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Process Safety and Environmental Protection x x x ( 2 0 1 6 ) xxx–xxx

Contents lists available at ScienceDirect

Process Safety and Environmental Protection

journal homepage: www.elsevier.com/locate/psep

Impact assessment of heavy metal pollution on

soil mite communities (Acari: Mesostigmata) from
Zlatna Depression – Transylvania

Minodora Manu a,∗ , Raluca Ioana Băncilă b,c , Virgil Iordache d ,

Florian Bodescu d , Marilena Onete a
a Romanian Academy, Institute of Biology Bucharest, Department of Ecology, Taxonomy and Nature Conservation,
Street Splaiul Independenţei, No. 296, Zip Code 0603100, PO-BOX 56-53, Bucharest, Romania
b University Ovidius Constanţa, Faculty of Natural Sciences, Al. Universităţii, Corp B, Constanţa, Romania
c Romanian Academy, “Emil Racoviţă” Institute of Speleology, Department of Biospeleology and Soil Edaphobiology,

13 Septembrie Road, No. 13, 050711 Bucharest, Romania

d Research Centre for Ecological Services (CESEC), Faculty of Biology, University of Bucharest, Romania

a r t i c l e i n f o a b s t r a c t

Article history: The heavy metal pollution level of soil from twelve grasslands and its impact on soil mite
Received 29 December 2015 communities was assessed. The impact assessment was investigated, taking into account
Received in revised form 15 May the distance from pollution source, the degree of pollution and the cumulative influence
2016 of heavy metals and other environmental variables. These variables were: temperature,
Accepted 7 June 2016 humidity, acidity, carbon content, nitrogen total, C/Nt ratio, slope, altitude, vegetation cover,
Available online xxx exposition and soil type.
The measured concentrations of all heavy metals for the investigated grasslands exceeded
Keywords: the reference values according to the national legislation. In order to make a comparison
Soil mite communities between investigated grasslands and in order to classify the ecosystems, total metal load
Heavy metal pollution was calculated. Three groups of grasslands were established based on different degrees of
Grassland soil pollution and taking into account the total metal load.
Environmental variables In total, 66 Mesostigmata species were identified, with 961 individuals. Mite communities
Distance from the most polluted areas were distinguishable from those from less polluted grasslands.
Metal load Some heavy metals (e.g. As, Cu, Pb and Zn) influenced the soil mites from highly polluted
ecosystems, while Mn and other environmental variables (altitude and soil humidity) were
strongly correlated with invertebrate communities from the medium polluted areas. Soil
temperature was the main factor influencing mites from the less polluted ecosystems.
© 2016 Institution of Chemical Engineers. Published by Elsevier B.V. All rights reserved.

1. Introduction
Soil pollution with heavy metals is a significant environmental
problem in Europe as well as in the entire world (Hernandez
et al., 2003; Mico et al., 2006; Dragovic et al., 2008; Wei and
Yang, 2010; Hu et al., 2013). Due to the intense industrialisation
from the 18th century and due to the mining on small or
large scale, this phenomenon has occurred in many countries,
including Romania. During the communist period, from 1945
to 1990, the Transylvanian region was famous for its min-
ing activities. Zlatna, Brad, Caraciu and Deva localities were
known as important source of nonferrous minerals, as: Cu, Zn,

∗
Corresponding author. Tel.: +40 212219202; fax: +40 212219071.
E-mail addresses: minodoramanu@gmail.com (M. Manu), bancila ralucaioana@yahoo.com (R.I. Băncilă), virgil.iordache@g.unibuc.ro
(V. Iordache), florianbodescu@gmail.com (F. Bodescu), marilena.onete@gmail.com (M. Onete).
http://dx.doi.org/10.1016/j.psep.2016.06.011
0957-5820/© 2016 Institution of Chemical Engineers. Published by Elsevier B.V. All rights reserved.

Please cite this article in press as: Manu, M., et al., Impact assessment of heavy metal pollution on soil mite communities (Acari: Mesostigmata)
from Zlatna Depression – Transylvania. Process Safety and Environmental Protection (2016), http://dx.doi.org/10.1016/j.psep.2016.06.011
PSEP-799; No. of Pages 14
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Pb, Au, Ag. In 1746, the first factory for metallurgical processing
of these minerals was built in Zlatna city. In 1970, a new fac-
tory appeared, named S.C. Ampellum S.S., which functioned
until 2003 (Keri et al., 2010). During all this long period of time
(more than 224 years), the atmospheric pollution was spread
not only in close proximity to the factory, but at big distances
as well, due to the plant having a dispersion chimney tower, of
220 m height (the prime pollution source). The long time pol-
lution affected the biodiversity of the area, as well as soil and
water (Lăcătuşu et al., 2001; Damian et al., 2008; Weindorf et al.,
2013). Soil is the favoured habitat for various invertebrates,
including mites.
Mites are cosmopolite invertebrates, which can be found
in all types of ecosystems (from aquatic ecosystems to terres-
trial ones), and habitats (on plant, soil, moss, decaying matter,
in nest, on mammals), due to their morphological and biolog-
ical specializations (Koehler, 1999; Walter and Proctor, 2013).
Through their high diversity and abundance, they are inte-
grally involved in many ecological interactions. From 1980,
they have gained an increasing interest as bioindicators, being
able to provide qualitative and quantitative changes of their
communities (Koehler, 1999; Skubala and Kafel, 2004; Van
Straalen, 2004; Filser et al., 2008; Haimi and Mätäsniemi,
2012). They have specific traits which explain their useful-
ness in soil ecotoxicology. They are involved in nutrient and
organic matter cycling. Moreover they are widespread, abun-
dant and diverse, and have short reproduction cycles and
they have an almost ubiquitous presence in soil. They are
in close with potential soil contaminants (Van Straalen, 1998,
2004; Santamaría et al., 2012; Huguier et al., 2015). Soil mites
were sensitive to heavy metal pollution and other environ-
mental disturbance/stress factors, such as soil temperature
(T), humidity (H), carbon content (C), total nitrogen (Nt) and
ratio C/Nt (Rantalainen et al., 2006; Gulvik, 2007; Barbercheck
et al., 2009; Ruf and Bedano, 2010; Kardol et al., 2011; Manu,
2011; Lindo et al., 2012). Soil C/Nt ratio is a sensitive indi-
cator of soil quality. Soil C/N ratio is often considered as a
sign of soil nitrogen mineralisation capacity. High soil C/N
ratio can slow down the decomposition rate of organic matter
and organic nitrogen by limiting the soil microbial activ-
ity ability, whereas low soil C/N ratio could accelerate the
process of microbial decomposition of organic matter and
nitrogen. The presence of decomposed organic matter consti-
tutes a favourable habitat for many soil invertebrates (such
as springtails, enchytraeides and nematodes), which repre-
sent the trophic source for soil mites (Acari: Mesostigmata)
(Walter and Proctor, 2013; Klarner et al., 2013). In the same
time soil mites were indirect participants in soil decomposi-
tion, regulating the population densities of these invertebrates
groups (Hasegawa, 2001; Cole et al., 2006; Klarner et al., 2013).
Many researches have shown that soil organic carbon and
nitrogen content are not only affected by climate, altitude,
terrain, but also land use management, as well as by pol-
lution. According to these studies, organic C, total N, were
positively correlated with the heavy metal content of the
soils (Gunther and Holger, 2003; Dai et al., 2004; Ge et al.,
2013).
Researches concerning the impact of heavy metals pollu-
tion on soil mite communities from grassland, in Europa, are
few (Van Straalen, 1998; Ruf and Beck, 2005; Manu et al., 2015).
Mostly oribatids from forest ecosystems were been used, less
predatory mites (Haimi and Siira-Pietikäinen, 1996; Skubala
and Kafel, 2004; Filser et al., 2008; Haimi and Mätäsniemi, 2012;
Skubala and Zaleski, 2012; Van Straalen, 2004).
Please cite this article in press as: Manu, M., et al., Impact assessment of heavy metal pollution on soil mite communities (Acari: Mesostigmata)
from Zlatna Depression – Transylvania. Process Safety and Environmental Protection (2016), http://dx.doi.org/10.1016/j.psep.2016.06.011
In 1980, research on soil mite fauna from forest ecosystems
near Zlatna city revealed that heavy metal pollution affected
the soil mite diversity and community structure (Georgescu,
1984). After 35 years, the main themes of the present research
were to establish the pollution level of the soil, using a mod-
ern technique of analysis (X-ray fluorescence spectrometer)
and to highlight the impact of this phenomenon on soil mite
communities from twelve grasslands situated in the Zlatna
Depression, taking into account the distance from the pollu-
tion source, the degree of pollution, the cumulative influence
of heavy metals and an increased number of environmental
variables, such as: soil temperature, soil humidity, soil acid-
ity, carbon content, nitrogen total, C/N ratio, slope, altitude,
percent of vegetation cover, exposition and soil type.
2. Materials and methods
2.1. Study site
The study was done in twelve grassland ecosystems (E1–E12),
situated in the Zlatna Depression within the Trascău Moun-
tains, Transylvania – Romania (Fig. 1). In this study the
distance from the pollution source (DPS) was considered, in
order to compare the mite communities from the twelve grass-
lands. The pollution source was represented by a chimney
tower of a factory for metallurgical processing of nonferrous
minerals, as: Cu, Zn, Pb, Au and Ag. They were classified
as: “closest” areas located at 976–1805 m from the pollution
source (E1, E4, E7 and E9); intermediate grasslands located at
1805–2240 m from the source (E2, E3, E6 and E8); and remote
ones situated at 2240–3147 m distance from the pollution
source (E5, E10, E11 and E12).
The complete geographical characterisation of the grass-
lands was presented in Table 1. All the investigated areas were
sub-steppic calciphilous grasslands, mainly characterised by
xerophytes, hemicryptophytes and other perennial species,
with a heterogeneous species composition. The species with
the overall highest coverage percentage cover were Agrostis
capillaris, Nardus stricta, Rumex acetosella and Trifolium pratense.
The grasslands were situated at altitudes between 464 and
958 m, and on slopes between 20◦ and 35.48◦ . The soil was
mostly sandy (regosol, haplic-luvisol and eutric-cambisol),
with pH from 4.52 to 5.85 (Table 1).
2.2. Soil samples
The concentrations of six heavy metals were mapped directly
in the field, using XRF (X-ray fluorescence spectrometer): As –
arsenic; Cu – copper; Ni – nickel; Mn – manganese; Pb – lead and
Zn – zinc. Twelve grasslands were investigated. Twenty-five
samples per ecosystems were analysed. The average heavy
metal concentrations from the investigated grasslands were
presented in Table 2. In order to make a comparison between
investigated grasslands and in order to classify them, total
metal load (ML) was calculated as the sum of their levels stan-
dardised by (x − xmin )/(xmax − xmin ), x = concentration of heavy
metal (Santamaría et al., 2012). Three groups were estab-
lished based on different degrees of soil pollution (DP), taking
into account the total metal load: E1, E4 high polluted areas
(ML = 5.30–7.28); E2, E3, E6, E7, E8 the medium polluted grass-
lands (ML = 2.92–3.89) and E5, E9, E10, E11, E12 the less polluted
ones (ML = 1–1.75) (Table 3).
The same number of samples were analysed for the envi-
ronmental variables: soil temperature – T; soil humidity – H%;
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Fig. 1 – Geographical characterisation of the investigated ecosystems from Zlatna Depression – Transilvania (P = pollution
source).
pH; carbon content – C; nitrogen total – N; C/N ratio; Slp
– slope; Alt – altitude; Veg – percent of vegetation cover;
Exp – exposition (W – West; S – South; N – North); Slt –
soil type (RG – Regosol; HL – Haplic-Luvisol; EC – Eutric-
Cambisol). The pH was measured with a C532 Jasco Consort
pH-metre. Soil humidity and temperature were measured
with a mobile soil hygrometer MST 3000+ and a bimetallic
soil thermometer respectively. Organic carbon and total nitro-
gen determinations were made using the Walkley-Black and
Kjeldahl methods respectively (Dalal and Henry, 1985). The
average values of abiotic factors were presented in Table 4.
The mite fauna was sampled in July (six grasslands) and
September (another six grasslands), in 2013, by taking 25 cores
to a depth of 10 cm, with a MacFadyen corer (5 cm diameter), at
each of the twelve grassland sites. The 25 cores were located
within a total of 2500 sq.m. In total 300 soil samples were ana-
lysed. The samples were taken randomly. 961 Mesostigmata
individuals were extracted from the 300 cores, comprising 66
species. The mites were extracted with a modified Berlese-
Tullgren funnel, in ethyl alcohol clarified in lactic acid and
identified to species level, using published identification keys
(Ghilyarov and Bregetova, 1977; Hyatt, 1980; Karg, 1993; Masan,
2003a,b; Masan and Fenda, 2004; Masan, 2007; Masan et al.,
2008; Mášan and Halliday, 2010). All species were deposited in
the collection of the Institute of Biology-Bucharest, Romanian
Academy.
2.3. Data analysis
We tested for significant differences among the three a pri-
ori defined levels of the degree of pollution (high, medium
and low) and the distance from the pollution source (close,
intermedium and remote) respectively, using one-way anal-
ysis of variance (ANOVA). Principal component analysis of
explanatory variables (environmental factors and metal con-
centrations) was used to synthesise major gradients in the
data. PCA was based on Z-transformed data and the correla-
tion matrix (Legendre and Legendre, 1998; Quinn and Keough,
2002).
Please cite this article in press as: Manu, M., et al., Impact assessment of heavy metal pollution on soil mite communities (Acari: Mesostigmata)
from Zlatna Depression – Transylvania. Process Safety and Environmental Protection (2016), http://dx.doi.org/10.1016/j.psep.2016.06.011
3
We modelled species assemblage relationships by apply-
ing a series of Constrained Correspondence Analyses (CCA)
and the so-called “partial CCA”. These approaches can be
used to model the multivariate response of a species assem-
blage to a matrix of explanatory variables, partialling out the
effect of other covariates (Borcard et al., 1992; Legendre and
Legendre, 1998). This technique allows variance partitioning
analogous to the unvaried partitioning of variance (Legendre
and Legendre, 1998). The Correspondence Analysis approach
is appropriate because it preserves the chi-square distance of
the objects to be ordered (samples) and thus correctly handles
community contingency tables (species occurrence and fre-
quency). Species-sample matrices are usually sparse (many
zeros), and several species occur just once or a few times (Hill,
1973; Legendre and Legendre, 1998). No strong pairwise corre-
lations were found between explanatory variables (|r| < 0.78),
indicating low multicollinearity (Berry and Feldman, 1985).
In particular, the following five models were considered:
CCA I: A ∼ f [Degree of pollution]; CCA II: A ∼ f [Distance from
pollution source]; CCA III: A ∼ f [Metals, Environmental Fac-
tors], where A is the species abundance matrix, the function
f is the linear combination of independent variables and the
operator [] describes the operation for partialling out the com-
ponent of variation described by the linear function within
the square brackets. The permutation procedure (based on
9999 cycles) was used to test the significance of constraints
(explanatory variables) in CCA for all eigenvalues (Oksanen
et al., 2006).
We used Generalised Linear Mixed Models (GLMM) to
test whether the main community features (total abundance
and species number) were related to: (1) pollution degree;
(2) distance form pollution source and (3) combination of
environmental factors and metals concentration. The rela-
tive performance of the above models was assessed using a
selection technique based on Akaike’s information criterion
corrected for sample size (AICc: Burnham and Anderson, 2002;
Johnson and Omland, 2004). Models were ranked, and the one
with the lowest AICc was used as the reference for calculating
the AIC difference (i) and the likelihood of a model given the
data and model weights (wi ). Models within two AIC units of
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Table 1 – Ecological characterisation of the investigated grasslands (E1–E12) from Zlatna Depression, in 2014.
Grassland E1 E2 E3 E4

Geographical N: 46◦ 6 37.74 N: 46◦ 6 15.87 N: 46◦ 6 17.13 N: 46◦ 6 48.9

coordination E: 23◦ 14 44.98 E: 23◦ 15 35.11 E: 23◦ 15 17.72 E: 23◦ 15 09.7
Altitude 591 m 544 m 464 m 530 m
Exposure South North West South
Slope 7◦ 35.48◦ 14.27◦ 20◦
FAO soil type Regosol Eutric-Cambisol Eutric-Cambisol Eutric-Cambisol
Dominant plants Achillea millefolium, Carex Achillea millefolium, Achillea millefolium, Agrostis capillaris,
species praecox, Cirsium arvense, Agrostis capillaris, Daucus Agrostis capillaris, Daucus Cynodon dactylon, Juncus
Crataegus monogyna, carota, Juncus inflexus, carota, Carex praecox, inflexus, Rumex acetosella,
Equisetum ramosissimum, Lotus corniculatus, Festuca arundinacea, Thymus sp.
Genista tinctoria, Medicago lupulina, Rumex Galium mollugo, Holcus
Genistella sagittalis, Poa acetosella lanatus, Medicago
pratensis, Rumex lupulina, Mentha
acetosella, Salvia pratensis pulegium, Potentilla
reptans.
Coverage 95% 82% 80% 75%
D.P. 975.71 m 2239.41 m 1907.25 m 1625.52 m
Observations 100 m from E1 is a 20 m from E2 is a Betula A developed moss layer. A bog area and a
deciduous forest forest. developed moss layer.
ecosystems (Fagus sp., A bog area.
Betula sp., Populus sp.).

Grassland E5 E6 E7 E8
◦   ◦   ◦   ◦  
Geographical N: 46 6 97.2 N: 46 6 88.2 N: 46 7 18.61 N: 46 7 21.87
coordination E: 23◦ 15 91.0 E: 23◦ 15 63.1 E: 23◦ 15 18.84 E: 23◦ 15 33.41
Altitude 608 m 519 m 600 m 646 m
Exposure South West South South
Slope 20◦ 20◦ 22.52◦ 26.23◦
FAO soil type Haplic-Luvisol Eutric-Cambisol Regosol Haplic-Luvisol
Dominant plants Agrostis capillaris, Achillea millefolium, Achillea millefolium, Achillea millefolium,
species Pilosella officinarum, Frangula alnus, Rubus Agrostis capillaris, Agrostis capillaris, Daucus
Rumex acetosella. caesius, Rumex acetosella. Cerastium glomeratum, carota, Lotus corniculatus,
Kohlrauschia prolifera, Medicago lupulina,
Nardus stricta, Pilosella Nardus stricta
officinarum
Coverage 80% 100% 85% 80%
D.P. 2507.41 m 2130.60 m 1803.9 m 2143.61 m
Observations A developed moss layer. A developed shrub area A developed moss layer.
with a thin soil layer
with organic matter.

Grassland E9 E10 E11 E12

◦   ◦   ◦   ◦  
Geographical N: 46 7 19.30 N: 46 7 95.1 N: 46 7 78.8 N: 46 8 18.6
coordination E: 23◦ 14 51.00 E: 23◦ 15 19.3 E: 23◦ 15 41.2 E: 23◦ 15 52.1
Altitude 633 m 875 m 808 m 958 m
Exposure South South West West
Slope 22.13◦ 24.51◦ 24◦ 20◦
FAO soil type Regosol Eutric-Cambisol Regosol Eutric-Cambisol
Dominant plants Achillea millefolium, Centaurea triumfetti, Agrostis capillaris, Agrostis capillaris,
species Agrostis capillaris, Genista Plantago lanceolata, Achillea millefolium, Achillea millefolium, Lotus
tinctoria, Lotus Minuartia verna, Nardus Nardus stricta, Pilosella corniculatus, Medicago
corniculatus, Medicago stricta, Potentilla erecta. officinarum, Potentilla lupulina, Nardus stricta,
lupulina, Nardus stricta, erecta, Sanguisorba Pilosella officinarum,
Onobrychis arenaria, officinalis, Thymus sp., Trifolium pratense.
Pilosella officinarum, Trifolium arvense.
Plantago lanceolata
Coverage 85% 85% 90% 95%
D.P. 1311.65 m 2581.47 m 2611.92 m 3146.52 m
Observations 90 m from E10 is an old 65 m from E11 is an old 110 m from E12 is an old
forest with Fagus forest with Fagus forest with Fagus
sylvatica (80–100 years), sylvatica (80–100 years), sylvatica (80–100 years),
situated on rocky situated on rocky situated on rocky
substrate. substrate. substrate.

D.P., distance from pollution source.

Please cite this article in press as: Manu, M., et al., Impact assessment of heavy metal pollution on soil mite communities (Acari: Mesostigmata)
from Zlatna Depression – Transylvania. Process Safety and Environmental Protection (2016), http://dx.doi.org/10.1016/j.psep.2016.06.011
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Table 2 – Concentrations of heavy metals (mg kg−1 ) from the investigated grasslands from Zlatna Depression, taking into
account the distance from pollution source.
Grassland As Cu Mn Ni Pb Zn

Closest to pollution source

E1 55.31 (±1.86) 576.3 (±71.32) 616.34 (±81.77) 34.13 (±8.82) 421.12 (±71.62) 211.69 (±18.72)
E4 23.37 (±2.95) 305.64 (±49.16) 869 (±51.07) 125.80 (±22.80) 278.96 (±36.03) 224.57 (±19.87)
E7 21.04 (±2.12) 156.35 (±76.52) 1156.17 (±451.65) 162.82 (±27.02) 110.68 (±51.67) 162.83 (±16.12)
E9 10.04 (±4.73) 63.63 (±21.62) 672.78 (±85.73) 105.25 (±24.51) 71.16 (±17.41) 119.4 (±20.56)

Intermediate from pollution source

E2 23.22 (±2.62) 135.55 (±61.54) 920.68 (±95.62) 109.72 (±12.52) 155.24 (±54.27) 161.12 (±15.13)
E3 24.38 (±2.74) 147.17 (±71.51) 896.74 (±57.78) 73.74 (±11.45) 167.23 (±56.22) 204.18 (±18.76)
E6 13.03 (±5.80) 100.66 (±64.64) 454.91 (±77.03) 127.23 (±16.37) 105.16 (±48.22) 121.57 (±21.02)
E8 24.38 (±2.62) 80.1 (±27.54) 1344.38 (±511.34) 125.94 (±19.76) 69.76 (±16.52) 121.09 (±20.98)

Remote from pollution source

E5 15.68 (±5.99) 91.49 (±29.87) 387.46 (±69.58) 109.06 (±13.01) 102.49 (±34.19) 99.66 (±13.32)
E10 12.07 (±3.01) 52.16 (±16.19) 1071.34 (±437.92) 102.56 (±23.04) 57.63 (±15.40) 90.83 (±14.35)
E11 10.89 (±4.52) 46.56 (±12.44) 911.17 (±137.47) 121.83 (±19.73) 36.88 (±9.04) 91.27 (±13.91)
E12 7.36 (±5.57) 22.11 (±11.36) 854.91 (±115.33) 100.45 (±18.40) 28.21 (±4.62) 74.49 (±8.41)

Legal normal 5 20 900 20 20 100

values
(reference
values)
according to
M.O. No.
756/03.11.1997

Table 3 – The heavy metal load (ML) for investigated grasslands from Zlatna Depression.
Grassland As Cu Mn Ni Pb Zn Total ML Pollution degree

E1 1 4.13 0.24 0 1 0.91 7.28 High polluted

E2 0.33 0.85 0.56 0.59 0.32 0.58 3.22 Medium polluted
E3 0.35 0.93 0.53 0.31 0.35 0.86 3.34 Medium polluted
E4 0.33 2.11 0.50 0.71 0.64 1 5.30 High polluted
E5 0.17 0.52 0.00 0.58 0.19 0.17 1.63 Low polluted
E6 0.12 0.59 0.07 0.72 0.20 0.31 2.01 Medium polluted
E7 0.29 1 0.80 1 0.21 0.59 3.89 Medium polluted
E8 0.35 0.43 1 0.71 0.11 0.31 2.92 Medium polluted
E9 0.06 0.31 0.30 0.55 0.11 0.30 1.62 Low polluted
E10 0.10 0.22 0.71 0.53 0.07 0.11 1.75 Low polluted
E11 0.07 0.18 0.55 0.68 0.02 0.11 1.62 Low polluted
E12 0 0 0.49 0.52 0 0 1 Low polluted

the AICmin were considered competitive and more plausible 3. Results

than others (Burnham and Anderson, 2002).
All analyses were performed using R version 3.2.1 (R
Development Core Team, 2006). In particular, PCA was com-
pleted using the prcomp procedure. CCA was performed using
the vegan package (Oksanen et al., 2006) and GLMMs using the
nlme package (Pinheiro and Bates, 2000).
Firstly considering the heavy metal concentrations from the
soil of the grasslands, the highest concentrations of As and Cu
were revealed in E1 and the lowest in E12. Medium concentra-
tions were obtained in E2–E11. The highest Pb concentration
was measured in E1 and the lowest in E11, E12. In grasslands

Table 4 – Abiotic factors from the investigated grasslands from Zlatna Depression (T – soil temperature; H – soil humidity;
pH – soil acidity; C – carbon content; Nt – total nitrogen; C/Nt – carbon content/total nitrogen).
Grassland T (◦ C) H (%) pH C% Nt (%) C/Nt

E1 24.24 (±1.91) 35.56 (±1.84) 5.01(±0.62) 5.24 (±0.81) 0.39 (±0.26) 15.73 (±1.71)
E2 22.37 (±1.62) 44.68 (±1.86) 5.73 (±0.12) 1.07 (±0.93) 0.09 (±0.01) 11.49 (±1.24)
E3 21.08 (±1.43) 44.96 (±1.71) 5.07 (±0.11) 2.31 (±0.36) 0.22 (±0.04) 12.01 (±1.26)
E4 31.22 (±5.59) 50.88 (±7.16) 6.16 (±0.94) 1.75 (±0.80) 0.14 (±0.05) 14.54 (±1.68)
E5 32.58 (±10.40) 48.44 (±7.87) 4.51 (±0.13) 2.36 (±0.35) 0.19 (±0.03) 14.43 (±1.13)
E6 29.24 (±0.43) 60.28 (±5.41) 4.90(±0.42) 2.15 (±0.43) 0.19 (±0.05) 12.82 (±1.09)
E7 28.73 (±2.36) 42.76 (±1.92) 5.76 (±0.06) 4.92 (±1.11) 0.41 (±0.28) 12.99 (±1.27)
E8 22.60 (±1.74) 50.24 (±1.62) 5.85 (±0.05) 2.83 (±0.39) 0.29 (±0.06) 11.11 (±1.19)
E9 25.29 (±2.21) 35.64 (±2.42) 5.51 (±0.04) 3.52 (±1.87) 0.30 (±0.05) 13.31 (±1.29)
E10 8.41 (±0.21) 85.48 (±2.63) 5.36 (±0.20) 4.32 (±1.05) 0.33 (±0.06) 15.06 (±2.49)
E11 20.56 (±0.30) 74.56 (±3.67) 5.77 (±0.20) 5.66 (±1.24) 0.38 (±0.05) 17.15 (±1.45)
E12 12.93 (±0.13) 72 (±3.12) 5.53 (±0.07) 4.62 (±0.80) 0.33 (±0.04) 16.18 (±1.55)

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Table 5 – Mean differences of the metal concentrations and lower and upper 95% confidence intervals (CI) from the Tukey
HSD post hoc comparisons among the three levels of pollution degree and distances from pollution source.
Pollution degree Distance from the pollution source

95% CI 95% CI

Mean Lower Upper P Mean Lower Upper P

difference difference

As
Low–high −1.517 −1.904 −1.131 0.000 Intermediate–close −0.529 −0.886 −0.172 0.002
Medium–high −1.030 −1.411 −0.650 0.000 Remote–close −0.924 −1.269 −0.579 0.000
Low–medium 0.487 0.210 0.764 0.000 Remote–intermediate −0.395 −0.726 −0.063 0.015

Cu
Low–high −1.816 −2.175 −1.457 0.000 Intermediate–close −0.858 −1.205 −0.512 0.000
Medium–high −1.475 −1.828 −1.121 0.000 Remote–close −1.115 −1.450 −0.780 0.000
Low–medium 0.341 0.084 0.599 0.006 Remote–intermediate −0.257 −0.578 0.065 0.146

Mn
Low–high 0.490 0.044 0.936 0.027 Intermediate–close 0.012 −0.367 0.392 0.997
Medium–high 0.310 −0.129 0.749 0.221 Remote–close 0.250 −0.117 0.617 0.245
Low–medium −0.180 −0.500 0.140 0.382 Remote–intermediate 0.237 −0.115 0.590 0.252

Ni
Low–high 0.769 0.317 1.222 0.000 Intermediate–close 0.137 −0.272 0.546 0.708
Medium–high 1.021 0.576 1.467 0.000 Remote–close 0.097 −0.298 0.492 0.831
Low–medium 0.252 −0.072 0.577 0.161 Remote–intermediate −0.040 −0.419 0.339 0.966

Pb
Low–high −1.734 −2.119 −1.350 0.000 Intermediate–close −0.745 −1.110 −0.379 0.000
Medium–high −1.371 −1.750 −0.992 0.000 Remote–close −1.035 −1.388 −0.681 0.000
Low–medium 0.364 0.088 0.640 0.006 Remote–intermediate −0.290 −0.629 0.049 0.110

Zn
Low–high −1.518 −1.923 −1.112 0.000 Intermediate–close −0.594 −0.940 −0.248 0.000
Medium–high −0.864 −1.263 −0.465 0.000 Remote–close −1.231 −1.566 −0.897 0.000
Low–medium 0.654 0.363 0.945 0.000 Remote–intermediate −0.637 −0.959 −0.316 0.000

E1 and E4 the maximum values of Zn concentration were
obtained and in E12 the minimum. Examining the results for
Mn and Ni showed a different situation. The highest values of
Mn concentration were recorded in E7, E8, E10, and the low-
est in E5 and E6. For Ni, the most polluted grasslands were E4,
E6, E7, E8 and the least affected ones were E1 and E3. Medium
values for Mn and Ni, were recorded in the rest of grasslands
(Table 2).
The highest total metal loads (ML) were obtained in E1 and
E4, and the lowest in E5, E9, E10, E11 and E12. Medium values of
this parameter were observed in E2, E3, E6, E7 and E8 (Table 3).
Comparison of the mean values of metal concentrations in
the three pollution degree plots revealed significant (ANOVA
F[2,297] > 3 and thus P ≤ 0.05) differences for all the metals with
higher concentration of metals in the high than in the medium
and low pollution gradient plots and in the medium than in the
low pollution gradient plot except for Mn (Table 5). Compari-
son of the mean values of metal concentrations in the three
plots located at close, intermediate and remote distance from
the pollution source showed no significant differences for Mn
(F[2,297] > 1.77, P = 0.173) and Ni (F[2,297] = 0.328, P = 0.721) and sig-
nificant differences for As, Cu, Pb and Zn (ANOVA F[2,297] > 19
and thus P ≤ 0.01) with higher concentration of metals in the
closer plots than in the intermediate and remote plots and
higher in the intermediate than in the remote plots (Table 5).
If we take into discussion the abiotic factors, the highest
average values of soil temperature was recorded in E5, whilst
in E10, we recorded the lowest value. Soil humidity was highest
in E10, E11, E12, in contrast to E1 and E9, where the values were
lowest. The most acid soil was identified in E5 and E6 and the
least acid in E4. The carbon content of the soil was greatest
in E1 and E11, whereas the lowest values were obtained in E2
and E4. Nitrogen content in the soil varied from 0.09% in E2 to
0.41% in E7. If we focus on the C/N ratio, the highest value of
this variable was recorded in E11 and the lowest in E8 (Table 4).
In others grasslands the values of these abiotic factors varied
between the maximum and the minimum limits.
In the twelve grasslands, 66 species of Mesostigmata mites
were identified, with 961 individuals. Each investigated grass-
lands were described by a characteristically structure of the
soil mite populations (species diversity, numerical abundance,
dominant species) (Table 6). The highest value of numerical
abundance and number of species (28 species with 267 indi-
viduals) was recorded in E12, in comparison with the other
grasslands and especially with E5 and E9, where the lowest
values were obtained (9 and 11 species, with 28 individuals
each) (Table 6). Dominant species were: Hypoaspis praesternalis
(258 individuals), Hypoaspis aculeifer (130 individuals), Asca
bicornis (93 individuals), Hypoapis oblonga (71 individuals) and
Hypoaspis vacua (60 individuals). In contrast, five species were
represented by a single individual: Parazercon radiatus, Proz-
ercon kochi, Zercon hungaricus, Trachytes irenae, Vulgarogamasus
kraepelini.
Principal component analysis (PCA) classified the sites in
three groups as a function of pollution degree and distance
from the pollution source (Figs. 2 and 3). The first two principal
components of the PCA accounted for 22.2 and 32.3% of the
variance respectively.
The low polluted and intermediate from the pollution
source plots form a separate cluster from high polluted and
close from the pollution source plots but partially overlapped
with medium polluted and remote from the pollution source

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Table 6 – Numerical abundance of the mesostigmatid mites identified from investigated grasslands (E1–E12).
No. Species Code E1 E2 E3 E4 E5 E6 E7 E8 E9 E10 E11 E12 Total

1 Amblyseius sp. Am sp 1 1 0 0 0 0 1 3 0 0 3 0 9
2 Androlaelaps casalis (Berlese, 1887) An ca 0 0 0 0 0 0 0 0 0 0 0 1 1
3 Antennoseius avius Karg, 1976 An av 0 0 0 0 0 0 1 0 0 0 0 0 1
4 Antennoseius bacatus Athias-Henriot, 1961 An ba 0 0 0 0 0 0 3 0 0 0 0 0 3
5 Arctoseius semiscissus (Berlese, 1892) Ar se 0 0 0 0 1 0 0 1 0 0 0 0 2
6 Asca bicornis (Canestrini and Fanzago, 1887) As bi 5 7 7 17 3 0 26 5 2 8 2 11 93
7 Cheiroseius borealis (Berlese, 1904) Ch bo 0 3 0 0 0 0 2 0 0 0 0 0 5
8 Cheiroseius bryophilus Karg, 1969 Ch br 2 0 0 0 0 0 0 0 0 0 0 5 7
9 Eviphis ostrinus (C.L. Koch, 1836) Ev os 0 0 0 0 0 1 0 0 0 0 0 0 1
10 Gamasellodes bicolor (Berlese, 1918) Ga bi 0 0 0 2 0 0 1 1 0 0 0 0 4
11 Geholaspis longispinosus Kramer, 1876 Ge lo 0 0 0 0 0 0 0 0 2 0 0 0 2
12 Holoparasitus calcaratus (C.L. Koch, 1839) Ho ca 0 0 4 0 0 0 0 1 0 0 0 0 5
13 Hypoaspis aculeifer (Canestrini, 1883) Hy ac 0 0 1 58 1 6 1 0 0 0 4 59 130
14 Hypoaspis angusta Karg, 1965 Hy an 0 0 0 2 0 0 0 0 0 0 0 0 2
15 Hypoaspis astronomica (C.L. Koch, 1839) Hy as 0 2 0 0 0 0 0 0 0 0 1 1 4
16 Hypoaspis claviger (Berlese, 1882) Hy cl 0 0 0 0 0 0 0 0 0 0 1 2 3
17 Hypoaspis karawaiewi (Berlese, 1903) Hy ka 2 0 0 2 0 0 1 0 4 1 0 2 12
18 Hypoaspis miles (Berlese, 1882) Hy mi 0 0 3 0 0 0 5 1 0 1 0 0 10
19 Hypoaspis oblonga (Halbert, 1915) Hy ob 1 2 0 0 0 0 1 8 2 4 22 31 71
20 Hypoaspis preasternalis (Wilmann, 1949) Hy pr 19 9 11 11 0 16 5 9 10 24 51 93 258
21 Hypoaspis sp.1 Hy sp.1 0 0 0 0 0 3 1 1 1 2 1 5 14
22 Hypoaspis vacua (Michael, 1891) Hy va 0 0 5 4 5 4 0 0 0 13 22 7 60
23 Hypoaspis austriaca (Sellnick, 1935) Hy au 0 0 0 0 0 0 0 0 0 1 0 0 1
24 Hypoaspis gracilis Meledjaeva,1963 Hy gr 3 0 0 0 0 0 0 0 0 0 0 0 3
25 Hypoaspis sp.2 Hy sp.2 0 0 0 0 0 0 4 2 3 0 0 0 9
26 Iphidonopsis pulvisculus (Berlese, 1921) Ip pu 0 0 0 0 0 0 0 0 0 1 0 1 2
27 Iphidonopsis sp. Ip sp 0 0 0 0 0 0 0 0 0 0 0 1 1
28 Iphidozercon gibbus Berlese, 1903 Ip gi 0 0 0 0 0 0 0 5 0 0 0 0 5
29 Lasioseius berlesei (Oudemans, 1938) La be 0 0 0 0 0 0 0 0 0 0 1 0 1
30 Lasioseius sp. La sp 0 1 0 0 0 0 0 0 0 0 4 2 7
31 Lasioseius youcefi Athais-Henriot, 1959 La yo 0 0 0 0 0 0 0 3 0 0 0 0 3
32 Leioseius insignitis (Hirschmann, 1963) Le in 0 0 0 0 0 0 0 0 0 2 0 0 2
33 Lysigamasus misellus (Berlese, 1904) Ly mi 9 3 3 0 0 0 1 0 0 2 1 7 26
34 Lysigamasus sp. Ly sp 4 4 2 0 0 0 0 0 0 0 0 0 10
35 Macrocheles recki Bregetova and Koroleva 1960 Ma re 0 0 0 0 1 0 0 0 1 0 0 2 4
36 Ololaelaps placentula (Berlese, 1887) Ol pl 0 0 0 0 1 2 0 0 0 0 0 1 4
37 Ololaelaps veneta (Berlese, 1904) Ol ve 0 0 3 0 0 0 0 3 0 0 0 0 6
38 Ololealaps sellnicki Bregetova and Koroleva 1964 Ol se 0 0 0 0 0 0 0 0 0 0 0 4 4
39 Oplitis minutissima (Berlese, 1903) Op mi 0 0 0 0 0 0 0 0 0 3 1 7 11
40 Pachylaelaps furcifer Oudemans, 1903 Pa fu 3 1 4 0 0 1 0 0 0 0 0 0 9
41 Pachylaelaps pectinifer (G. and R. Canestrini, 1881) Pa pe 0 0 0 1 0 0 0 0 0 0 0 1 2
42 Pachylaelaspis troglophilus Halbert, 1915 Pa tr 2 0 0 0 0 0 0 0 0 0 0 0 2
43 Parasitus fimetorum (Berlese, 1904) Pa fi 1 0 2 0 0 0 0 2 0 0 0 0 5
44 Parazercon radiatus (Berlese, 1910) Pa ra 0 0 0 0 0 0 0 0 0 0 1 0 1
45 Pergamasus crassipes Berlese, 1906 Pe cr 0 3 0 0 0 0 0 0 0 0 0 0 3
46 Proctolaelaps pygmaeus (Muller, 1860) Pr py 0 0 0 1 0 0 0 0 0 0 0 0 1
47 Protogamasellus mica (Athias-Henriot, 1961) Pr mi 0 0 0 0 0 6 0 0 0 0 0 0 6
48 Prozercon kochi Sellnick, 1943 Pr ko 0 0 0 0 0 1 0 0 0 0 0 0 1
49 Prozercon sellnicki Halaskova, 1963 Pr se 0 0 1 0 0 0 4 0 0 0 0 0 5
50 Rhodacarellus perspicuus Halaskova, 1958 Rh pe 0 4 0 1 2 0 0 0 0 3 0 3 13
51 Rhodacarellus silesiacus Willmann, 1953 Rh si 1 0 1 8 3 3 0 1 1 2 3 10 33
52 Rhodacarus coronatus Berlese, 1921 Rh co 0 0 0 0 0 0 0 0 0 0 0 2 2
53 Rhodacarus denticulatus Berlese, 1921 Rh de 0 0 0 0 11 6 0 1 0 4 0 0 22
54 Rhodacarus roseus Oudemans, 1902 Rh ro 0 0 0 0 0 0 1 6 0 0 0 1 8
55 Trachytes aegrota (C.L. Koch, 1841) Tr ae 0 0 2 0 0 0 3 0 0 0 0 0 5
56 Trachytes irenae Pecina, 1969 Tr ir 0 0 0 0 0 1 0 0 0 0 0 0 1
57 Trachytes pauperior Berlese, 1914 Tr pa 0 0 0 0 0 0 0 0 0 0 0 2 2
58 Uropoda orbicularis (O.F. Muller, 1776) Ur or 0 0 0 0 0 0 0 0 0 1 0 3 4
59 Uropoda sp. Ur sp 0 0 11 0 0 0 0 0 0 0 0 0 11
60 Veigaia exigua (Berlese, 1916) Ve ex 0 0 1 0 0 0 2 2 0 0 0 2 7
61 Veigaia nemorensis (C.L. Koch, 1839) Ve ne 3 0 3 0 0 0 0 0 0 0 0 0 6
62 Vulgarogamasus kraepelini (Berlese, 1905) Vu kr 0 0 0 0 0 0 0 0 1 0 0 0 1
63 Zercon berlesei Sellnick, 1958 Ze be 0 0 0 0 0 1 5 0 0 0 0 0 6
64 Zercon hungaricus Sellnick, 1958 Ze hu 0 0 0 0 0 1 0 0 0 0 0 0 1
65 Zercon triangularis (C.L. Koch, 1836) Ze tr 0 0 0 0 0 0 2 0 0 0 0 0 2
66 Zerconopsis remiger (Kramer, 1876) Ze re 0 0 0 0 0 0 0 3 1 1 0 1 6

Total no. of individuals 56 40 64 107 28 52 70 58 28 73 118 267 961

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Fig. 2 – Principal component analysis of the explanatory variables – sites (ordered objects) matrix as a function of pollution
degree. Samples were coded as follows: high polluted plot (back closed circle), medium polluted (dark grey closed triangle)
and low polluted plot (light grey square). The arrow coordinates are built from the PC1 and PC2 eigenvector coefficients.
Variables are: T – soil temperature, H – soil humidity; C – carbon content, Nt – nitrogen total; Alt – altitude, Slp – slope, Veg –
percent of vegetation cover; C/N; heavy metals: As, Cu, Pb, Zn, Ni, Mn.

Fig. 3 – Principal component analysis of the explanatory variables – sites (ordered objects) matrix as a function of distance
from the pollution source. Sites were coded as follows: closest to the pollution source (back closed circle), intermediate from
the pollution source (dark grey closed triangle) and remote from the pollution source (light grey square) plot. The arrow
coordinates are built from the PC1 and PC2 eigenvector coefficients. Variables are: T – soil temperature, H – soil humidity; C –
carbon content, Nt – nitrogen total; Alt – altitude, Slp – slope, Veg – percent of vegetation cover; C/N; heavy metals: As, Cu,
Pb, Zn, Ni, Mn.

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plots. High polluted and close from the pollution source and
medium polluted and remote from the pollution source plots
cannot be differentiated and high-polluted plots and close
from the pollution source vary more than medium polluted
and remote from the pollution source plots (Figs. 2 and 3).
The group defined by low pollution and location interme-
diate from the pollution source was negatively correlated with
soil temperature (T); the medium pollution and remote from
the pollution source groups were positively correlated with
environmental factors (Alt and H) and Mn. The group defined
by high pollution and close proximity to the pollution source
were strongly correlated with As, Cu, Pb and Zn (Figs. 2 and 3).
For the distance from pollution source differences among
the close to the pollution source, intermediate from the pollu-
tion source and remote from the pollution source plots were
less pronounced. All the three clustered overlapped within PC1
and PC2 (Fig. 2).
When the CCA for the models of equations CCAI, CCA
II and CCA III (see Section 2) were applied to the species
abundance matrix A, the permutation test indicated that
explanatory variables accounted for a significant (999 permu-
tations, P < 0.05) portion of species distribution variations in all
three models. The first two canonical axes clarifies the main
community patterns (Fig. 4A–C): species assemblages show
a gradient in species composition that is collinear with the
variation in pollution degree (Fig. 4A), distance from the pol-
lution source (Fig. 4B), and to overall environmental and metal
pollution (Fig. 4C).
In the biplots, Optilis minutissima and Hypospis oblonga were
the most abundant in low and remote polluted plots; whilst

Fig. 4 – Biplots of the CCA models for the species abundance matrix: species and (A) pollution degree (B) distance from the
pollution source and (C) pooled environmental factors and heavy metals. Variables are: DP – pollution degree, DPS –
distance from the pollution source, T – soil temperature, H – soil humidity; C – carbon content, Nt – Nitrogen total; C/N;
heavy metals: As, Cu, Pb, Zn, Ni, Mn, Slp – slope; Alt – altitude; Veg – percent of vegetation cover; ExpW – exposition West;
ExpS – exposition South; SltRG – soil type Regosol; SltHL – soil type Haplic-Luvisol. Species names were abbreviated using
the initials of the genus and species name (abbreviations are reported in Table 6).

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Table 7 – Akaike statistics for model including the species richness and the species abundance. AIC (Akaike’s
Information Criterion) differences (AICc) and Akaike weights (wi ) were used to rank models relative to the best model
(minimum AIC). K – number of parameters; LL – log likelihood.
Model Covariates LL K AICc AIC wi

Species richness
1 Pollution degree 391.59 5 793.17 0 0.58
2 Distance from pollution source 392.34 5 794.67 1.5 0.27
3 Environmental factors and heavy metals 375.93 22 795.87 2.69 0.15

Abundance
1 Pollution degree −645.11 5 1300.21 1.65 0.23
2 Distance from pollution source −644.28 5 1298.56 0 0.51
3 Environmental factors and heavy metals −627.96 22 1299.92 1.36 0.26

Rhodacarus denticulatus and Uropoda sp. were commonest in
medium and intermediate polluted plots (Fig. 4A and B). The
CCA results for the global model showed that C/N, H, Alt,
Slp, Nt, Mn and As are the strongest determinants of species
community composition. Cu and South exposition showed
a role in grouping Parasitus fimetorum and Asca bicornis. Zn
showed more association with Geholapsis longispinosus and
Pb with Zercon berlesei. Hypoaspis angusta, Proctolaelaps pyg-
maeus, Eviphis ostrinus and Hypoaspis aculeifer were associated
with West exposition. Rhodacarus roseus with haplic-luvisol
soil type, respectively (Fig. 4C).
Based on model selection, using AIC, models with a propri
defined pollution gradient (degree of pollution and distance
to the pollution source) were best supported, whereas those
including environmental factors and heavy metals were con-
sidered less likely (Table 7).
4. Discussion
According to national legislation, all heavy metal concentra-
tions on the studied grasslands exceeded the reference values
(M.O. 756/03.11.1997), except locally for Mn in a few areas (E2,
E7, E8, E10, E11) where the soil concentrations were lower than
legal-reference values.
Focussing on the distance from pollution source, we
observed that the concentrations of As, Cu, Pb were the high-
est in the grasslands located closest to the chimney tower (E1,
E4) and the lowest in remote areas (E10, E11 and E12). Medium
concentrations of heavy metals were obtained in E2, E3, E6 and
E8. The total heavy metal load for the investigated grasslands
revealed that the most polluted were E1 and E4, situated clos-
est to the pollution source. The least polluted areas were E5,
E9, E10, E11 and E12, most of them in greater distance from
the chimney tower. Although the grasslands E7 and E9 were
situated near to the pollution source, only medium values (E7)
and low values (E9) of heavy metals were recorded in these
areas. In the same time it is possible that the same type of
soil (regosol), the same exposure (South) and indirectly the
wind direction to determine a lower level of pollution. Stud-
ies concerning the heavy metals concentrations from different
type of soils revealed that protisols class (including regosol
type) accumulated lower concentrations of pollutants than
cambisols (Damian et al., 2008).
The highly polluted grasslands were characterised by the:
highest soil temperatures, acid soils, medium values of soil
humidity and carbon content. In the same time in polluted
areas were identified high or medium values of nitrogen total
(Table 4).
In the medium polluted areas most soil temperatures
recorded had medium values, the lowest soil humidity, acid
soils, the lowest carbon content, nitrogen total and decom-
posed organic matter (C/Nt < 15) (Lăcătuşu, 2006; Ge et al.,
2013) (Table 4).
The low polluted areas were characterised by medium val-
ues of soil temperatures, by the highest values of pH, carbon
content, nitrogen total and by undecomposed organic matter
(C/Nt > 15) (Lăcătuşu, 2006; Ge et al., 2013).
We observed that even if the E1 and E4 was classified as
high pollution areas, the soil pH (6.16) and nitrogen content
(0.39%) were the highest (Table 4).
In soil from investigated grasslands, 66 mite species were
identified. This parameter recorded lower values in compar-
ison with those obtained by other researchers in natural
grasslands from Latvia (75 species) (Salmane, 2001); but com-
parable with those from Ireland and Norway, where were
identified 52–54 species (Arroyo et al., 2015; Slomian et al.,
2005). In other countries the number of species is lower:
20–50 species in Germany and Austria (Curry, 1969; Buryn and
Hartmann, 1992; Ruf and Beck, 2005; Wissuwa et al., 2012);
21–42 species in Poland and Irish natural sites (Niedbala et al.,
1990; Skorupski et al., 2008). In Romania studies on the mites
communities from two types of grasslands – hay fields and
pastures – situated in the Moldavian Plain, revealed the pres-
ence of 38 species (Călugăr, 2006a,b).
Principal components analysis (PCA) revealed that the soil
mite communities from the most polluted grasslands, as
well from the areas situated closest to the pollution source
were distinguishable from those from less polluted ones, dis-
tanced from chimney tower. Grasslands located closest to
the pollution source were characterised by the lowest num-
ber of species, in comparison with those more distant from
the chimney tower, where these parameters had the high-
est values. The same situation was obtained for numerical
abundances. These results were in concordance with other
studies which confirmed that mites represented a sensitive
soil group to heavy metal pollution (Georgescu, 1984; Haimi
and Siira-Pietikäinen, 1996; Ruf, 1998; Santamaría et al., 2012).
In the same time, the mite communities from low polluted
and intermediate grasslands and those from medium polluted
and remoted from the pollution source, had recorded closed
values of numerical densities and common species, as: Cheiro-
seius borealis, Holoparasitus calcaratus, Hypoaspis astronomica,
Hypoaspsis oblonga, Ololaelaps veneta, Pergamasus crassipes, Proz-
ercon sellnicki, Trachytes aegrota and Uropoda sp. In these two
types of grasslands, mentioned above, the influence of pol-
lution metal is low. The influencing factors were altitude,
soil humidity and temperature. Species as Trachytes aegrota

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or Uropoda sp., are indicator mites for less undisturbed
ecosystems (with soil rich in organic matter and high humid-
ity) (Napierała and Błoszyk, 2013; Napierala et al., 2015). Other
species as Holoparasitus calcaratus and Pergamasus crassipes,
prefer mainly forest soils (Skorupski et al., 2008; Manu, 2011).
It is possible that the small distance from the forest ecosys-
tems situated closed to grasslands (even 20 m) to influence the
composition of mite communities.
The statistical analysis revealed that the heavy metals
concentrations influenced the soil mites from high polluted
grasslands, while the Mn and abiotic factors were more impor-
tant for invertebrate communities from the medium and low
polluted areas. The investigated mite communities are an
edaphic group of fauna. When pollution is not a stress fac-
tor, as in medium and low polluted areas (where the ML for
the Mn is lowers than 1), the soil environmental conditions
became the main influencing variables for mite populations.
Acid soil and the presence of decomposed organic matter
from medium polluted areas, were suitable conditions for
other invertebrates (enchytraeids, springtails, nematodes, ori-
batids), which are the trophic source for Mesostigmata mites
(Walter and Proctor, 2013; Klarner et al., 2013).
The most relevant species, identified as numerically
dominant were: Hypoaspis praesternalis, Hypoaspis aculeifer,
Asca bicornis, Hypoaspis oblonga, Hypoaspis vacua, Lysigamasus
misellus and Rhodacarellus silesiacus. These species were char-
acteristic for dry grasslands from Europe (Călugăr, 2006a,b;
Skorupski et al., 2008; Wissuwa et al., 2012; Arroyo et al., 2015).
Hypoaspis aculeifer has a wide ecological plasticity, being
capable to resist to unfavourable environment conditions
as those from polluted ecosystems (Masan, 2007; Manu
and Honciuc, 2010; Van Gestel, 2012). Hypoapis aculeifer and
Hypoaspis vacua are generalist species, with holarctic distribu-
tion (Salmane and Brumelis, 2010). Hypoaspis praesternalis is
a cosmopolite species, founded in Europe and Asia, but pref-
erential praticolous mite in Romania (Călugăr, 2006b; Manu
et al., 2015). Asca bicornis inhabits a wide range of habitats and
conditions from cold and wet to xerothermic habitats, forests,
meadows, and agricultural habitats. It is a species with wide
ecological adaptability and an unclear preference to habitat
in Europe (Salmane and Brumelis, 2010; Dirilgen et al., 2015).
European study concerning the mite community composition
across a European transect, revealed that Lysigamasus misellus
was identified only in continental grasslands (Dirilgen et al.,
2015). In other studies from Europe, Rhodacarellus silesiacus was
found in natural grasslands, but also in spruce forest, bog-
lands, arable fields and urban parks. It is considered a good
indicator of not the type of habitat but the processes that habi-
tat undergoes (Skorupski et al., 2008; Manu and Honciuc, 2010;
Kaczmarek et al., 2012; Wissuwa et al., 2012).
In contrast Vulgarogamasus kraepelini, Parazercon radiatus,
Prozercon kochi, Zercon hungaricus and Trachytes irenae are
species that inhabit soil rich in organic matter from natural,
undisturbed ecosystems (Masan and Fenda, 2004; Napierała
and Błoszyk, 2013; Manu and Ion, 2014; Napierala et al., 2015).
Temperature was strongly related with soil mites from the
less polluted grasslands, higher values of this abiotic factor
being associated with decreased numerical abundance. This
phenomenon was observed by other specialists, only constant
temperature being favourable for more numerous populations
(Huhta and Hänninen, 2001; Malmstrom, 2008; Jung et al., 2010;
Manu, 2011; Kardol et al., 2011). On the other hand, in other
studies, it was observed that even if the warming had only
minor direct effects on the fauna, increased temperatures are
Please cite this article in press as: Manu, M., et al., Impact assessment of heavy metal pollution on soil mite communities (Acari: Mesostigmata)
from Zlatna Depression – Transylvania. Process Safety and Environmental Protection (2016), http://dx.doi.org/10.1016/j.psep.2016.06.011
11
often associated with lower moisture, and the indirect effects
of changes in soil moisture may be more important for the
survival and reproductive ability of soil fauna than the direct
effects of warming (Xu et al., 2012).
Canonical correspondence analysis showed us that not
only heavy metals influenced the mites (Cu, Zn, Pb), but also
some environmental variables as C/N, H, Nt, altitude and
slope were the strongest determinants of species community
composition. It is scientifically proven that these parameters
influenced the soil fauna in general as well as the mites specif-
ically (Chikoski et al., 2006; Cole et al., 2006; Santamaría et al.,
2012).
Asca bicornis and Parasitus fimetorum were influenced by the
Cu concentrations. Asca bicornis was identified by other spe-
cialists in the first stage of succession in derelict industrial
lands, in polluted forest ecosystems with heavy metals, as
well as in air-polluted urban areas (Georgescu, 1984; Seniczak
et al., 1995; Masan and Fenda, 2004; Gwiazdowicz, 2007; Manu
and Honciuc, 2010). Parasitus fimetorum was recorded as mite
species identified in industrial and postindustrial areas from
Poland, being considered as pioneer specie found on rail-
way embankments and in sludge (Gołda and Madej, 1996;
Skorupski et al., 2013).
On the other hand, populations of Geholaspis longispinosus
were influenced by Zn pollution and those of Zercon berlesei by
Pb. Although these species have a wide ecological plasticity
and tolerance, being well adapted to the xerothermophilous
phytocoenosis, the increased value of heavy metals, especially
in the most polluted grasslands (up to 20 times for Pb and 2
times for Zn, in comparison with legal reference values) influ-
ence their numerical abundance (Masan, 2003a; Masan and
Fenda, 2004).
Rhodacarus roseus was correlated with haplic-luvisol. In
comparison with regosol, luvisols are characterised by a high
nutrient content, good drainage and by a surface accumula-
tion of humus (Lăcătuşu et al., 2001). Organic matter was a
favourable habitat for other invertebrates fauna, which repre-
sent the trophic source for predator mite, as Rhodacarus roseus
(Lavelle et al., 2006; Walter and Proctor, 2013). In general, Rho-
dacarus roseus is a characteristic species for forest ecoystems
(Salmane, 2001; Salmane and Brumelis, 2010; Manu, 2011;
Manu and Ion, 2014). The location of the grasslands closed to
Fagus sylvatica forests and the type of soil influence the mite
community composition.
5. Conclusions
Each investigated grassland was described by a characteristic
structure of the soil mite populations. All heavy metals exceed
the reference legal values concentrations in almost all inves-
tigated grasslands. The heavy metal concentrations increased
with the proximity to the pollution source. The degree of pol-
lution with heavy metal from soil in investigated areas and
the distance from pollution source were the main variables
that influenced the soil invertebrates. The mite communities
from the most polluted areas, as well from the ecosystems
situated closest to the pollution source, were distinguishable
from those from less polluted grasslands, further away from
chimney tower. Heavy metals Cu, As, Zn and Pb influence the
soil mites from highly polluted ecosystems. At the same time,
the influence of some heavy metals on mite populations is cor-
related with other environmental variables, as soil humidity,
soil temperature, altitude, slope, exposure and type of soil, Nt
and C/N.
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All applied statistical tools highlighted that heavy metal Mică smelters – Romania. Carpathian J. Earth Environ. Sci. 3,
pollution, as well as investigated environmental variables, 65–82.
have an important impact on soil mite communities, resulting Dirilgen, T., Arroyo, J., Dimmers, W.J., Faber, J., Stone, D., Martins
da Silva, P., Carvalho, F., Schmelz, R., Griffiths, B.S., Francisco,
in modified species diversity, and altered numerical abun-
R., Creamer, R.E., Sousa, J.P., Bolger, T., 2015. Mite community
dance and species composition. These features allow the use composition across a European transect and its relationships
of the soil mite fauna as a valuable biological tool for heavy to variation in other components of soil biodiversity. Appl.
metal impact assessment from polluted ecosystems. Soil Ecol. 97, 86–97.
Dragovic, S., Mihailovic, N., Gajic, B., 2008. Heavy metals in soils:
Acknowledgments distribution, relationship with soil characteristics and
radionuclides and multivariate assessment of contamination
sources. Chemosphere 72, 491–495.
This study was carried out in the framework of the projects:
Filser, J., Koehler, H.H., Ruf, A., Rőmbke, J., Prinzing, A., Schaefer,
RO1567-IBB01/2016 from Institute of Biology Bucharest, Roma- M., 2008. Ecological theory meets soil ecotoxicology: challenge
nian Academy and No. 50/2012 (ASPABIR) – Priority Uefiscdi and chance. Basic Appl. Ecol. 9, 346–355.
Partnerships. The authors wish to thank Owen Mountford, Ge, S., Xu, H., Ji, M., Jiang, Y., 2013. Characteristics of soil organic
from NERC (National Environment Research Council, Centre carbon, total nitrogen, and C/N ratio in Chinese apple
for Ecology and Hydrology, UK) for advice on the English text. orchards. Open For. Sci. J. 3, 213–217.
Georgescu, A., 1984. Fauna de Gamaside (acarieni) din soluri
We thank to Simona Plumb and Rodica Iosif for their assis-
poluate din zona industrială Zlatna (Gamasids fauna (mites)
tance in the lab and the field. from polluted soil from Zlatna industrial area). St. Cerc. Biol.
Seria Biol. Anim. 36, 33–39.
References Ghilyarov, M.S., Bregetova, N.G., 1977. Opredelitel’ obitayushchikh
v pochve kleshcheı̆ (Mesostigmata) (Handbook for the
identification of soil-inhabiting mites (Mesostigmata)).
Arroyo, J., Grady, A.O., Vance, H., Bolger, T., 2015. The mite (Acari:
Zoological Institute of the Academy of Sciences, Petrograd,
Oribatida, Mesostigmata) assemblages associated with Lasius
Russia.
flavus (Hymenoptera: Formicidae) nests and surrounding soil
Gołda, T., Madej, G., 1996. Preliminary investigations on
in an Irish grassland. Biol. Environ.: Proc. R. Irish Acad. 115,
Mesostigmata mite community in the soil at initial forming
1–12.
stage on recultivated areas of sulphur mining. Acta Biol. Sil.
Barbercheck, M.E., Neher, D.A., Anas, O., El-Allaf, S.M., Weicht,
45 (28), 139–146.
T.R., 2009. Response of soil invertebrates to disturbance across
Gulvik, M.E., 2007. Mites (Acari) as indicators of soil biodiversity
three resource regions in North Carolina. Environ. Monit.
and land use monitoring: a review. Pol. J. Ecol. 55, 415–450.
Assess. 152, 283–298.
Gunther, S., Holger, K., 2003. Bulk soil C to N ratio as a simple
Berry, W.D., Feldman, S., 1985. Multiple Regression in Practice.
measure of net N mineralization from stabilized soil organic
Sage, Newbury Park, CA.
matter in sandy arable soils. Soil Biol. Biochem. 35, 629–632.
Borcard, D.P., Legendre, P., Drapeau, P., 1992. Partialling out the
Gwiazdowicz, D., 2007. Ascid mites (Acari, Gamasina) from
spatial component of ecological variation. Ecologia 73,
selected forest ecosystems and microhabitats in Poland.
1045–1055.
University Augusta Cieszkowskiego, Poznan.
Burnham, K.P., Anderson, D.R., 2002. Model Selection and
Haimi, J., Siira-Pietikäinen, A., 1996. Decomposer animal
Multimodel Inference: A Practical Information – Theoretic
communities in forest soil along heavy metal pollution
Approach, second ed. Springer, New York.
gradient. Fresenius J. Anal. Chem. 354, 672–675.
Buryn, R., Hartmann, P., 1992. Gamasid fauna (Acari,
Haimi, J., Mätäsniemi, L., 2012. Soil decomposer animal
Mesostigmata) of a hedge and adjacent meadows in Upper
community in heavy-metal contaminated coniferous forest
Franconia (Bavaria, Germany). Pedobiologia 36, 97–108.
with and without liming. Eur. J. Soil Biol. 38 (2), 131–136.
Călugăr, A., 2006a. Qualitative and quantitative studies upon the
Hasegawa, M., 2001. The relationship between the organic matter
edaphic microarthropods fauna in some grassland
composition of a forest floor and the structure of a soil
ecosystems from Moldavia Plain (Romania). Complexul
arthropod community. Eur. J. Soil Biol. 37, 281–284.
Muzeal de Ştiinţele Naturii “Ion Borcea” Bacău, St. Com 21,
Hernandez, L., Probst, A., Probst, J.L., Ulrich, E., 2003. Heavy metal
230–231.
distribution in some French forest soils: evidence for
Călugăr, A., 2006b. On the gamasid fauna (Acari: Gamasina) from
atmospheric contamination. Sci. Total Environ. 312, 195–219.
the grassland ecosystems from Moldavia Plain (Romania).
Hill, M.O., 1973. Reciprocal averaging: an eigenvector method of
Complexul Muzeal de Ştiinţele Naturii “Ion Borcea” Bacău, St.
ordination. J. Ecol. 61, 237–249.
Com 21, 231–235.
Hu, Y., Liu, K., Bai, J., Shih, K., Zeng, E.Y., Cheng, H., 2013.
Chikoski, J.M., Ferguson, S.H., Meyer, L., 2006. Effects of water
Assessing heavy metal pollution in the surface soils of a
addition on soil arthropods and soil characteristics in a
region that had undergone three decades of intense
precipitation-limited environment. Acta Oecol. 30, 2003–2211.
industrialization and urbanization. Environ. Sci. Pollut. Res.
Cole, L., Bradford, M.A., Shaw, P.J.A., Bardgett, R.D., 2006. The
20, 6150–6159.
abundance, richness and functional role of soil meso- and
Huguier, P., Manier, N., Owojori, O.J., Bauda, P., Pandard, P.,
macrofauna in temperate grassland—a case study. Appl. Soil
Rombke, J., 2015. The use of soil mites in ecotoxicology: a
Ecol. 33, 186–198.
review. Ecotoxicology 24 (1), 1–18.
Curry, J.P., 1969. The qualitative and quantitative composition of
Huhta, V., Hänninen, S.M., 2001. Effects of temperature and
the fauna of an old grassland site at Celbridge, Co. Kildare.
moisture fluctuations on an experimental soil
Soil Biol. Biochem. 1, 219–227.
microarthropod community. Pedobiologia 45, 279–286.
Dai, J., Rouiller, J.H., Reversta, G., Bernhard-Reversat, F., Lavelle, P.,
Hyatt, K.H., 1980. Mites of the subfamily Parasitinae
2004. Influence of heavy metals on C and N mineralisation
(Mesostigmata: Parasitidae) in the British Isles. Bull. Br. Mus.
and microbial biomass in Zn-, Pb-, Cu-, and Cd-contaminated
38, 237–378.
soils. Appl. Soil Ecol. 25, 99–109.
Johnson, J.B., Omland, K.S., 2004. Model selection in ecology and
Dalal, D.C., Henry, R.J., 1985. Simultaneous determination of
evolution. Trends Ecol. Evol. 19, 101–108.
moisture, organic carbon, and total nitrogen by near infrared
Jung, C., Kim, J.W., Marquardt, T., Kaczmarek, S., 2010. Species
reflectance spectrophotometry. Soil Sci. Soc. Am. J. 50,
richness of soil gamasid mites (Acari: Mesostigmata) in
120–123.
fire-damaged mountain sites. J. Asia Pac. Entomol. 13,
Damian, F., Damian, G., Lăcătuşu, R., Iepure, G., 2008. Heavy
233–237.
metals concentration of the soils around Zlatna and Copşa

Please cite this article in press as: Manu, M., et al., Impact assessment of heavy metal pollution on soil mite communities (Acari: Mesostigmata)
from Zlatna Depression – Transylvania. Process Safety and Environmental Protection (2016), http://dx.doi.org/10.1016/j.psep.2016.06.011
PSEP-799; No. of Pages 14
ARTICLE IN PRESS
Process Safety and Environmental Protection x x x ( 2 0 1 6 ) xxx–xxx
Kaczmarek, S., Marquardt, T., Faleńczyk-Koziróg, K., Marcysiak,
K., 2012. Diversity of soil mite communities (Acari) within
habitats seasonally flooded by the Vistula river (Ostromecko,
Poland). Biol. Lett. 49 (2), 97–105.
Kardol, P., Reynolds, W.N., Norby, N.J., Classen, A.T., 2011. Climate
change effects on soil microarthropod abundance and
community structure. Appl. Soil Ecol. 47, 37–44.
Karg, W., 1993. Acari (Acarina), Milben Parasitiformes
(Anactinochaeta). Cohors Gamasina Leach (Acari (Acarina)
supraorder Parasitiformes (Anactinochaeta) Cohors Gamasina
Leach – predatory mites). Die Tierwelt Deutsch. 59, 1–513.
Keri, A.A., Avram, S., Rusu, T., 2010. Aspecte privind modificarea
geomorfologică a terenului aferent exploatării miniere Larga
de Sus, perimetrul minier Zlatna, judeţul Alba.
ProEnvironment 3, 498–501.
Klarner, B., Maraun, M., Scheu, S., 2013. Trophic diversity and
niche partitioning in a species rich predator guild – natural
variations in stable isotope ratios (13C/12C, 15N/14N) of
mesostigmatid mites (Acari, Mesostigmata) from Central
European beech forests. Soil Biol. Biochem. 57, 327–333.
Koehler, H.H., 1999. Predatory mites (Gamasina, Mesostigmata).
Agric. Ecosyst. Environ. 74, 395–410.
Lavelle, P., Decaëns, T., Aubert, M., Barot, S., Blouin, M., Bureau, F.,
argerie, P., Mora, P., Rossi, P., 2006. Soil invertebrates and
ecosystem services. Eur. J. Soil Biol. 42, S3–S15.
Lăcătuşu, R., Dumitru, M., Râşnoveanu, I., Ciobanu, C., Lungu, M.,
Cârstea, S., Kovacsovics, B., Baciu, C., 2001. Soil pollution by
acid rains and heavy metals in Zlatna region, Romania. In:
Stott, D.E., Mohtar, R.H., Steinhardt, G.C. (Eds.), Sustaining the
Global Farm. Selected papers from the 10th International Soil
Conservation Organization Meeting held May 24–29, 1999 at
Purdue University and the USDA-ARS National Soil Erosion
Research Laboratory. , pp. 817–820.
Lăcătuşu, R., 2006. Agrochimie, Terra Nostra, Iaşi.
Legendre, P., Legendre, L., 1998. Numerical Ecology, 2nd English
edn. Elsevier, Amsterdam.
Lindo, Z., Whiteley, J., Gonzalez, A., 2012. Traits explain
community disassembly and trophic contraction following
experimental environmental change. Glob. Change Biol. 18,
2448–2457.
Malmstrom, A., 2008. Temperature tolerance in soil
microarthropods: simulation of forest-fire heating in the
laboratory. Pedobiologia 51, 419–426.
Manu, M., Honciuc, V., 2010. Rang correlations at the level of the
predator and the decomposer populations soil mites (Acari:
Mesostigmata-Gamasina; Oribatida) from central parks of
Bucharest city, Romania. Acta Entomol. Serbica 5, 129–140.
Manu, M., 2011. The influence of some environmental factors on
the species diversity of the predator mites (Acari: Gamasina)
from natural forest ecosystems in Bucegi massif. Trav. Mus.
d’Hist. Nat. “Grigore Antipa” 54, 9–20.
Manu, M., Ion, S., 2014. Characteristic soil mite’s communities
(Acari: Gamasina) for some natural forests from Bucegi
Natural Park – Romania. Period. Biol. 116, 93–101.
Manu, M., Iordache, V., Băncilă, R.I., Bodescu, F., Onete, M., 2015.
The influence of the environment variables on soil mite
communities (Acari: Mesostigmata) from overgrazed
grassland ecosystems – Romania. Ital. J. Zool. 83 (2), 89–97.
Masan, P., 2003a. Macrochelid mites of Slovakia (Acari,
Mesostigmata, Macrochelidae). Institute of Zoology, Slovak
Academy of Science, Bratislava.
Masan, P., 2003b. Identification key to Central European species of
Trachytes (Acari: Uropodina) with redescription, ecology and
distribution of Slovak species. Eur. J. Entomol. 100, 435–448.
Masan, P., Fenda, P., 2004. Zerconid mites of Slovakia (Acari,
Mesostigmata, Zerconidae). Institute of Zoology, Slovakia
Academy of Science, Bratislava.
Masan, P., 2007. A review of the family Pachylaelapidae in
Slovakia with systematics and ecology of European species
(Acari: Mesostigmata: Eviphidoidea). Institute of Zoology,
Slovak Academy of Science, Bratislava.
Masan, P., Fenda, P., Mihal, I., 2008. New edaphic mites of the
genus Veigaia from Slovakia and Bulgaria, with a key to the
Please cite this article in press as: Manu, M., et al., Impact assessment of heavy metal pollution on soil mite communities (Acari: Mesostigmata)
from Zlatna Depression – Transylvania. Process Safety and Environmental Protection (2016), http://dx.doi.org/10.1016/j.psep.2016.06.011
13
European species (Acari, Mesostigmata, Veigaiidae). Zootaxa
1897, 1–19.
Mášan, P., Halliday, B., 2010. Review of the European genera of
Eviphididae (Acari: Mesostigmata) and the species occurring
in Slovakia. Zootaxa 2585, 1–122.
M.O. 756/03.11.1997. Romanian Waters, Forests and
Environmental Protection No. 756 from 3 November 1997
concerning the arrangement approval of the environmental
pollution assessment.
Mico, C., Recatala, L., Peris, M., Sanchez, J., 2006. Assessing heavy
metal sources in agricultural soils of an European
Mediterranean area by multivariate analysis. Chemosphere
65, 863–872.
Napierała, A., Błoszyk, J., 2013. Unstable microhabitats
(merocenoses) as specific habitats of Uropodina mites (Acari:
Mesostigmata). Exp. Appl. Acarol. 60, 163–180.
Napierala, A., Labijak, B., Skwierczynski, F., Konwerski, S.,
Bloszyk, J., 2015. Influence of habitat type and natural
disturbances on uropodine mite communities (Acari:
Mesostigmata: Uropodina) in oak-hornbeam forests in Central
Europe. Int. J. Acarol. 41 (1), 41–52.
Niedbala, W., Bloszyk, J., Kaliszewski, M., Kazmierski, A.,
Olszanowski, Z., 1990. Structure of soil mite (Acari)
communities in urban green of Warsaw. Fragm. Faun. 33,
21–44.
Oksanen, J., Kindt, R., Legendre, P., O’Hara, R.B., 2006. Vegan:
community ecology package version 1.8-2,
http://cran.r-project.org/.
Quinn, G.P., Keough, M.J., 2002. Experimental Design and Data
Analysis for Biologists. Cambridge University Press,
Cambridge, UK.
Pinheiro, J.C., Bates, D.M., 2000. Mixed-Effects Models in S and
S-PLUS. Springer.
R Development Core Team, 2006. http://www.r-project.org.
Rantalainen, M.L., Torkkeli, M., Strommer, R., Setala, H., 2006.
Lead contamination of an old shooting range affecting the
local ecosystem — a case study with a holistic approach. Sci.
Total Environ. 369, 99–108.
Ruf, A., 1998. A maturity index for predatory soil mites
(Mesostigmata: Gamasina) as an indicator of environmental
impacts of pollution on forest soils. Appl. Soil. Ecol. 9,
447–452.
Ruf, A., Beck, L., 2005. The use of predatory soil mites in
ecological soil classification and assessment concepts, with
perspectives for oribatid mites. Ecotoxicol. Environ. Saf. 62,
290–299.
Ruf, A., Bedano, J.C., 2010. Sensitivity of different taxonomic
levels of soil Gamasina to land use and anthropogenic
disturbance. Agric. For. Entomol. 12, 203–212.
Salmane, I., 2001. Investigations of Gamasina mites (Acari,
Mesostigmata) in natural and man-affected soils in Latvia. In:
Reemer, M., Helsdingen, P.J., Kleukers, R.M.J.C. (Eds.),
Proceedings of the 13th International Colloquium of the
European Invertebrate Survey. September 2–5, Leiden, The
Netherlands. European Invertebrate Survey, The Netherlands,
Leiden, pp. 129–137.
Salmane, I., Brumelis, G., 2010. Species list and habitat preference
of Mesostigmata mites (Acari, Parasitiformes) in Latvia.
Acarologia 50 (3), 373–394.
Santamaría, J.M., Moraza, M.L., Elustondo, D., Baquero, E.,
Jordana, R., Lasheras, E., Bermejo, R., Arino, A.H., 2012.
Diversity of Acari and Collembola along a pollution gradient
in soils of a Pyrenean forest ecosystem. Environ. Eng. Manage
J. 11, 1159–1169.
Seniczak, S., Dabrowski, J., Dlugosz, J., 1995. Effect of copper
smelting air pollution on the mites (Acari) associated with
young scots pine forests polluted by a copper smelting works
at Giogow, Poland. I. Arboreal Mites. Water Air Soil Pollut. 94,
71–84.
Slomian, S., Gulvik, M.E., Madej, G., Austad, I., 2005. Gamasina
and Microgyniina (Acari, Gamasida) from soil and tree
hollows at two traditional farms in Sognog Fjordane, Norway.
Norw. J. Entomol. 52, 39–48.
PSEP-799; No. of Pages 14
ARTICLE IN PRESS
14 Process Safety and Environmental Protection x x x ( 2 0 1 6 ) xxx–xxx

Skorupski, M., Belter, W., Kamczyc, J., Wierzbicka, A., 2008. Soil
mites (Acari, Mesostigmata) of the ‘Torfowiska Doliny Izery’
Reserve in the Sudety Mountains. Soil Organ. 80 (2), 261–270.
Skorupski, M., Horodecki, P., Jagodziński, A.M., 2013. Roztocze z
˛
rzedu Mesostigmata (Arachnida, Acari) na terenach
przemysłowych i poprzemysłowych w Polsce (Mite species of
Mesostigmata order (Arachnida, Acari) in industrial and
postindustrial areas of Poland). Nauka Przyr. Technol. 7, 1–11.
Skubala, P., Kafel, A., 2004. Oribatid mite communities and metal
bioaccumulation in oribatid species (Acari, Oribatida) along
the heavy metal gradient in forest ecosystems. Environ.
Pollut. 132 (1), 51–60.
Skubala, P., Zaleski, T., 2012. Heavy metal sensitivity and
bioconcentration in oribatid mites (Acari, Oribatida): gradient
study in meadow ecosystems. Sci. Total Environ. 414 (1),
364–372.
Van Gestel, C.A.M., 2012. Soil ecotoxicology: state of the art and
future directions. ZooKeys 176, 275–296.
Van Straalen, N.M., 1998. Evaluation of bioindicator systems
derived from soil arthropod communities. App. Soil Ecol. 9
(1–3), 429–437.
Van Straalen, N.M., 2004. The use of soil invertebrates in
ecological survey of contaminated soils. In: Doelman, P.,
Eijsackers, H.J.P. (Eds.), Vital Soil Function, Value and
Properties. Elsevier, pp. 159–194.
Walter, D.E., Proctor, H.C., 2013. Mites: Ecology, Evolution and
Behaviour. Life at a Microscale, second ed. Springer-Verlag.
Wei, B., Yang, L., 2010. A review of heavy metal contaminations in
urban soils, urban road dusts and agricultural soils from
China. Microchem. J. 94, 99–107.
Weindorf, D.C., Paulette, L., Man, T., 2013. In-situ assessment of
metal contamination via portable X-ray fluorescence
spectroscopy: Zlatna, Romania. Environ. Pollut. 182, 92–100.
Wissuwa, J., Salamon, J.A., Frank, T., 2012. Effects of habitat age
and plant species on predatory mites (Acari, Mesostigmata) in
grassy arable fallows in Eastern Austria. Soil Biol. Biochem. 50,
96–107.
Xu, G.L., Kuster, T.M., Günthardt-Goerg, M.S., Dobbertin, M., Li,
M.H., 2012. Seasonal exposure to drought and air warming
affects soil Collembola and mites. PLOS ONE 7 (8), e43102,
http://dx.doi.org/10.1371/journal.pone.0043102.

Please cite this article in press as: Manu, M., et al., Impact assessment of heavy metal pollution on soil mite communities (Acari: Mesostigmata)
from Zlatna Depression – Transylvania. Process Safety and Environmental Protection (2016), http://dx.doi.org/10.1016/j.psep.2016.06.011