hypothesis that converting pristine forest to pasture changes the composition of AMF communities but not AMF species abundance and richness.

was located in the rural community of Guanabara, which is a territory occupied by Ticuna cultures. Cambissolos (Inceptsols) are the dominant soils in both areas (Coelho et al., 2005). The Pasture area is covered by imperial grass (Axonopus scoparius), brachiaria grass (Brachiaria brizantha, B. humidicola), bahiagrass (Paspalum notatum), and several invasive plants. The site was originally covered by terra rme forest, cleared in 1945 for establishment of sugarcane and converted to pasture in 1970 for cattle ranching. The Forest area is typical pristine terra rme forest representative of the western Brazilian Amazon forest and neither deforestation nor selective logging has occurred. A total of 599 plant species has been registered with the most abundant being Heliconia juruana, Heterostemon ellipticus, Pariana radiciora, Cecropia concolor, Rinorea racemosa, Iriartea deltoidea, Ischnosiplon sp. and Geonoma sp. Families with high densities were Fabaceae, Araceae, Arecaceae, Myriticaceae, Cecropiaceae, Moraceae, Poaceae, and Heliconaceae (Nogueira et al., 2007). 2.2. Sampling design Grids (300 m 300 m) containing geo-referenced sampling points were established in several land use systems to follow the norms of the CSM-BGDB project (Huising et al., 2008). For this study, grids number 1 and 6 covered by Forest (n = 11 sampling points) and Pasture (n = 13 sampling points) were selected and all samples were collected during the rainy season in a eld campaign during 1015 March 2004 and detailed in Strmer and Siqueira (2011). In each sample point a wooden stick was placed as a center reference for soil sampling. Each sample was composed of 12 subsamples collected as follow: four subsamples collected 3 m from the center point and another eight subsamples collected 6 m from the center point, with four in cardinal directions and four between them. All 12 subsamples were collected with a soil core sampler (020 cm depth) and pooled into a plastic bag. Forest litter was scraped and not included in the soil sample. Soil was then homogenized in plastic trays, conditioned in new plastic bags, transported to the laboratory inside thermic boxes and kept at 4 C until processing (one to two months after sampling). 2.3. Soil chemical characteristics Soil chemical analysis were performed according to EMBRAPA (1997) and described in Moreira et al. (2009). A sub-sample from each composite sample was removed from the plastic bag, air dried and passed through a 2 mm mesh sieve before analysis. Briey, soil pH was measured in a soil:water suspension (1:2.5) and phosphorus extracted by Mehlich 1 and analyzed by spectrophotometry (660 nm). Mehlich 1 was also used to extract exchangeable K followed by photometry. KCl 1 mol L1 was used to extract exchangeable Al, Ca and Mg. Available Zn, Fe, Mn and Cu were extracted by Mehlich 1 and further determined by atomic absorption spectrometry. Organic carbon was determined by oxidation with dichromate and the value used to calculate organic matter (%). We also calculated after analysis above the sum of bases and the cation exchange capacity (CEC). 2.4. Spore extraction and species identication

2. Material and methods 2.1. Study area The benchmark area is in the municipality of Benjamin Constant (4 21 and 4 26 S, 69 36 and 70 1 W, 65 m above sea level), located in the Alto Solimes river region at the western portion of the Amazon state, Brazil. Mean annual precipitation is 2562 mm, with precipitation concentrated between December and April, and mean annual temperature is 25.7 C. Climate is Af type according to Kppen (tropical humid and superhumid with no dry season). Pasture site (PS) was located in private land in the surrounding areas of Benjamin Constant town while pristine Amazon Forest (FO)

An aliquot of 100 cm3 of soil from each sample was used to extract AMF spores following the method of wet sieving (Gerdemann and Nicolson, 1963) and sucrose gradient centrifugation (20% and 60%). Briey, soil sample was placed in a 2 L bucket, lled with tap water and swirled using a glass rod. Soil suspension was poured onto two nested sieves with 710 and 45 m opening. Material retained in the 710 m sieve was conditioned in large Petri dish and observed under dissecting microscope for large spores

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P.L. Leal et al. / Applied Soil Ecology 71 (2013) 7280 Table 1 Mean values of soil parameters in pasture (PS) and forest (FO). Within rows, means followed by different letters indicate that values are signicantly different (P 0.05). N = number of samples. Soil attributes pH P (mg dm3 ) K (mg dm3 ) Ca (cmolc dm3 ) Mg (cmolc dm3 ) Al (cmolc dm3 ) Zn (mg dm3 ) Fe (mg dm3 ) Mn (mg dm3 ) Cu (mg dm3 ) Sum of bases (cmolc dm3 ) Cation exchange capacity (cmolc dm3 ) Organic matter (dag kg1 ) Pasture (N = 13) 5.21 2.8 40.3 2.23 1.43 2.75 7.7 471.76 40.47 2.15 3.79 6.55 1.58 0.04 a 0.21 b 3.5 b 0.20 b 0.20 a 0.25 b 1.78 a 80.0 a 9.4 a 0.33 a 0.36 b 0.46 b 0.06 a Forest (N = 11) 4.46 4.1 58.7 3.63 1.94 5.14 5.85 194.5 61.79 1.22 5.71 10.85 1.55 0.03 b 0.18 a 3.7 a 0.42 a 0.13 a 0.37 a 1.48 a 17.4 b 6.9 a 0.09 b 0.41 a 0.41 a 0.08 a

and sporocarps. Material from the 45 m sieve was poured into Falcon tubes containing the sucrose gradient and centrifuged for 2000 rpm for 1 min. The supernatant was dispensed over the 45 m sieve, washed under tap water and placed on Petri dish. Spores were observed, collected and separated by morphotypes under a dissecting microscope (Zeiss Stemi-2000). Spores were mounted in permanent slides in polyvinyllactoglycerol (PVLG) and PVLG mixed with Melzers reagent. Taxonomic composition of AMF community was assessed after spores were identied through the analysis of spore wall characteristics observed under a microscope (Zeiss, Axiostar) associated with spore color, size, and shape observed under the dissecting microscope. Comparison with both original species description protocols and description of reference isolates (INVAM at West Virginia University, USA, http://www.invam.caf.wvu.edu) and Plant Pathology Department homepage at Agriculture University, Poland (http://www.agro.ar.szczecin.pl/jblaszkowski/) was used to assign morphotypes into species. 2.5. AMF community analysis Differences in AMF communities between pasture and forest areas were investigated by using a suite of community descriptors. Number of spores was counted for each species and used as a measurement of species abundance. Summing the number of spores for each species in a sample yielded the total number of spores. Frequency of occurrence of AMF species within pasture and forest was calculated as the number of samples that a species was present over the total number of samples and expressed as percentage. AMF species richness (S) was determined by counting fungal species per soil sample. Spore number was used to calculate the Shannon diversity index (H = i pi (log pi ), where pi is the relative spore abundance of ith species considering all species) and the Pielou evenness (J) according to Magurran (2004) using the PAST (PAleontological STatistics) software (Hammer et al., 2001). Spore abundance of each species was used to generate species rank-log abundance plot to depict species abundance distribution (Magurran, 2004). 2.6. Surveyed publications We surveyed twelve publications that have information on AMF species richness occurring in tropical forest in the Americas (PenaVenegas et al., 2007; Picone, 2000; Lovelock et al., 2003; Gavito et al., 2008; Aguilar-Fernandez et al., 2009; Violi et al., 2008; Guadarrama and lvarez-Snchez, 1999; Mangan et al., 2004), Africa (Wilson et al., 1992; Mason et al., 1992), and Asia (Zhao et al., 2003). For each study, the number of identied and nonidentied species pertaining to Gigasporaceae, Acaulosporaceae, Glomeraceae sensu lato and other families in the Glomeromycota was analyzed. AMF community composition between studies was compared using Srensen coefcient of similarity: C = 2w/a + b, where C = the coefcient of similarity (ranging from 0 = no similarity to 1 = complete similarity), w = the number of species common to both studies being compared, a = the number of species in one study, and b = the number of species of the other study. To calculate similarity index the following studies were not included as the number of non-identied species was higher than the number of identied: Pena-Venegas et al. (2007), Guadarrama and lvarezSnchez (1999), and Mangan et al. (2004). 2.7. Statistical analysis Total spore abundance data was log(x + 1) transformed prior to analysis to meet normality and homogeneity of variance. Differences in soil chemical properties, total spore abundance and

species richness between pasture and forest were tested using a one-way analysis of variance (ANOVA) following Tukey post hoc test (P < 0.05) and treating the number of sampling points collected in each area as replicates. Spore abundance of each species was log (x + 1) transformed and differences among pasture and forest for species spore abundance were tested using a Students t test at P < 0.05. Shannon diversity and Pielou evenness were compared using a t test according to the statistical procedures to compare diversity indices in PAST (Hammer et al., 2001). The species rank-abundance plots were compared between systems using the KolmogorovSmirnov two-sample test (Tokeshi, 1993). ANOVA and post hoc tests were performed in JMP (SAS Institute, 1995). Multivariate analyses were applied using PCORD 6.0 to infer relationships between AMF spore abundance and soil properties. We rst used detrended correspondence analysis (DCA) to the response variable data (spore abundance) to estimate heterogeneity in species abundance throughout the length of the gradient. After conrming the length of the gradient on the rst DCA axis, principal component analysis (PCA) was carried out to infer relationships between AMF spore abundance and soil properties. Multivariate analyses were applied to AMF species that had frequency of occurrence higher than 10%. 3. Results Soil pH was signicantly higher in pasture (5.21) compared to forest (4.46) (Table 1). Values of P, K, Ca, and Al were signicantly higher in forest and those of Fe and Cu levels were signicantly higher in pasture. Organic matter did not differ signicantly between both systems (Table 1). A total of 36 species were recovered from both systems and 25 were identied to the species level (Table 2). Twenty two species were recovered from pasture and 25 were found under forest. Most of the species (83%) pertained to the families Acaulosporaceae (Acaulospora) and Glomeraceae (Glomus and Rhizophagus). The genera Gigaspora, Diversispora, Archaeospora, and Ambispora were represented by only one species each while four species were identied in the genus Scutellospora (Table 2). Species richness of Acaulosporaceae was higher in pasture compared to forest while species of Glomeraceae and Gigasporaceae were in higher number in forest. Twelve species were shared between pasture and forest: Acaulospora foveata Trappe & Janos, Acaulospora gedanensis cf, Acaulospora spinosa Walker & Trappe, Acaulospora tuberculata Janos & Trappe, Acaulospora walkeri Kramadibrata & Hedger, Glomus corymbiforme Blaszkowski, Glomus 04, Glomus 15, Scutellospora pellucida (Nicolson & Schenck) Walker & Sanders, Archaeospora

P.L. Leal et al. / Applied Soil Ecology 71 (2013) 7280 Table 2 Spore 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 Family Acaulosporaceae Acaulospora colombiana (Spain & Schenck) Kaonongbua, Bever & Morton Acaulospora delicata Walker, Pfeiffer & Trappe Acaulospora elegans cf Acaulospora foveata Trappe & Janos Acaulospora gedanensis cf Acaulospora laevis Gerd. & Trappe Acaulospora mellea cf. Acaulospora rehmii Sieverding & Toro Acaulospora scrobiculata Trappe Acaulospora spinosa Walker & Trappe Acaulospora tuberculata Janos & Trappe Acaulospora walkeri Kramadibrata & Hedger Acaulospora 01 Family Glomeraceae Glomus australe cf. Glomus corymbiforme Blaszkowski Glomus glomerulatum Sieverding Glomus lacteum cf. Glomus tortuosum Schenck & Smith Rhizophagus clarus (Nicolson & Schenck) Walker & Schussler Rhizophagus intraradices (Schenck & Smith) Walker & Schussler Glomus 01 Glomus 02 Glomus 04 Glomus 08 Glomus 09 Glomus 12 Glomus 15 Glomus 16 Family Gigasporaceae Gigaspora 01 Scutellospora biornata Spain, Sieverding & Toro Scutellospora pellucida (Nicolson & Schenck) Walker & Sanders Scutellospora scutata Walker & Diederichs Scutellospora 01 Family Diversisporaceae Diversispora spurca cf. Family Archaeosporaceae Archaeospora trappei (Ames & Linderman) Morton & Redecker Family Ambisporaceae Ambispora appendicula (Spain, Sieverding & Schenck) Walker
a

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PS 47.7 14.9 4.0 1.5 4.9 2.2 83 31 a 2.0 1.7 0.15 0.1 0.23 0.16 0.76 0.62 42.7 29.1 0.53 0.33 0.30 0.30 1.00 0.48 1.38 1.01

FO 30.7 11.7 1.2 0.6 11 6 b 3.5 1.5 1.54 1.01 0.63 0.36 0.72 0.48 1.1 0.70 0.09 0.09 1.45 0.69 0.36 0.24 0.27 0.27 0.27 0.27 0.63 0.63 0.18 0.18 1.45 1.45 0.27 0.19 0.09 0.09 2.00 0.57 0.27 0.19 0.09 0.09 0.09 0.09 0.27 0.19 0.45 0.24 0.09 0.09

Signicance a PS FO PS ns PS ns FO ns FO ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns PS ns ns ns ns ns ns ns ns PS

0.84 0.84 2.07 2.07 52.15 30.01 4.07 2.93 0.07 0.07 0.07 0.07 3.31 2.00 0.53 0.53 3.31 1.53

Species with signicantly higher number of spores in pasture or forest are indicated by PS and FO, respectively. ns, not signicant.

trappei (Ames & Linderman) Morton & Redecker, and Ambispora appendicula (Spain, Sieverding & Schenck) Walker. Species exclusively found in pasture and forest numbered 11 and 14, respectively (Table 2). Spore abundance of most AMF species was not signicantly different between pasture and forest. Acaulospora colombiana (Spain & Schenck) Kaonongbua, Bever & Morton, A. elegans cf, A. gedanensis cf., Glomus 15, and Ambispora appendicula were signicantly more abundant in pasture while A. delicata Walker, Pfeiffer & Trappe, A. mellea cf., and A. scrobiculata Trappe were signicantly more abundant in forest (Table 2). Only eight AMF species in each system were detected in more than 30% of the samples and among those only three (Glomus 15, A. gedanensis, and A. foveata) were shared between systems (Fig. 1). A. colombiana, A. gedanensis cf., and Glomus 15 were the most frequent species recovered in pasture while Glomus 15, A. delicata, and A. mellea were the most frequent species in forest. Spore abundance per sample (100 cm3 soil) ranged from 25 to 779 in pasture and from 11 to 139 in forest. Spore abundance was signicantly different between pasture and forest (P < 0.05) averaging 255 and 58 spores/100 cm3 soil, respectively (Fig. 2). Species richness per sample ranged from 35 to 10 in both systems. Mean species richness was not signicant differences between pasture

(7.0) and forest (6.1). Shannon diversity and Pielous evenness were not signicantly different between both systems (Fig. 2). Species abundance distribution for AMF community was depicted for pasture and forest by ranking AMF species against the log of spore abundance (Fig. 3). For both systems, the curves had a steep initial slope suggesting a log normal distribution. For pasture, the initial steep slope was due to high abundance of A. gedanensis cf., Glomus 15, A. colombiana, and A. mellea. In forest the steep slope resulted from high sporulation by A. delicata, A. gedanensis cf., and A. mellea. Kolomogorov-Smirnov two sample test comparing pasture and forest (D0.01, 22, 25 = 250) yielded no statistical differences on the pattern of species abundance distribution between systems. From the DCA analyses, the length of the gradient of the rst axis was computed to be 3.22. PCA used as the linear ordination method yielded eigenvalues of the rst and second axes of 3.63 and 2.49, respectively. The rst two axes of PCA explained 38.3% of the variability in species abundance data. The resulting ordination diagram (Fig. 4) indicates that most species sporulated preferentially in a higher soil pH. Acaulospora scrobiculata, A. tuberculata, A. mellea, A. spinosa, A. delicata and Glomus corymbiforme were more abundant at relatively higher Ca and CEC. Studies surveying AMF species richness in tropical forest found that mycorrhizal communities are dominated by species of

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Diversispora spurca cf Rhizophagus clarus Ambispora leptoticha Acaulospora elegans Acaulospora foveata Glomus 15 Acaulospora gedanensis Acaulospora colombiana 0 20 40 60

Pasture

forest (Lovelock et al., 2003) than to any other forest site (Table 4). Communities of AMF in tropical forest in distinct continents are highly dissimilar as only 11% of the comparisons yielded a similarity coefcient 0.50 (Table 4). 4. Discussion We provided data to support the working hypothesis that conversion of pristine Amazon forest to managed pasture provokes changes to AMF species composition while not affecting species abundance distribution and species richness. We acknowledge that our results are from eld-collected spores and that some AMF species could not be represented in our study if they were not sporulating at the sampling time. Previous results from trap cultures (Leal et al., 2009) revealed only two additional species (Gigaspora margarita, Entrophospora infrequens) in trap cultures established with distinct hosts, suggesting that most of AMF community composition is represented in this study. Forest site represented a climax area of tropical Amazon forest subject only to natural succession process while the pasture area was submitted to the slash-and-burn practice to remove native vegetation following cropping with sugarcane and nally, establishment of grass species for pasture since approximately 42 years ago. Despite the high disturbance imposed by changes in plant species and soil conditions when converting forest to pasture, species abundance distribution, species richness and diversity indices were not affected negatively. Resiliency of AMF community in tropical soils has been already detected by Picone (2000) in Central America when studying AMF in tropical forests and pastures. From an ecological point of view, this resiliency is a positive attribute of mycorrhizal community as it should not be a limitation for plant natural succession to occur in pasture areas (Picone, 2000) and contributes to maintenance of high diversity of AMF in distinct land use in Amazonian soils as previously reported (Strmer and Siqueira, 2011). The number of AMF species recovered from pristine Amazon forest and pasture land is similar to the one found in other studies in tropical soils comparing these systems. Johnson and Wedin (1997) and Picone (2000) found 24 and 25 species, respectively, in tropical forest and pasture in Central America. In Mexico, Gavito et al. (2008) recovered 18 AMF species in pasture and 29 species in Forest, while Aguilar-Fernandez et al. (2009) found minor differences in species number between forests and pasture sites after one year of conversion. Violi et al. (2008) found 25 species in mature forest compared to 21 in adjacent pasture. In the Amazon region of Colombia,

80

100

Acaulospora gedanensis Glomus corymbiforme Acaulospora spinosa Acaulospora scrobiculata Acaulospora foveata Acaulospora mellea Acaulospora delicata Glomus 15 0 20 40 60

Forest

80

100

Frequency (%)
Fig. 1. Frequency of occurrence (%) of the most commonly recovered AMF species in pasture and forest. Bars not lled evidence the most frequent species shared between systems.

Acaulosporaceae or Glomeraceae (Table 3). Exception to this pattern was the study of Violi et al. (2008) in Mexico where the number of species in Gigasporaceae was the same of that in Glomeraceae. Total number of species per study varied widely, the lowest (12 to 14) being found in plantations of Terminalia in Africa by Wilson et al. (1992) and Mason et al. (1992) and the largest (37) in three areas of tropical forest in Mexico by Violi et al. (2008). Most of studies detected 15 to 26 AMF species. The AMF community in Amazon tropical forest was more similar to Costa Ricas tropical

Table 3 Number of species of arbuscular mycorrhizal fungi by family in tropical forest around the world. Number in parenthesis represents non-identied species within each family. Continent/studies Asia Zhao et al. (2003) [CH] Africa Wilson et al. (1992) [CI] Mason et al. (1992) [CM] Central America Picone (2000) [NC] Johnson and Wedin (1997) [CR1] Lovelock et al. (2003) [CR2] Gavito et al. (2008)[MX1] Aguilar-Fernndez et al. (2009) [MX2] Violi et al. (2008) [MX3] Guadarrama and lvarez-Snchez (1999) [MX4] Mangan et al. (2004) [PN] South America Pena-Venegas et al. (2007) [CO] This study [BR] Country Number of samples 118 Gigasporaceae Acaulosporaceae Glomeraceae Other families 0 1 1 3 1 0 2 0 3 0 0 1 2 Total species richness/study 26 12 14 26 24 17 29 15 37 16 15 18 25

China Cote dIvoire Cameroon Costa Rica/Nicaragua Costa Rica Costa Rica Mexico Mexico Mexico Mexico Panama Colombia Brazil

2 2 2 4 (1) 3 2 (2) 3 (1) 3 (1) 8 (2) 1(1) 1 1 (1) 2 (2)

9 4 5 8 (1) 5(5) 6 (3) 4 (3) 2 (2) 10 (4) 2(1) 5 3(1) 8

15 5 6 5 (4) 6(4) 2 (2) 7 (9) 5 (2) 6 (4) 2(9) 1(9) 2(9) 5 (6)

282 57 10 97 90 54 60 144 90 11

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Mean AMF spores (in 100 ml soil)

350 300 250 200 150 100 50 0

A)

a
Mean species richness

B)

a a

Pasture

Forest

Pasture

Forest

2 Shannon diversity index (H)

C)

a
Pielous evenness (J)

0.7 0.6 0.5 0.4 0.3 0.2 0.1

D)

1.5

0.5

0 Pasture Forest

0 Pasture Forest

Fig. 2. Comparison of pasture and forest areas according to (a) mean of AMF spores (in 100 cm3 soil), (b) mean species richness, (c) Shannons index of diversity, and (d) Pielous evenness. Within each graph, bars with different letters indicate that values are signicantly different (P < 0.05).

Pena-Venegas et al. (2007) also found the same number of AMF species (18) when comparing forest and pasture areas. Our results combined with others found in tropical forest soils provide important insight into the debate on plant versus fungal diversity relationship, as the conversion of a high plant diversity forest to a low plant diversity pasture area had no signicant effect on the alpha diversity of AMF species. Moreover, similar AMF species number in tropical forest areas occurring in distinct geographical regions supports the principle of convergence, i.e. independent communities from similar habitats in different parts of the world containing similar number of species (Schluter and Ricklefs, 1993). Composition of mycorrhizal fungal community is also shared between Amazon forest and other American tropical forest sites at the family level. In this study, Acaulosporaceae and Glomeraceae were the most speciose families accounting for 19 out of 25 species recovered in forest sites. Both families were also dominant

in another site of Amazon forest (Pena-Venegas et al., 2007), in lowland evergreen forest in Nicaragua and Costa Rica (Picone, 2000; Lovelock et al., 2003) and Panama (Mangan et al., 2004), and dry tropical forest in Costa Rica (Johnson and Wedin, 1997) and Mexico (Gavito et al., 2008; Aguilar-Fernandez et al., 2009) and tropical montane cloud forest in Mexico (Violi et al., 2008). Similar to other studies, conversion of Amazon forest to pasture also had no effect on mean species richness and diversity indices. Mean species richness found in this study (6.1 to 7.0) was higher than that found by Pena-Venegas et al. (2007) studying pristine forest and pastures within the same geographic region of the Amazon forest and values found in Costa Rica tropical forest by Lovelock et al. (2003). However, Johnson and Wedin (1997) found a mean species richness of ca. 13 when comparing dry tropical forest areas and pasture land dominated by the grass Hyparrhenia rufa in Costa Rica. Diversity indices were also not signicantly different

Table 4 Coefcient of similarity of arbuscular mycorrhizal fungal community in tropical forest. NC CR1 MX1 MX2 CR2 CH MX3 CI CM BR 0.46 0.28 0.17 0.38 0.52 0.38 0.44 0.53 0.32 CR1 0.19 0.32 0.24 0.44 0.23 0.22 0.27 0.19 MX1 MX2 CR2 CH MX3 CI CM

0.46 0.23 0.38 0.23 0.21 0.20 0.30

0.10 0.27 0.16 0.36 0.25 0.07

0.38 0.27 0.45 0.42 0.52

0.41 0.47 0.50 0.23

0.25 0.34 0.27

0.53 0.34

0.25

NC, Picone (2000); CR1, Johnson & Wedin (1997); MX1, Gavito et al. (2008); MX2, Aguilar-Fernndez et al. (2009); CR2, Lovelock et al. (2003); CH, Zhao et al. (2003); MX3, Violi et al. (2008); CI, Wilson et al. (1992); CM, Mason et al. (1992); BR, this study.

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P.L. Leal et al. / Applied Soil Ecology 71 (2013) 7280

10000

Pasture

10000

Forest

1000

1000

100

100

10

10

Species rank
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 distribution in both systems by plotting species rank against the log of spore abundance. Species abundance distributions (SADs) summarize a

community by combining information on species richness and abundance (Dumbrell et al., 2009). In our study, both systems tended to follow a log normal distribution and SADs were not signicantly different between pasture and forest. This provides evidence that extreme differences of plant communities regarding plant species life form, plant physiology, plant diversity and aboveground productivity are not impacting the commonness and rarity of AMF species. Both systems shared few AMF species that were very abundant and the majority of AMF species that were less abundant, a universal pattern of SADs observed for plant and animals but seldom examined in microbial communities (Dumbrell et al., 2009). This pattern has been detected for AMF communities from several Brazilian ecosystems by Strmer and Siqueira (2006) based on spore abundance data and for 32 data sets from distinct habitats by Dumbrell et al. (2009) based on molecular techniques. In tropical forest of Costa Rica, Lovelock et al. (2003) found an overwhelming dominance of Acaulospora mellea and A. morrowiae that together accounted for 98% of the spores. In this study, four species accounted for 88% of the spores in pasture and three species were responsible for 57% of the sporulation in forest, demonstrating that only few species sporulate profusely within the AMF communities studied. Among the most abundant species found in both systems, sporulation of Glomus 15, A. colombiana and A. gedanensis was inuenced by soil pH while sporulation of A. mellea and A. delicate were associated with Ca and CEC. Soil pH is well known to inuence spore abundance and occurrence of AMF species (Siqueira et al., 1989), but we do not have a reasonable explanation for the role of Ca and CEC to inuence AMF sporulation, although Ca and pH

Log spore abundance

Gl15
A wal

Aml e Ael e Gcor Adel

1

Ascr

Aspi Amel

Axis 2

Ca CEC
Atub

pH
Rcla

-1

Art p Dspu

Aged Afov

Acol

-3 -3 -1 1 3

Axis 1
Fig. 4. Diagram of a PCA of arbuscular mycorrhizal fungal abundance with soil pH, Ca, and cation exchange capacity in pasture and forest. (Awal, Acaulospora walkerii; Aele, A. elegans; Acol, A. colombiana; Afov, A. foveata; Aged, A. gedanensis cf; Atub, A. tuberculata; Amel, A. mellea; Aspi, A. spinosa; Ascr, A. scrobiculata; Adel, A.delicata; Dspu, Diversispora spurca; Gcor, Glomus corymbiforme; Gl15, Glomus 15; Rcla, Rhizophagus clarus; Amle, Ambispora leptoticha; Artp, Archaeospora trappei.)

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are often found to covary. Nevertheless, these results show how limited is our knowledge about the inuence of soil factors on AMF sporulation. Differences between Amazon forest and pasture lands were found in this study regarding the mean number of AMF spores that were four-fold higher in pasture compared to forest (paired t test, P = 0.05, t = 2.07). Similar results were found by Siqueira et al. (1989) who detected low sporulation of AMF in the savanna-like Cerrado compared to agrosystems. We can attribute the high sporulation in pasture to the fact that grass species are generally good hosts to multiply AMF. Carneiro et al. (1995) observed that Brachiaria decumbens increased up to 400% sporulation of AMF. It is know that grassland species have more abundant ne-root system than a mature forest and this correlates positively with arbuscular mycorrhizal colonization and sporulation across the Pantanal, Atlantic forest and Araucaria forest ecosystems in Brazil (Zangaro et al., 2012). Although no root traits were measured in our study, differences on spore abundance between pasture and forest support these ndings. Moreover, lower sporulation levels in forest might be related to the higher P soil found in this system that was significantly higher than in pasture. Qualitative difference in the composition of AMF community was the main component to set apart forest and pasture. First, among the eight most frequent species found in both systems, only three were shared between pasture and forest. Glomus 15 was the most frequent in forest and third on pasture, A. gedanensis cf. was the second most frequent in pasture but ranked the last among the eight most frequent in forest while A. foveata ranked fourth in frequency in both systems. Second, the most abundant AMF species were also distinct between pasture and forest and only A. gedanensis was shared as one of the abundant species. Third, number of Acaulospora species was slightly higher than Glomus in pasture while the opposite occurred in forest. Picone (2000) reported Acaulospora foveata and a Glomus small brown (90130 m) as one of the most common species producing a large number of dead empty spores in forest and pasture sites. The latter is similar to Glomus 15 found herein, a species producing brown rod-shaped spores and one of the most common species in our study. Comparison of community from the same ecosystem occurring in distinct parts of the world is a rst step to establish a pattern of distribution of AMF species, genera and families. Two patterns emerged from comparisons of AMF communities in tropical forest: (a) Number of AMF species per study ranges widely, and (b) AMF communities are dominated by Acaulosporaceae and Glomeraceae in this ecosystem. Indeed, the average number of species recorded from these spore-based surveys was 21 species per study and it is within the range of the number of AMF species found per host plant in tropical forest by pik et al. (2010) based on molecular data. Considering that the sampling size was dissimilar between studies and the sampling intensity affects the outcome of the similarity index, it is clear that AMF communities from different sites of tropical forest around the world are highly dissimilar. In fact, from the 70 AMF species identied in the ten studies used to calculated similarity index, Sclerocystis clavispora, Acaulospora foveata, A. mellea, A. scrobiculata, A. spinosa, A. tuberculata, and Scutellospora pellucida were the only species found in at least six studies. In conclusion, we demonstrated that AMF community has a high resilience when experiencing a change from tropical Amazon forest to a managed pasture land. One possible mechanism for this resiliency is the shifting of the most abundant and most frequent species as forest is converted to pasture, following by large spore production of the entire fungal community. This explanation is based on the fact that most of AMF communitys descriptors were not distinct between forest and pasture, except taxonomic composition and total number of spores. Number of AMF species found in forest area in this study was similar to others found for tropical

forests elsewhere, suggesting convergence of AMF diversity in tropical forest. Acknowledgments We thank Conselho Nacional de Desenvolvimento Cientco e Tecnolgico (CNPq), Brazil, for research grants to J.O. Siqueira (Process number 304781/2006-1) and S.L. Strmer (Process number 302667/2009-1). PLL thanks CAPES for an assistantship (Program PNPD, Process number 0113085). This publication presents part of the ndings of the international project Conservation and Sustainable Management of Below-Ground Biodiversity (CSM-BGBD), implemented in seven countries Brazil, Cte dIvoire, India, Indonesia, Kenya, Mexico, and Uganda. This project is coordinated by the Tropical Soil Biology and Fertility Institute of CIAT (TSBFCIAT with co-nancing from the Global Environmental Facility GEF), and implementation support from the United Nations Environment Program (UNEP), and coordinated in Brazil by Dr. F.M.S. Moreira (UFLA, Lavras, MG). Views expressed in this publication are those of their authors and do not necessarily reect those of the authors organization, the UNEP and the GEF. Carlos R. Grippa is also acknowledged for contribution to soil sampling. We are in debt to Marta Helena Crio de Caetano and Greici Buzzi for the English review and two anonymous reviewers for their valuable contribution to this paper. References
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