2 3 Archives of Environmental Contamination and Toxicology Impacts of Manganese Mining Activity on...

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Archives of EnvironmentalContamination and Toxicology ISSN 0090-4341 Arch Environ Contam ToxicolDOI 10.1007/s00244-012-9827-7

Impacts of Manganese Mining Activity onthe Environment: Interactions Among Soil,Plants, and Arbuscular Mycorrhiza

Facundo Rivera-Becerril, LucíaV. Juárez-Vázquez, Saúl C. Hernández-Cervantes, Otilio A. Acevedo-Sandoval,Gilberto Vela-Correa, et al.

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Impacts of Manganese Mining Activity on the Environment:Interactions Among Soil, Plants, and Arbuscular Mycorrhiza

Facundo Rivera-Becerril • Lucıa V. Juarez-Vazquez • Saul C. Hernandez-Cervantes •

Otilio A. Acevedo-Sandoval • Gilberto Vela-Correa • Enrique Cruz-Chavez •

Ivan P. Moreno-Espındola • Alfonso Esquivel-Herrera • Fernando de Leon-Gonzalez

Received: 13 February 2012 / Accepted: 9 October 2012

� Springer Science+Business Media New York 2012

Abstract The mining district of Molango in the Hidalgo

State, Mexico, possesses one of the largest deposits of

manganese (Mn) ore in the world. This research assessed

the impacts of Mn mining activity on the environment,

particularly the interactions among soil, plants, and

arbuscular mycorrhiza (AM) at a location under the influ-

ence of an open Mn mine. Soils and plants from three sites

(soil under maize, soil under native vegetation, and mine

wastes with some vegetation) were analyzed. Available Mn

in both soil types and mine wastes did not reach toxic

levels. Samples of the two soil types were similar regarding

physical, chemical, and biological properties; mine wastes

were characterized by poor physical structure, nutrient

deficiencies, and a decreased number of arbuscular

mycorrhizal fungi (AMF) spores. Tissues of six plant

species accumulated Mn at normal levels. AM was absent

in the five plant species (Ambrosia psilostachya, Cheno-

podium ambrosoides, Cynodon dactylon, Polygonum

hydropiperoides, and Wigandia urens) established in mine

wastes, which was consistent with the significantly lower

number of AMF spores compared with both soil types.

A. psilostachya (native vegetation) and Zea mays showed

mycorrhizal colonization in their root systems; in the for-

mer, AM significantly decreased Mn uptake. The following

was concluded: (1) soils, mine wastes, and plant tissues did

not accumulate Mn at toxic levels; (2) despite its poor

physical structure and nutrient deficiencies, the mine waste

site was colonized by at least five plant species; (3) plants

growing in both soil types interacted with AMF; and (4)

mycorrhizal colonization of A. psilostachya influenced low

uptake of Mn by plant tissues.

Manganese (Mn) is an essential micronutrient to the plant

cell requirements. Mn plays an important role in the

reactions of enzymes (malic dehydrogenase, oxalosucci-

nate decarboxylase, superoxide dismutase); it is also nee-

ded for water-splitting in photosystem II (Nagajyoti et al.

2010). Extractable Mn concentration reported in nonpol-

luted agricultural soils worldwide can attain 30.6 (Wang

et al. 2008), 37.6 to 38.5 (Peris et al. 2007), or 58.5 mg/kg

(Carrillo Gonzalez and Gonzalez-Chavez 2006); all of

these are considered to fall within the normal range

(\100 mg/kg [Alloway 1995]). In contrast, studies on

contaminated sites reported that available concentrations of

Mn reached 226 mg/kg in a soil-ore crushing area, 550 mg/

kg in soil-tailings in an abandoned mine site (Archer and

Caldwell 2004), and 289 to 1356 mg/kg in heavily con-

taminated tailings (Franco-Hernandez et al. 2010).

The mining district of Molango (with an area of

180 km2 in Hidalgo State, Mexico) has one of the largest

F. Rivera-Becerril (&) � S. C. Hernandez-Cervantes �G. Vela-Correa � A. Esquivel-Herrera

Departamento El Hombre y su Ambiente, Universidad

Autonoma Metropolitana-Xochimilco, Mexico, DF, Mexico

e-mail: [email protected]

L. V. Juarez-Vazquez

Maestrıa en Ciencias Agropecuarias, Universidad Autonoma

Metropolitana-Xochimilco, Mexico, DF, Mexico

O. A. Acevedo-Sandoval � E. Cruz-Chavez

Centro de Investigaciones en Ciencias de la Tierra y Materiales,

Universidad Autonoma del Estado de Hidalgo,

Ciudad Universitaria, Pachuca, Hidalgo, Mexico

I. P. Moreno-Espındola � F. de Leon-Gonzalez

Departamento Produccion Agrıcola y Animal, Universidad

Autonoma Metropolitana-Xochimilco,

Mexico, DF, Mexico

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Arch Environ Contam Toxicol

DOI 10.1007/s00244-012-9827-7

Author's personal copy

deposits of Mn ore in the world: C30 million tons of

proven reserves (Rodrıguez-Agudelo et al. 2006; Catalan-

Vazquez et al. 2010). Since 1960, exploitation, extraction,

and transformation of Mn have occurred, leading to a

massive amount of Mn particle waste released into the

surrounding environment. The levels of Mn in the air reach

B5.86 lg/m3 (Rodrıguez-Agudelo et al. 2006).

The human population, the surrounding environment

(soil, air, water), and many organisms are exposed to these

Mn mining wastes. It has been reported that persons living

near Mn mines and processing plants in the mining district

of Molango tend to exhibit an incipient motor deficit as a

result of inhalation of Mn-rich dust (Rodrıguez-Agudelo

et al. 2006). In addition, drinking water contaminated with

Mn is associated with intellectual disabilities in children

(Bouchard et al. 2011).

Normal concentrations of Mn in plant tissues range from

15 to 150 mg/kg (Reimann and de Caritat 1998; Nagajyoti

et al. 2010). Accumulation of high concentrations of Mn in

leaves causes a decrease of the photosynthetic rate;

necrotic brown spotting on leaves, petioles, and stems is a

common symptom of Mn toxicity; over time the speckles

can increase in both number and size resulting in necrotic

lesions, leaf browning, and death of the plant; and roots are

commonly brown in color (Nagajyoti et al. 2010). In

Nonoalco, where the current study was conducted, leaves

of maize and of a nonidentified species of grass accumu-

lated 304 and 135 mg/kg dry weight Mn, respectively

(Rodrıguez-Agudelo et al. 2006). In addition, stems and/or

leaves of Prunus persica, Citrus limon, and Cynodon ple-

ystostachyus sampled in home gardens accumulated Mn at

levels ranging from 152.7 to 440.7 mg/kg (Ortega 2005).

To our knowledge, no information exists on Mn accumu-

lation in mining waste areas.

Arbuscular mycorrhizal fungi (AMF), a group of bene-

ficial microorganisms that interact with plant roots by

establishing arbuscular mycorrhiza (AM) symbiosis, are

also susceptible to contamination by toxic elements in

soils. Malcova et al. (2003) reported that Glomus intrara-

dices, an AMF, exhibited low tolerance against Mn pol-

lution in soil. It has also been reported that AM contributes

to the decrease of Mn uptake by plants. In this regard,

soybeans (Glycine max) inoculated with two species of

AMF (G. etunicatum and G. macrocarpum) took up sig-

nificantly less Mn than uninoculated plants (Nogueira et al.

2007).

The current study was performed to assess the impacts

of Mn mining on the following: (1) Mn content in two soils

(under cultivated maize and native vegetation) and mine

waste substrate; (2) accumulation of Mn in the plant tissues

of several plant species, and (3) the presence of AM in

plant species growing in the vicinity of the mine.

Materials and Methods

Description of the Study Area

Nonoalco, with a total population of 831 persons (Instituto

Nacional de Estadıstica y Geografıa 2011), is located in the

mining district of Molango (20�580000N, 98�450000W;

1680 m altitude) in the northern region of Hidalgo State

(Fig. 1). Nonoalco’s climate is temperate and humid during

summer rains (Rodrıguez-Agudelo et al. 2006). The Mn

mine is located at the bottom of a watershed and has been in

operation since 1964; rural homesteads are located around

this Mn mine at a distance of\1 km. Soil uses include maize

and common bean crops, pasture for cattle and sheep, forests

of Pinus spp., and deposits of mine wastes.

Field Work

This study included three sites near the mine and dominated

by different plant species that were selected for their high

biomass production: (1) soil under maize (Z. mays L.,

Gramineae); (2) soil under native vegetation (primarily

Ambrosia psilostachya DC., Asteraceae), and (3) mine

wastes dumped in tailing dams (A. psilostachya; Chenopo-

dium ambrosoides L., Chenopodiaceae; Cynodon dactylon

L., Gramineae; Polygonum hydropiperoides Michx., Po-

lygonaceae; Wigandia urens [Ruiz & Pavon], Hydrophyll-

aceae). In July 2007, three plots were selected at each site. In

each plot, three plants were randomly selected and collected

(roots and shoots), and three soil samples were taken from

the top 20 cm of soil adjacent to the plants (substrates

adjacent to P. hydropiperoides roots were sampled in the

mine waste plots). To assess Mn accumulation in plant tis-

sues, shoots and roots were analyzed separately. All samples

were placed in plastic bags, and a portion of each root sys-

tem was stored at 4 �C to quantify mycorrhizal colonization.

Mexico

Hidalgo State

Nonoalco

Fig. 1 Location of Nonoalco in Hidalgo State, Mexico


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Laboratory Analyses

Soil samples and mine wastes (1.5 kg) were dried at room

temperature and sieved through a 2.0 mm–diameter sieve.

Soil particle and bulk densities were measured using a

pycnometer and undisturbed soil core methods, respec-

tively (United States Department of Agriculture 2004).

Soil porosity was calculated according to Soil Survey

Staff (2011). Soil texture was determined according to

Gee and Bauder (1982). Soil pH was measured in water

with a glass electrode potentiometer (Orion STR 3) at a

ratio of 1:2.5. Soil organic matter content was determined

employing the wet combustion method (United States

Department of Agriculture 2004); organic carbon and total

nitrogen were calculated from these results. The concen-

tration of available phosphorus (P) was determined using

the United States Department of Agriculture method

(2004), the content of exchangeable cations Ca2? and

Mg2? by the Versenate method (United States Department

of Agriculture 2004), and Na? and K? by flamometry

(Corning 400). The cation-exchange capacity (CEC) was

calculated by saturation with ammonium acetate and

analysis with ethylene diamine tetraacetic acid (Jackson

1982). Total oxides (SiO2, TiO2, Fe2O3, Al2O3, MnO,

MgO, and P2O5) were measured using an X-ray fluores-

cence analyzer (Siemens SRS 3000, Karlsruhe, Germany).

The concentration of assimilable nutrients (aluminum

[Al], manganese [Mn], iron [Fe], silicon [Si], and zinc

[Zn]) was estimated using DTPA (United States Depart-

ment of Agriculture 2004). Finally, the concentrations of

several nutrients (Mn, Al, Fe, Zn, Na?, K?, Ca2?, Mg2?,

and P) in plant tissues was performed using inductively

coupled plasma–atomic emission spectroscopy (Piper

1947; Plank 1992).

Identification of plant species was conducted accord-

ing to Lopez (1988) and de Rzedowski and Rzedowski

(2001). To estimate the level of colonization of plant

roots by AMF, roots from 9 plants of each plant species

were digested with 10 % KOH and stained with trypan

blue (Phillips and Hayman 1970) in lactoglycerol. From

each root system, 30 1-cm root segments were placed on

a slide with glycerol and observed under a microscope.

Levels of mycorrization were calculated according to the

intensity of mycorrhizal colonization (M%: hyphae,

vesicles, and arbuscules) and the abundance of arbus-

cules (A%) in the root system (Trouvelot et al. 1986).

The presence of Paris and Arum morphotypes of AM in

roots was recorded (Dickson et al. 2007). Extraction of

spores from soil and substrates (three samples from each

site) was performed according to the wet sieving–and–

decanting method (Gerdemann and Nicolson 1963), and

centrifugation was performed along a 60 % sucrose

gradient.

Processing and Analysis of Results

The data were checked for normal distribution using SPSS 17

(SPSS Inc., Chicago, IL, USA) software; when normal dis-

tribution was not observed, data were normalized with

z-score. One-way analysis of variance (ANOVA) was per-

formed on each variable. Whenever ANOVA resulted in

significant differences, Tukey tests were conducted to

determine differences among homogeneous groups of means

(p\0.05). For data ordination, principal component analysis

(PCA) was conducted to examine aggregation by site and by

variable (Pielou 1984). Canonical correspondence analysis

(CCA) was employed for ordination of biological data

according to the physical and chemical properties of the soils

and substrates (ter Braak 1986). This resulted in a triple

classification: by sample, by physical and chemical vari-

ables, and by biological variables. These analyses were

computed using STATISTICA 8.0 (StatSoft, Tulsa, OK,

USA) software.

Results

Physical and Chemical Soil and Substrate Properties

Soil and substrate properties are listed in Table 1. The

levels of available Mn at the three studied sites (42.6 to

58.0 mg/kg) exhibited no significant differences among

these and did not attain critical limits in soils. Organic

matter, organic carbon, and total nitrogen were highest in

soils under native vegetation, intermediate in agricultural

soils, and lowest in mine wastes (p \ 0.05). The available

P was highest in the soil under maize (2.4 mg/kg) and

intermediate in the soil under native vegetation (0.9 mg/

kg), whereas only traces were found in the mine wastes.

Ca2? and Mg2? concentrations were high at all three sites.

Na? and K? levels were low in mine wastes and inter-

mediate in soils under native vegetation and maize. Al, Fe,

and Zn values were highest in soil under maize. The pre-

vailing oxide at all three sites was SiO2 (range 28.8 to 60.3

%). MnO, a nonavailable form of Mn, was the second most

abundant compound. MnO reached highest concentrations

in mine wastes (28 %), which was[2 times higher than in

soil under native vegetation and nearly 20 times greater

than in soil under maize.

Accumulation of Mn in Plant Tissues

Considering the normal concentrations (40 to 150 mg/kg)

reported by Reimann and de Caritat (1998), none of the six

plant species accumulated Mn at toxic levels. Mn accu-

mulation was lowest in Z. mays (\2 mg/kg) and in

A. psilostachya (6.2 mg/kg) from the native vegetation site

and highest in the five plant species growing in the mining


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wastes. A. psilostachya and C. dactylon had the highest

Mn concentrations (89.8 and 45.5 mg/kg, respectively)

(Tables 2, 3). There was a greater proportion of Mn in

roots (range 52.8 to 95.3 %) than in shoots (range 4.7 to

47.2 %) in all species except for W. urens (Table 3).

AM Colonization

In plants growing in mine wastes (A. psilostachya, C. ambro-

soides, C. dactylon, P. hydropiperoides, and W. urens),

mycorrhization was absent (Table 4). Z. mays exhibited pri-

marily Arum-type mycorrhiza, whereas Paris-type was most

frequent in A. psilostachya. A. psilostachya established in soil

under native vegetation showed highest levels of mycorrhizal

intensity (M% = 30.4 %) and abundance of arbuscules (A% =

3 %) in the root system, followed by Z. mays (M% = 9.8 %,

A% = 1.2 %). These two mycorrhizal plant species accumu-

lated the lowest Mn contents in their tissues; in contrast,

nonmycorrhizal plant species established in mine wastes

accumulated the highest Mn levels. This behavior is clearly

appreciated when comparing mycorrhizal and nonmycorrhi-

zal A. psilostachya plants growing in soil under native vege-

tation and mine wastes, respectively. This suggests an

important role of AM in decreasing Mn uptake by plants

Table 1 Physical and chemical

variables (mean ± SD) in soils

and mine wastes from three sites

under the influence of Mn

mining activities

For each variable, different

letters indicate significant

differences (p \ 0.05) among

sites (n = 9 for all variables

except total oxides where

n = 3)

Soil under maize Soil under native

vegetation

Mine wastes

Physical properties

Soil water content (%) 28.8 ± 4.32a 27.6 ± 6.14a 20 ± 2.64b

Bulk density (g/cm) 0.9 ± 0.04b 0.9 ± 0.15b 1.2 ± 0.04a

Real density (g/cm) 2.2 ± 0.22a 3.2 ± 1.28a 3.1 ± 0.65a

Porosity (%) 59.5 ± 3.22a 66.5 ± 10.22a 61.5 ± 6.12a

Sand (%) 29 ± 5.76b 34.1 ± 22.63b 86.9 ± 5.16a

Silt (%) 35.7 ± 6.81a 45.8 ± 21.03a 11.9 ± 4.60b

Clay (%) 35.4 ± 10.89a 20.2 ± 12.09b 1.2 ± 1c

Texture Silty Silty Sandy

Chemical properties

pH 5.7 ± 0.16c 6.5 ± 0.31b 6.9 ± 0.13a

Organic matter (%) 3.1 ± 1.88b 6.1 ± 2.67a 0.4 ± 0.41c

Organic carbon (%) 1.8 ± 1.09b 3.5 ± 1.53a 0.2 ± 0.23c

Total nitrogen (%) 0.1 ± 0.09b 0.3 ± 0.13a 0.02 ± 0.02c

Available P (mg/kg) 2.4 ± 2.81a 0.9 ± 1.53ab 0 ± 0b

Cation-exchange capacity (meq/100 g) 12.1 ± 1.31b 16.2 ± 3.33a 16.3 ± 1.22a

Exchangeable cations (meq/100 g)

Ca2? 14.3 ± 4.52c 26.7 ± 5.17a 21.2 ± 3.45b

Mg2? 8.8 ± 4.24b 17.6 ± 6.52a 17.5 ± 2.57a

Na? 7.9 ± 1.43a 8.3 ± 1.15a 2.9 ± 0.46b

K? 4.3 ± 1.06a 4.6 ± 0.90a 1.6 ± 0.16b

Micronutrients (mg/kg)

Al 4.4 ± 3.52a 2.5 ± 1.35ab 0.3 ± 0.07b

Mn 42.6 ± 15.65a 56.1 ± 26.00a 58 ± 7.82a

Fe 13 ± 5.26a 8.9 ± 5.54ab 5.8 ± 1.24b

Si 0 ± 0a 0.14 ± 0.37a 0 ± 0a

Zn 3.1 ± 2.43a 2 ± 2.13ab 0.01 ± 0.02b

Total oxides (%)

SiO2 60.3 ± 9.89a 45.6 ± 13.99ab 28.8 ± 5.40b

TiO2 0.7 ± 0.14a 0.5 ± 0.10ab 0.3 ± 0.07b

Al2O3 15.6 ± 4.52a 11.1 ± 2.31ab 8 ± 0.79b

Fe2O3 7.7 ± 2.96a 12.1 ± 4.39a 14.5 ± 1.41a

MnO 1.5 ± 1.62b 13.1 ± 10.54ab 28.1 ± 5.34a

MgO 0.9 ± 0.10a 0.6 ± 0.18ab 0.5 ± 0.03b

P2O5 0.3 ± 0.05a 0.3 ± 0.07a 0.2 ± 0.02a


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Table 2 Uptake of elements (mg/kg ± SD) in plants established in three sites under the influence of Mn mining activities (n = 9)

Element Soil under maize Soil under native vegetation Mine wastes

Z. m. A. p. A. p. C. a. C. d. P. h. W. u.

Shoots

Mn 0.8 ± 0.58 3.7 ± 1.26 4.4 ± 1.54 8.1 ± 1.67 6 ± 1.75 9.4 ± 4.77 17 ± 6.78

Al 1 ± 0.52 0.6 ± 0.24 0.7 ± 0.16 2.5 ± 1.93 1.6 ± 2.36 0.7 ± 0.25 1.7 ± 0.67

Fe 1.1 ± 0.48 1.5 ± 0.71 1.2 ± 0.36 3 ± 0.94 2 ± 0.46 2.7 ± 2.06 7.5 ± 2.85

Zn 0.03 ± 0.04 0.01 ± 0.01 0 ± 0 1.1 ± 1.81 0 ± 0 0 ± 0 0 ± 0

Na? 7.1 ± 0.89 4.2 ± 0.35 4.7 ± 0.97 5.6 ± 0.88 6.6 ± 1.21 2.9 ± 0.22 6.4 ± 1.86

K? 4.2 ± 2.29 2.8 ± 2.29 37.3 ± 18.64 188.4 ± 38.92 58.6 ± 13.62 6.5 ± 1.06 196 ± 134.38

Ca2? 9 ± 4.77 1.7 ± 1.32 128.4 ± 47.80 252.3 ± 29.45 42 ± 7.60 8.4 ± 1.17 214.8 ± 103.97

Mg2? 7.5 ± 4.84 7 ± 6.85 40.6 ± 15.10 95.8 ± 23.94 17.9 ± 2.60 5.3 ± 6.83 54.6 ± 27.22

P 2.1 ± 1.45 0.2 ± 0.30 18.2 ± 5.39 20.7 ± 1.60 21.1 ± 1.35 1.4 ± 0.23 19.3 ± 6.23

Roots

Mn 1.8 ± 1.59 6.2 ± 3.03 89.8 ± 27.07 12.7 ± 0.95 45.5 ± 11.56 10.5 ± 6.36 14.5 ± 8.80

Al 7.4 ± 1.94 2.5 ± 1.12 3 ± 0.63 1.2 ± 0.05 2.2 ± 0.54 7.9 ± 18.47 7.7 ± 9.77

Fe 10.2 ± 4.37 6.1 ± 1.39 20.9 ± 4.72 4.3 ± 0.53 11.1 ± 2.64 6.4 ± 3.47 5.7 ± 3.35

Zn 0 ± 0 0 ± 0 0.04 ± 0.08 0.01 ± 0.01 0 ± 0 0 ± 0 0 ± 0

Na? 5.7 ± 1.77 4.6 ± 0.70 25.7 ± 46.64 6.9 ± 0.73 6.7 ± 0.28 3.7 ± 0.37 8.2 ± 0.96

K? 7.2 ± 1.48 7.6 ± 1.51 58.6 ± 24.46 166.3 ± 67.10 22.2 ± 0.78 5.9 ± 0.67 191.7 ± 77.77

Ca2? 7.7 ± 2.60 7.5 ± 7.00 54.2 ± 7.22 105.6 ± 31.65 19.4 ± 1.95 4.6 ± 0.72 96.8 ± 27.28

Mg2? 4 ± 2.15 12.8 ± 1.85 40.1 ± 7.12 73.4 ± 3.77 7.6 ± 0.40 12.2 ± 4.27 21.2 ± 0.93

P 1.5 ± 0.17 1.8 ± 0.21 22.7 ± 0.26 24.5 ± 0.43 21.5 ± 0.60 1.2 ± 0.39 23.2 ± 0.10

Z. m., Z. mays; A. p., A. psilostachya; C. a., C. ambrosoides; C. d., C. dactylon; P. h., P. hydropiperoides; W. u., W. urens

Table 3 Mn accumulated in the tissues of different plant species established in Nonoalco

Plant species Substrate, mg/kg Shoots, mg/kg (%)a Roots, mg/kg (%)a References

A. psilostachya 56.1 3.7 (37.4) 6.2 (62.6) This work

A. psilostachya 58 4.4 (4.7) 89.8 (95.3) This work

C. ambrosoides 58 8.1 (38.8) 12.7 (61.2) This work

C. limon 11.6 152.7 – Ortega (2005)

Citrus sinensis 11.6 48.2 – Ortega (2005)

C. dactylon 58 6 (11.6) 45.5 (88.4) This work

C. pleystostachyus 11.6 440.7 – Ortega (2005)

Eriobotrya japonica 11.6 133.2 – Ortega (2005)

Ficus carica 11.6 76.2 – Ortega (2005)

Grass 67 135 – Rodrıguez-Agudelo et al. (2006)

Malus pumila 11.6 33.6 – Ortega (2005)

Persea americana 11.6 129.8 – Ortega (2005)

P. hydropiperoides 58 9.4 (47.2) 10.5 (52.8) This work

P. persica 11.6 431.2 – Ortega (2005)

Psidium guajava 11.6 119.7 – Ortega (2005)

W. urens 58 17 (53.9) 14.5 (46.1) This work

Z. mays 42.6 0.8 (30.6) 1.8 (69.4) This work

Z. mays 67 304 – Rodrıguez-Agudelo et al. (2006)

a Numbers in parentheses indicate percentage of Mn accumulated in shoots and roots


123


(Fig. 2). The number of AMF spores in soils under native

vegetation and maize was similar (Table 4) but significantly

greater than in mine wastes (p \ 0.05).

Multivariate Analyses

PCA of the physical, chemical, and biological properties of

each sample of soils, mine wastes, and plants from all 3

sites illustrates that soils under maize and native vegetation

were closely grouped (Fig. 3). The primary variables that

influenced this group included greater clay and silt in

substrates, mycorrhizal colonization (M%), and lower

Ca2? content in shoots. Samples from mine wastes were

clearly separated from those of the 2 soil types and were

grouped according to plant species. A. psilostachya was

positively correlated with Mn concentrations in roots as

well as the level of sand particles. Samples of W. urens and

C. ambrosoides showed larger dispersion (Fig. 3). It should

be noted that samples of A. psilostachya and soils from the

site under native vegetation were completely separated

from those belonging to mine wastes; mycorrhization, soil

texture, and Mn uptake by roots influenced this separation.

The CCA allowed for triple by-case ordination. The 18

samples from the 2 soil types were closely grouped and

were primarily influenced by mycorrhizal colonization,

content of silt, clay, organic matter, organic carbon, total

nitrogen, and available P in substrates (Fig. 4). The

majority of the samples from mine wastes were grouped

together and correlated with the content of sand, Mn, bulk

density, and pH in substrates as well as Mn content in roots

(Fig. 4).

Discussion

Physical and Chemical Soil and Substrate Properties

In this work, concentrations of available Mn in the studied

soils and mine wastes are considered to fall within reported

normal levels (Alloway 1995) in the range of nonpolluted

agricultural soils. These results are close to those previously

observed (67 mg/kg) in plots under maize and a grass spe-

cies near the mining area of Nonoalco (Rodrıguez-Agudelo

et al. 2006). Ortega (2005) reported Mn concentrations of

11.6 mg/kg in soils from orchards in Molango, which is near

Nonoalco. In the mining areas of Zacatecas State (northern

Mexico), available Mn ranged from 0.2 to 68.4 mg/kg

(Carrillo Gonzalez and Gonzalez-Chavez 2006).

The greater water content in both soil types (maize and

native vegetation) is most likely explained by the greater

water-retention capacity of clay and silt particles (Porta

et al. 1999). Several factors affect the availability of Mn in

soils. Fine clay particles absorb Mn on their surfaces

(Navarro 2003). Mn solubility is higher in acidic pH

Fig. 2 Accumulation of elements in tissues of A. psilostachyagrowing in soil under native vegetation (mycorrhizal plant) and mine

wastes (nonmycorrhizal plant). Bars indicate SE (n = 9), and

asterisks indicate significant differences (p \ 0.05) between sites

Table 4 Arbuscular mycorrhizal colonization of plant roots and

numbers of spores (mean ± SD) in substrates from three sites under

the influence of Mn mining activities

Plant species M (%) A (%) Spores/250 g

substrate

Soil under maize

Z. mays 9.8 ± 6.68 1.2 ± 1.18 668.7 ± 274.4a

Soil under native vegetation

A. psilostachya 30.4 ± 19.65 3.0 ± 2.62 1016 ± 323.8a

Mine wastes

A. psilostachya 0 0 44.7 ± 5.03b

C. ambrosoides 0 0

C. dactylon 0 0

P. hydropiperoides 0 0

W. urens 0 0

Different letters indicate significant differences (p \ 0.05) among

sites (n = 9 for M% and A%; n = 3 for spores)

M intensity of mycorrhizal colonization in the root system; A abun-

dance of arbuscules in the root system


123


environments (Arines et al. 1989). Soils under maize and

native vegetation had moderately acidic pH, which may

have resulted from the presence of some organic com-

pounds, microbial activity, and soil moisture (Ramos-

Arroyo and Siebe-Grabach 2006). The neutral pH of min-

ing wastes can most likely be attributed to the weak

capacity of the coarsely textured waste materials to retain

particulate organic matter concentrations (\0.5 g/100 g),

which generate acidic environments. The high concentra-

tions of Ca2?, as observed in this research, tend to pre-

cipitate elements such as Mn (Navarro 2003).

The results obtained from PCA and CCA (Figs. 3, 4),

in which the samples of both soil types were grouped

together, confirm their closer physical, chemical, and

biological properties. The separation of samples from

mine wastes compared with those of the two soil types is

attributed to poor physical structure (low clay and silt

content), nutrient deficiency (low organic carbon, organic

matter, total nitrogen, and available P), incipient weath-

ering of mineral material, and the absence of processes

that contribute to the accumulation of organic substances,

which is typical in tailings (Mendez and Maier 2008).

These unstable physical and poor chemical properties are

similar to those reported for other tailings (Ramos-Arroyo

and Siebe-Grabach 2006; Mendez and Maier 2008;

Juarez-Vazquez et al. 2011).

Clay

Sand

Silt

SWC

DaDrEPpH

MOCONCaMg

NaK

CIC

Al

Mn

Fe

SiZnPTAAlTAMnTAFeTANa

sK+

sCa2+

sMg2+

TAZn

sP

RAl

rMn

rFerNa+

rK+

rCa2+

rMg2+

RZn

rP

M%

A

12

34

5

6

7

8

910

11

12

1314 15

16

17

18

19 20

212223

2425

26

27

28

29

3031

32

33

3435

36

37

38

39

40

41

42

43

44

45

46

47

48

4950

51

5253

54

55

5657

58

5960

61 6263

-180 -120 -60 60 120 180 240 300 360

Component 1

-80

-60

-40

-20

20

40

60

80

Com

pone

nt2

Fig. 3 PCA. Numbers indicate

the origin of the samples

according to the following

scheme: 1 to 9 (soil cultivated

with maize and Z. mays); 10 to

18 (soil under native vegetation

and A. psilostachya); 19 to 27

(mine wastes and P.hydropiperoides); 28 to 36

(mine wastes and A.psilostachya); 37 to 45 (mine

wastes and W. urens); 46 to 54

(mine wastes and C.ambrosoides); and 55 to 63

(mine wastes and C. dactylon)

sAl

sMn

sFe

sNa+

sK+

sCa2+

TAMg

sZn

sP

rAl

rMn

rFe

rNa+RKrCa2+

rMg2+

rZn

RP

M%

A%

1 23

4

56

78

9

10

1112

131415

1617

18

19

202122232425

2627282930313233 343536373839404142434445464748495051525354 555657585960616263

Clay

Sand

Silt

SWC

BDDr

Po

pH

OMOC

N

Ca2+Mg2+

Na+K+

CEC

Al

Mn

Fe

Si

ZnP

-1.8 -1.2 -0.6 0.6 1.2 1.8 2.4 3 3.6

Axis 1

-4.8

-3.6

-2.4

-1.2

1.2

2.4

3.6

4.8

Axi

s 2

Fig. 4 CCA. Numbers indicate

the origin of the samples as in

Fig. 3. The ellipse on the right

encompasses soil cultivated

with maize, Z. mays, and soil

under native vegetation and

A. psilostachya. The ellipse on

the left groups plant samples

(A. psilostachya, C. ambro-soides, C. dactylon,

P. hydropiperoides, and

W. urens) and all of the

substrates from mine wastes


123


Accumulation of Mn in Plant Tissues and AM

All of the six studied plant species accumulated Mn at

normal concentrations (Reimann and de Caritat 1998), thus

indicating that maize and the grass C. dactylon do not

represent a risk for grazers as a source of Mn. In a previous

study also performed at Nonoalco (Ortega 2005), Mn was

measured in plants growing in a soil substrate with

11.6 mg/kg. Mn concentrations were high in two fruit

trees, P. persica and C. limon (431.2 and 152.7 mg/kg,

respectively), and at greater-than-normal levels (440.7 mg/

kg) in the grass C. pleystostachyus, according to Reimann

and de Caritat (1998) and Nagajyoti et al. (2010).

The five plant species established in Mn mine wastes

(A. psilostachya, P. hydropiperoides, W. urens, C. ambrosoides,

and C. dactylon) can be considered pioneer plants; none of

these showed mycorrhizal colonization in their roots despite the

fact that the grass C. dactylon (Wu et al. 2010) and A. psilo-

stachya are able to establish AM symbiosis. The number of

AMF spores in mine wastes was significantly lower than in the

two soil types, which was due to a lack of plant cover as a

result of the substrate’s stressful physical and chemical condi-

tions. There is the possibility that some toxic Mn ions could be

delivered in the mine wastes, which by leaching processes

could arrive in aquifers, below the first top 20 cm of the surface

layer where plant roots and AMF spores were sampled. This

indicates that absence of vegetation is the main reason for the

decreased number of AM propagules, which limit AM colo-

nization. The higher presence of AMF spores in the two soil

types is favored by plant cover, organic matter, and nutrients,

which contribute to germination, intraradical growth, extra-

radical mycelium development, and fungal sporulation (Paw-

lowska and Charvat 2004).

Previous reports do not analyze the mycorrhizal status of

Mn-accumulating plants growing in mining zones (Wang

et al. 2008; Franco-Hernandez et al. 2010; Juarez-Santillan

et al. 2010). In the present study, AM appears to be par-

ticularly important in significantly decreasing Mn uptake in

the roots and shoots?roots of A. psilostachya from soil

under native vegetation; nonmycorrhizal A. psilostachya

growing in mine wastes exhibited considerably greater Mn

uptake (approximately 15-fold more) in roots. Nogueira

et al. (2007) reported that two Glomus species influenced

lower Mn uptake by soybean plants relative to nonmy-

corrhizal ones because the metal was retained by the

extraradical mycelium. In this regard, it has been reported

that extraradical mycelium (Joner et al. 2000) and spores

(Pagano et al. 2010) of AMF accumulate elements, such as

cadmium, Si, Al, copper, and/or Fe. The significantly

greater accumulation of Mn in the tissues of nonmycor-

rhizal A. psilostachya could also be explained by the lower

clay content in mine wastes, which favors greater avail-

ability of Mn. Multivariate analyses (Figs. 3, 4) confirmed

that plant species distribution was directly influenced by

substrate factors and interaction with AMF; mycorrhizal

A. psilostachya and maize, growing in the two studied soil

types, were always grouped together and were separated

from plants established in the mine wastes.

Pioneer plants growing in the mine wastes of Nonoalco

are candidates for programs of vegetation of tailings, par-

ticularly C. dactylon, which has previously been reported

as the predominant plant species in abandoned mines and

smelting sites (Wu et al. 2010). The extensive root-hair

system of C. dactylon shows high efficiency in adhering

soil particles and forming rhizosheaths (Moreno-Espındola

et al. 2007), a microecosystem that stimulates microbial

activity. Soil formation increases when a permanent plant

cover is established; in this way, programs of vegetation of

tailings will transform these stressful environments (Lei

and Duan 2008). Plant cover buffers wind and water ero-

sion of mine wastes and also contributes to decreasing the

inhalation of Mn-rich dust dispersed by the air, which

appears to be a risk for human population living in the

vicinity of Mn-mining activities (Rodrıguez-Agudelo et al.

2006).

Conclusion

Available Mn did not reach toxic concentrations in two soils

(under maize and under native vegetation) subjected to Mn-

rich dust derived from mining activities. Low levels of par-

ticles having clay sizes\2 lm, available Mn, water content,

organic matter, organic carbon, total nitrogen, available P,

and a very poor number of AMF spores characterized the Mn

mine wastes. At least five plant species (A. psilostachya,

C. ambrosoides, C. dactylon, P. hydropiperoides, and

W. urens) tolerate the unstable physical and poor chemical

conditions prevailing in the mine wastes; C. dactylon could

be considered in vegetation programs in these tailings. All of

the six plant species accumulated Mn at normal levels.

Contrary to plants from mine wastes, plant species estab-

lished in both soil types (Z. mays and A. psilostachya) inter-

acted with AMF. Mycorrhizal colonization of A. psilostachya

influenced low uptake of Mn by plant tissues.

Acknowledgments L.V. Juarez-Vazquez received a scholarship

from CONACyT-Mexico while studying for a master’s degree in

science. The authors acknowledge Aurora Chimal-Hernandez (UAM-

X) for identification of the plant species, David Lopez-Hernandez for

help during field sampling, as well as two anonymous reviewers for

improving the manuscript.

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