Artigo Folsomia Toxicidade

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APSOIL-1892; No. of Pages 11
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Applied Soil Ecology xxx (2013) xxxxxx
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Applied Soil Ecology

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Collembolan response to red mud pollution in Western Hungary

Daniel Winkler
Institute of Wildlife Management and Vertebrate Biology, University of West Hungary, Bajcsy-Zs. str. 4., 9400 Sopron, Hungary
a r t i c l e
i n f o
Article history:
Received 7 February 2013
Received in revised form 24 June 2013
Accepted 8 July 2013
Keywords:
Collembola communities
Red sludge
Soil pollution
Sodium alkalinity
Heavy metals
Bioavailability
a b s t r a c t
Effects of red mud pollution on the community structure of Collembola were studied in soils from open
grassland and forest habitats following the red mud disaster in Western Hungary. Nearby unpolluted
control plots of each habitat types were selected for comparative purposes. Analyses revealed that soil
became strongly alkaline and, even nine months after the disaster, pH exceeded a value of 9.0 in the
polluted forests. Water soluble Na content found to be 50160 times greater in the polluted area, and
total content of metals (e.g. Fe, Al, Mn, Zn, As, Cr, Cu, Ni, Pb, Zn) also increased considerably. Nevertheless,
owing to the high alkalinity and red muds adsorption capacity, bioavailable forms of heavy metals were
lower in comparison to the acid control soils. Collembola species richness was about the same in the
polluted and control forests (31 and 32, respectively), but lower in the polluted meadows compared to
the control plots (21 and 27, respectively). Total community abundance changed differently in the open
habitat and in the forest. Its value dropped by 45% in the polluted meadows, while almost tripled in
the polluted forests. Changes in the abundance of individual species involved both decrease/elimination
of sensitive species (e.g. Isotomiella minor, Sminthurinus aureus) and displacement of species tolerant
to pollution (e.g. Micranurida pygmaea) into higher abundance classes. Certain species (e.g. Folsomia
manolachei, Sphaeridia pumilis), following the pollution, showed a reverse pattern of abundance in the
two habitat types; increasing in the forest while decreasing in the meadow. This study has suggested
that soil alkalinity and salt (Na) toxicity were presumably the two most important factors determining
the structure of Collembola communities in the area affected by red mud pollution. Despite the high
toxicity risk associated with this accident, no adverse effect has been observed in Collembola abundance.
Nevertheless, as a consequence of soil re-acidication, re-mobilisation of xed metals may occur in the
long term, constituting to a potential risk to soil Collembola.
2013 Elsevier B.V. All rights reserved.
1. Introduction
Legacy of the 20th century has left us with two signicant ecological questions for the new century:
How can we validate an ecologically conscientious view in economical decision making?
How can we put a stop to the dramatic decline of biodiversity?
The strong interconnection between these two questions has
enforced the need for rapid action especially in light of detrimental
industrial disasters. Unfortunately, large scale industrial disasters
continue to occur even in the 21st century. The most well known
international incident of the new era is the Japanese Fukushima
disaster; however, there have also been local incidents, where the
affects were localised, but their ecological impact could not be
neglected. One such localised disaster occurred in 2010 in Hungary
Tel.: +36 70 3170807; fax: +36 99 518350.

E-mail address: dwinkler@emk.nyme.hu
which became known as the red mud incident in international

news. The nature of this disaster spillage of red mud from a reservoir has directed focus onto soil conservation and protection of
soil biodiversity. One major reason for the increased interest in soil
biodiversity was related to the fact that from very early on it became
apparent that the red mud contaminated soil can only be utilised
and inhabited after complete soil removal. This point of view considered the benets to Homo sapiens alone. But what happens to the
soil biodiversity in those areas where the contaminated soil cannot
be removedfor example: in forested areas? The answer will probably be found in soil fauna recolonisation which will most likely
originate from surrounding habitats where contamination did not
reach and from so called survival spots. However, how soon this
can happen and how will all this take place nobody can predict for
as long as this sadly unique in situ experimentation does not stop.
On October 2010, in Western Hungary, one of the dykes of a
red mud reservoir of an aluminium processing factory breached
and more than 1.3 million m3 of toxic sludge broke free, ooding the surrounding area (Szpvlgyi, 2011). This event destroyed
nearly 1000 hectares of land, including nearby rivers, where practically all aquatic life was destroyed (Mayes et al., 2011); forests and
0929-1393/$ see front matter 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.apsoil.2013.07.006
Please cite this article in press as: Winkler, D., Collembolan response to red mud pollution in Western Hungary. Appl. Soil Ecol. (2013),
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agricultural elds, where the soil surface was covered with an average 510 cm thick red mud layer after the ood (Anton et al., 2012).
This red mud disaster turned out to be one of the most severe
ecological disasters ever experienced in the country (Burai et al.,
2011), leaving behind long-term environmental impacts which are
impossible to assess at the present time.
The red mud is a ne fraction by-product of the so-called Bayer
alumina process which uses sodium hydroxide for recovering substantially pure alumina from bauxite (Liu et al., 2007; Power et al.,
2011). Red mud is therefore strongly alkaline with a pH of 912.5
(Milacic et al., 2012). Its main components typically include residual minerals and oxides, such as hematite, goethite, boehmite,
quartz, sodium aluminosilicates, titanium dioxide, calcium carbonate/aluminate and magnesium oxide (Mayes et al., 2011). Further
components in lower concentrations also include heavy metals
such as copper, zinc, chromium, cadmium, arsenic, mercury, lead,
nickel and vanadium; and a few rare-earth metal elements (Cablik,
2007).
To assess the environmental impact of the red mud disaster,
some investigations have already been carried out. Gelencsr et al.
(2011) focused on the potential health effects of red mud dust,
while other studies evaluated the impact of red sludge pollution
on water quality and aquatic life (Harka, 2011; Mayes et al., 2011;
Klebercz et al., 2012). Effects of red mud on plant growth and
plant composition have been extensively studied (Friesl et al., 2003;
Koulikourdis et al., 2005; Ruyters et al., 2011a); however, in regards
of soil fauna, no investigations have been carried out.
It is without doubt that red mud had considerable effect on soil
properties and soil biodiversity (Ruyters et al., 2011b; Anton et al.,
2012). The high sodium content and the extremely ne grain size
of the red mud can deteriorate soil structure (Ruyters et al., 2011a).
Further risks associated with red mud that affect soil properties are
related to alkalinity, heavy metal content and radioactive material

contamination (Klauber et al., 2011; Anton et al., 2012). High pH
itself can be a source of direct toxicity to soil organisms (Mertens,
1975; Hutson, 1978), as well as, heavy metal pollution also tends
to affect, often adversely, soil animal communities (Hodson, 2013).
Effects of individual pollutants on soil Collembola have been widely
studied (e.g. Hgvar and Abrahamsen, 1990; Hopkin, 1994; Gillet
and Ponge, 2003; Lock et al., 2003; Smit and van Gestel, 1996);
however, studies examining the toxic affect of complex mixtures
of pollutants, such as sludges, on these organisms are less widely
documented (Cole et al., 2001; Domene et al., 2008, 2010; Natalda-luz et al., 2009).
The objectives of the present research were to (i) determine
whether there are signs of revitalisation and recolonisation by
Collembola of the selected red mud polluted area not affected
by remediation; (ii) evaluate the changes in Collembola community species composition and abundance in polluted compared to
unpolluted plots selected as control from nearby locations; and (iii)
collect new information on pH tolerance of Collembola species in
eld. The study was conducted 9 months after the red mud disaster.
2. Materials and methods
2.1. Study area
The study was conducted in the area of the Torna stream valley, which was the main area affected by the toxic red mud ood.
The site is located near the village of Tskevr (Fig. 1); it is characterised by a variety of semi-natural and agricultural habitats such
as forests, grasslands and arable lands. Sampling was carried out in
both forest and open meadow habitats. Of each habitat type, three
polluted and three unpolluted plots were selected for sampling and
Fig. 1. Study area, location of sampling plots.
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comparative analyses. Mean plot size was 3.38 ha (SE 0.22, n = 15).
The polluted plots were situated in the formerly ooded area, next
to the Torna stream, while nearby unpolluted control plots were
located at slightly higher elevations which were unaffected by the
ood. Plant species composition and vegetation structure characteristic were taken into account in selecting control sampling plots,
so as to make the most accurate comparisons possible. The sampled forests were characterised by a tree layer composed of Quercus
robur, Fraxinus excelsior and scattered trees of Carpinus betulus and
Ulmus laevis. The sampled grasslands were tall herb communities
with dominance of Arrhenatherum elatius, Deschampsia caespitosa
and Dactylis glomerata.
2.2. Soil chemistry
Simultaneously with the Collembola sampling, in August of 2011,
ve soil core samples were collected (after litter removal) at each
of the polluted and unpolluted plots in order to determine the soil
properties and the degree of heavy metal pollution.
Soil pH was determined potentiometrically in H2 O and 1 M KCl
using a soil-to-solution ratio of 1:5. Percentage quantity of the
soil organic matter (Som) content was evaluated using the potassium dichromate oxidation method. Soil hygroscopicity (hy ) was
determined by using Kurons method (Stefanovits, 1992). Water
soluble content of Na was measured following shaking method.
Arsenic content was quantied in the aqua regia solution. Total content of heavy metals was measured with ame atomic absorption
spectrometer (AAS) in hydrochloric solution resulted by digestion of soil samples in HClO4 HNO3 mixture. Bioavailable forms
of selected heavy metals were determined using extraction with
0.1 M Na2 EDTA.
2.3. Sampling and extraction of Collembola
From each of the selected plots, ve soil cores of 100 cm3
volume
(3.6 cm in diameter and 10.0 cm in depth) were sampled randomly;
at least 10 m from the edges to ensure that edge effects do not bias
the results. Springtails were extracted from the total of 60 soil samples within 14 days using a modied Tullgren apparatus. Specimens
were identied at species level following principally taxonomical keys by Deharveng (1982), Fjellberg (1980, 1998), Babenko
et al. (1994), Zimdars and Dunger (1994), Weiner (1996), Jordana
et al. (1997), Pomorski (1998), Bretfeld (1999), Potapov (2001) and
Thibaud et al. (2004). Taxonomic classication is primarily based on
the most recent classication by Janssens and Christiansen (2011).
2.4. Data analyses
In the analysis of the collembolan community structure, species
abundance distributions were compared with three corresponding theoretical distributions: geometric (Motomura, 1932), broken
stick (MacArthur, 1957) and logarithmic series (Fisher et al., 1943).
For comparison of observed rank abundance curves and expected
theoretical curves Chi-square tests were performed.
In addition to the observed species richness nonparametric
richness estimators (abundance-based estimators Chao1 and ACE
and incidence-based estimators Chao2 and ICE) were evaluated
using v2.1 of the Species Richness Estimators Eco-Tool (Russell,
2011), which implements the techniques described in Colwell and
Coddington (1994) as well as those of Colwell et al. (2004). Singletons and doubletons (number of species represented by one or two
individuals) were also veried.
Three measures of species diversity were calculated for quantitative evaluation of collembolan species diversity in the polluted
and control areas: the ShannonWeavers index (Shannon and
Weaver, 1949), the Simpson index (Simpson, 1949) and Pielous
(1966) evenness index. The Shannon indices were compared

according to the modied t-test proposed by Hutcheson (1970).
Rnyi diversity proles (Tthmrsz, 1997) were used for partial
ranking of the Collembola communities based on diversity. A community of higher diversity has a prole consistently above the
prole of a less diverse community. In case the diversity proles
cross each other, the communities are not comparable, and thus
the diversity comparison carried out by using t-test gets overruled.
Dominance was measured using the community dominance
index (McNaughton, 1968) calculated as the percentage of abundance that is contributed by the two most abundant species
within the community. To evaluate the similarities of species composition, Jaccards similarity coefcient (Jaccard, 1901) and the
MorositaHorn index were used (Magurran, 1988).
Effect of selected environmental variables on collembolan
community composition was evaluated by canonical correspondence analysis (CCA) performed with the software Past ver. 2.17b
(Hammer et al., 2001). In the nal analysis only those variables were
included (Som, hy , pH, Na content), which equalled to the measured Collembola sample size (n = 15 per habitat). Species found in
less than 5 samples and those represented by less than 10 individuals were excluded from the analysis (33 from total 59 species) due
to uncertain relationship with environmental factors. Unrestricted
Monte Carlo permutation tests, with 1000 randomisations, were
carried out for the total inertia of the CCA, thus, providing an overall test on the effect of the constraining parameters used in the
analysis (ter Braak, 1986).
3. Results
3.1. Chemical analysis of soil
The control forest and meadow in this study presented strong
acid to moderately acid alluvial soils, with average pH (in H2 O)
values of 5.2 and 5.8, respectively (Table 1). Soil became alkaline
after the red sludge ooding and, even nine months after the disaster, pH reached an average of 9.20 (very strongly alkaline) in the
red mud polluted forest and 8.20 (strongly alkaline) in the polluted
open grassland. Hygroscopic moisture content (hy ), which also represents soil texture, was higher in the polluted habitats. Na content
found to be almost 50 greater in the polluted forest compared to
the control, and this ratio was even higher (160) in relation to
the meadows. Total content of Fe and Al, which represent major
red mud components, was remarkably higher in the polluted soil
samples. As, Cr and Ni concentrations were found to be considerably high in the polluted sites, however; these did not exceed the
threshold concentrations dened by Hungarian legislation for toxic
trace metals in soil (MSZ-21470-50, 1998). Concentrations of other
heavy metals such as Zn, Pb and Cd, although increased after the red
mud pollution, did not show extreme levels. Bioavailable content
of heavy metals as extracted by EDTA showed an opposite pattern:
Fe, Mn was orders of magnitude lower in the polluted soils where
also Cu and Zn were found in lower concentrations in comparison
to the control samples.
3.2. Collembola species richness, diversity and abundance
A total of 4339 specimens representing 15 families, 35 genera and 59 species of Collembola were collected and identied
(Table 2). A particular species of the genus Lepidocyrtus, namely
Lepidocyrtus tomosvaryi, was also found and proved to be new to
science (Winkler and Traser, 2012). Structural characteristics of
the communities are presented in Table 3. The highest observed
species richness was identied from the control forest (32) followed by the red mud polluted forest (31), while the open grassland
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Table 1
Soil parameters (mean SE) in the polluted and control habitats.
Forest
Meadow
Polluted
pH H2 O*
pH KCl*
Som (%)*
hy *
Na (mg/kg)a , *
As (mg/kg)b
Total Ca (mg/kg)
Total Al (mg/kg)
Total Fe (mg/kg)
Total K (mg/kg)
Total Mn (mg/kg)
Total Cd (mg/kg)
Total Cr (mg/kg)
Total Cu (mg/kg)
Total Ni (mg/kg)
Total Pb (mg/kg)
Total Zn (mg/kg)
EDTA Fe (mg/kg)
EDTA Mn (mg/kg)
EDTA Cu (mg/kg)
EDTA Zn (mg/kg)
9.2
8.1
12.3
2.8
883
9.8
854
17,658
67,356
1173
1264
0.57
57.8
14.3
38.6
41.3
84.3
60
8.4
2.37
1.60
Control
0.09
0.11
0.25
0.16
34.9
0.39
59
833
2599
65
171
0.09
7.94
1.48
2.04
5.98
8.0
10.3
1.9
0.39
0.49
5.2
4.6
11.1
2.2
18.5
4.1
1764
6894
11,432
994
328
0.32
14.1
6.9
11.6
17.2
44.3
587
694
3.54
9.07
Polluted
0.15
0.12
0.21
0.08
0.71
0.08
87
353
766
58
80
0.04
1.75
1.30
1.79
1.45
6.7
130
137
0.79
1.39
8.8
7.6
8.7
1.8
543
8.7
1214
19,473
64,023
1372
1422
0.49
54.4
12.3
37.4
44.2
79.3
40
43.6
1.85
1.98
Control
0.12
0.15
0.17
0.16
14.9
0.27
41
1067
3257
116
106
0.08
7.00
0.88
1.83
3.98
10.5
4.2
13.0
0.41
0.48
5.8
5.1
8.8
1.51
3.4
4.4
1371
7470
10,514
1018
247
0.24
15.2
7.8
11.2
12.9
41.4
237
241
2.83
5.46
0.12
0.10
0.14
0.09
0.30
0.15
52
334
492
78
38
0.04
1.44
0.87
1.13
1.12
4.4
78.9
67.8
0.35
1.19
Som: Soil organic matter; hy : hygroscopicity; n = 3 (consisting of ve pooled samples) with the exception of *n = 15.
a
Water soluble.
b
Aqua regia solution.
habitats (control and polluted) had lower number of species; 28

and 21, respectively. Similarly, estimated species richness was the
highest in the control forest spanning from 39 (incidence-based
ICE) to 41 (abundance-based Chao1) compared to the 32 actually collected. Chao1 estimator also gave the highest estimate of
species richness in the polluted meadow, while maximum species
richness was predicted by ICE in the polluted forest and control
meadow. The Shannon and Simpson diversity indices and species
evenness indicated the highest collembolan diversity in the control
meadow. According to the t-test proposed by Hutcheson (1970),
Shannon diversity was signicantly lower in both polluted habitat
types (p < 0.001), which is reected also in Rnyis diversity proles
(Fig. 2).
Collembola abundance was the highest in the polluted forest, exceeding 90,000 ind./m2 , while abundance was signicantly
Fig. 2. Comparison of Collembola diversities in red mud polluted and control habitats
using Rnyis diversity proles.
lower (t-test, P < 0.01), only about one third in the control forest. The open meadows were less abundant (ranging from 8367
to 14,900 ind./m2 ) and the order of abundance was just the opposite but with no signicant difference observed between the
polluted and control area. Changes in the abundance of species
under the inuence of red mud soil contamination involved both
decrease/elimination of sensitive species (e.g. Isotomiella minor, L.
tomosvaryi, Pseudosinella cf. bohemica, Sminthurinus aureus) and
displacement of species tolerant to pollution (e.g. Micranurida pygmaea, Brachystomella parvula, Folsomia candida, Orchesella spp.) into
higher abundance classes (Fig. 3). Certain species (e.g. Folsomia
manolachei, Folsomia quadrioculata, Parisotoma notabilis, Sphaeridia
pumilis) showed an opposite abundance pattern in the two habitat types: increasing in the forest while decreasing in the open
grassland.
The analysis of species abundance distribution (Fig. 4) showed a
slight difference between the forest and open communities. Moreover, very similar abundance distribution patterns were observed
for the polluted-control communities paired according to habitat
types. While in the studied forests the geometric series was the best
model tted (polluted-chi2 = 3435, P < 0.001; control-chi2 = 801;
P < 0.001), MacArthurs broken stick model was found to explain
adequately the observed distributions in the meadow communities (polluted-chi2 = 74.7, P < 0.01; control-chi2 = 107.4, P < 0.001).
Community dominance index (CDI) was the highest in the polluted
forest: 65.27% of the total abundance was represented by F. quadrioculata (33.58%) and F. manolachei (31.69%). The same two species
were also the most dominant ones in the control forest accounting for 56.11% of the total abundance. The relatively low values of
CDI in the meadow habitats (30.6538.64%) indicated that none
of the species occurred in extreme abundance. The most dominant species were S. pumilis (15.66%) in the control meadow and
Hypogastrura vernalis (19.92%) in the polluted meadow.
Based on Jaccard similarity index of paired control-polluted
habitats (Table 4), forest communities showed higher similarity
(0.47), with 20 species common to both the contaminated and control samples, while lower similarity (0.36) was observed between
the paired meadow samples (13 common species). These results
are conrmed by the MorisitaHorn index of similarity which also
takes account collembolan abundance.
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Table 2
Species of Collembola and their abundance (number of individuals/m2 ) in the red mud polluted and unaffected control habitats. Data are means followed by standard errors.
Signicant differences between the paired polluted and control habitats (P < 0.05) are indicated in italicised letters.
Forest
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
Neanuridae
Frisea truncata Cassagnau, 1958
Deutonura conjuncta (Stach, 1926)
Neanura muscorum (Templeton, 1835)
Micranurida pygmaea Brner, 1901
Pseudachorutes parvulus Brner, 1901
Pseudachorutes pratensis Rusek, 1973
Brachystomellidae
Brachystomella parvula (Schffer, 1896)
Hypogastruridae
Ceratophysella luteospina (Stach, 1920)
Ceratophysella succinea (Gisin, 1949)
Hypogastrura vernalis (Carl, 1901)
Xenylla corticalis Brner, 1901
Onichiuridae
Protaphorura armata (Tullberg, 1869)
Protaphorura campata (Gisin, 1952)
Protaphorura gisini (Haybach, 1960)
Tullbergidae
Mesaphorura critica Ellis, 1976
Mesaphorura hylophila Rusek, 1982
Mesaphorura krausbaueri Brner, 1901
Mesaphorura macrochaeta Rusek, 1976
Metaphorura riozoi Castano-Meneses,

Palacios Vargas and Traser, 2000
Stenaphorurella lubbocki (Bagnall, 1935)
Tomoceridae
Pogonognathellus avescens (Tullberg,
1871)
Isotomidae
Cryptopygus bipunctatus (Axelson, 1903)
Folsomia candida Willem, 1902
Folsomia manolachei Baggnall, 1939
Folsomia quadriocuculata (Tullberg, 1871)
Isotoma caerulea (Bourlet, 1839)
Isotoma viridis Bourlet 1839
Isotomiella minor (Schffer, 1896)
Isotomodes productus (Axelson, 1906)
Isotomodes sexsetosus da Gama, 1963
Parisotoma notabilis (Schffer, 1896)
Entomobryidae
Entomobrya dorsalis Uzel, 1891
Entomobrya handschini Stach, 1922
Entomobrya muscorum (Nicolet, 1842)
Lepidocyrtus cyaneus Tullberg, 1871
Lepidocyrtus cf. arrabonicus Traser, 2000
Lepidocyrtus tomosvaryi Winkler and
Traser, 2012
Lepidocyrtus paradoxus Uzel, 1890
Pseudosinella alba (Packard, 1873)
Pseudosinella cf. bohemica Rusek, 1979
Seira sp. Juv
Heteromurus major (Moniez, 1889)
Heteromurus nitidus (Templeton, 1835)
Orchesella albofasciata Stach, 1960
Orchesella cincta (Linnaeus, 1758)
Orchesella avescens (Bourlet, 1839)
Orchesella multifasciata (Stscherbakow,
1898)
Orchesella spectabilis Tullberg, 1871
Paronellidae
Cyphoderus sp. juv
Neelidae
Megalothorax minimus Willem, 1900
Sminthurididae
Sphaeridia pumilis (Krausbauer, 1898)
Katiannidae
Sminthurinus aureus (Lubbock, 1862)
Sminthurinus elegans (Fitch, 1863)
Arrhopalitidae
Arrhopalites caecus Tullberg, 1871
Sminthuridae
Meadow
Polluted (n = 15)
Control (n = 15)
Polluted (n = 15)
Control (n = 15)
67 45
67 45
33 33
933 425
33 33
0
33 33
33 33
133 77
33 33
100 53
0
0
0
0
33 33
0
33 33
0
100 72
0
0
0
33 33
1167 585
1467 559
33 33
233 108
33 33
133 133
33 33
0
0
0
0
0
0
1667 822
0
0
0
1533 1276
0
0
0
0
33 33
267 267
0
367 260
0
1567 371
1033 269
0
900 214
0
0
0
0
0
0
33 33
0
467 204
0
133 77
0
0
133 77
0
300 118
0
100 72
1633 572
67 45
67 67
33 33
267 267
5233 3263
28,533 6256
30,233 6761
0
0
0
0
0
7667 1867
4100 1268
67 45
7433 1405
10,167 2331
0
0
600 208
0
0
500 176
733 381
33 33
267 128
233 145
0
0
0
0
0
367 192
2233 1154
0
0
100 53
1667 490
0
167 105
33 33
0
33 33
400 298
0
1267 338
0
567 381
0
0
0
0
0
267 128
0
433 182
67 67
33 33
67 45
100 72
0
0
200 118
1033 226
0
100 72
867 424
1800 951
0
0
833 270
33 33
0
267 83
0
0
233 128
667 446
0
0
0
0
0
0
233 200
0
33 33
0
100 53
0
0
0
0
33 33
0
0
0
67 67
1533 1498
300 266
33 33
67 45
6800 2005
2033 517
267 168
2333 1394
0
467 251
267 145
167 80
0
0
433 217
233 128
333 116
1000 229
1033 303
267 145
33 33
0
67 67
33 33
500 183
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ARTICLE IN PRESS
6
Table 2 (Continued )
Forest
55.
56.
57.
58.
59.
Meadow
Polluted (n = 15)
Control (n = 15)
Polluted (n = 15)
Control (n = 15)
Allacma fusca (Linnaeus, 1758)

Spatulosminthurus aviceps (Tullberg,
1871)
Lipothrix italica (Cassagnau, 1968)
Bourletiellidae
Fasciosminthurus strigatus (Stach, 1922)
Fasciosminthurus virgulatus (Skorikow,
1899)
0
0
167 135
500 276
0
0
0
0
67 45
100 72
0
0
0
0
67 45
100 53
0
0
Total
90,033 16,467
31,367 5062
8367 1284
14,900 3240
Table 3
Structural indices of Collembola communities in the studied polluted and control habitats.
Forest
S
Singletons/Doubletons
ACE
ICE
Chao1
Chao2
Number of presumed species
H
D
J
CDI
Meadow
Polluted
Control
Polluted
Control
31
4/5
34
35
32
33
14
1.899
0.769
0.553
65.27
32
8/2
40
39
41
40
79
2.186
0.813
0.631
56.11
21
6/1
27
26
29
25
48
2.385
0.874
0.783
38.64
28
6/4
34
36
31
35
38
2.659
0.908
0.798
30.65
S: total number of species; ACE, ICE, Chao1 and Chao2: nonparametric richness estimators; H : ShannonWeavers diversity index; D: Simpsons diversity index; J: Pielous
evenness index; CDI: community dominance index (%).
The CCA analysis reects a more detailed response of collembolan communities to environmental changes (Fig. 5). The
eigenvalue of axis 1, as well as the explained variance of both
axes were relatively high (axis 1: eigenvalue: 0.445, explained
variance: 63.84%; axis 2: eigenvalue: 0.193; explained variance:

27.69%). Monte Carlo permutation testing was used to test the
null hypothesis of no association between species and soil environmental factors, and rejected this hypothesis for both axis 1
Fig. 3. Changes in the abundance of Collembolan species after the red mud pollution.
ARTICLE IN PRESS
G Model
Table 4
Pairwise comparison of the polluted and control habitats using Jaccards similarity coefcient (normal letters) and the MorisitaHorn index (italicised letters).
Forest control
Forest control
Forest polluted
Meadow control
Meadow polluted
0.47
0.30
0.23
Forest polluted
Meadow control
Meadow polluted
0.92
0.51
0.38
0.20
0.16
0.57
0.31
0.24
Fig. 4. Species rank abundance of the red mud polluted and unaffected control
habitats.
and axis 2 (P < 0.01 and P < 0.05, respectively). The rst axis of this
data set represents mainly soil organic-matter content (Som) and
higroscopicity (hy ), whereas the second axis represents mainly the
chemical factors (soil pH, water soluble Na). Axis 1 clearly separated the forest and meadow habitats while axis 2 separated the
polluted and control plots.
Species typical for open grassland are those far from the origin
of the positive side of axis 1 (B. parvula, H. vernalis, Protaphorura
armata, Protaphorura gisini, Mesaphorura critica and Entomobrya
handschini), while species found exclusively or predominantly in
forests (e.g. P. cf. bohemica, Orchesella spectabilis, Arrhopalites caecus) were projected on the negative side of the same axis. As shown
by their position in Fig. 5, the most sensitive species to red mud
pollution and by this to remarkable pH change appeared to be I.
minor, P. cf. bohemica, L. tomosvaryi, S. aureus and Spatulosminthurus
aviceps, whereas other species like B. parvula, M. pygmaea, F. candida showed tolerance to the increased pH.
4. Discussion
4.1. Soil properties
The red mud disaster caused considerable changes in soil physical and chemical properties. As the increased soil hygroscopicity
indicates in the polluted area, red mud modied the particle size
structure, mostly by raising clay fraction. This has also been proved
by laboratory experiments, modelling the effects of red mud ood
(Anton et al., 2012). Because of the high content of sodium hydroxide in the sludge, the soil became strongly alkaline and total
concentration of several trace metals increased considerably. The
0.36
potential toxicity of heavy metals in soils depends on not only

their concentration but principally on their bioavailability, strongly
inuenced by various soil properties including pH, organic matter
and clay contents (Crommentuijn et al., 1997; Frische et al., 2002;
Van Gestel and Koolhaas, 2004; Van Gestel, 2008). Usually, with
increased clay content, bioavailability and toxicity of metals are
reduced (Van Gestel, 2008); while the opposite is true for salinity (Owojori, 2009). Although previous studies pointed out that for
certain soil organisms acute toxicity in soils polluted with sludges
was primarily related to water-soluble elements (Domene et al.,
2008, 2010); total concentrations of toxic heavy metals should not
be neglected either as pollutant uptake by specic groups of Collembola can also be more directly related to the solid phase of soil
(Vijver et al., 2001).
In acidic soil environments, the availability and mobility of
metal ions are higher due to the chemical form in which these ions
are present in soil solutions (Reddy et al., 1995; Takc et al., 2009;
Violante et al., 2010). From the obtained data, it is well reected in
the higher EDTA Fe, Mn and Zn content of the acid control soils compared to levels of the same elements in the red mud polluted soils.
It has to be noted, that red mud itself is a highly complex substance.
Despite its heavy metal content and thus its potential adverse
effects, red mud has shown some encouraging results as heavy
metal sorbent, decreasing the bioavailability of elements such as
As, Cd, Cu, Ni, Pb, Zn in polluted soils (Lombi et al., 2002; Bertocchi
et al., 2006; Garau et al., 2007, 2011). Owing to its hyper-alkalinity,
metals can be precipitated as hydroxides; and its high Al and Fe
content, in the form of oxides and hydroxides, can provide surfaces
for the adsorption of potentially toxic elements (Anton et al., 2012).
The results clearly revealed that the pH increase caused by the red
sludge ood was responsible for increasing of the residual fraction of heavy metals. Focusing on the pore-water hypothesis (Van
Gestel, 1997), at the time of the sampling, soil alkalinity and salt
(Na) toxicity were presumably the most important factors determining the structure of Collembola communities in the area affected
by red mud pollution.
Soil pollution can affect Collembola directly and indirectly. In
case of the red mud disaster, the ood of the highly alkaline slurry
can be considered as primary direct toxic effect. The high sodium
content can induce osmotic stress in haemolymph (Witteveen
et al., 1987) and can negatively affect collembolan reproduction
(Hutson, 1978; Domene et al., 2010). Further direct toxic effect is
linked with uptake of polluted food, as observed in the digestive
tract of several, mainly epigeic and hemiedaphic species collected
from the polluted area which clearly showed the presence of red
sludgehemorganic humus mixture.
Indirect effects of soil pollutions are mainly associated with
changes in food resources (Rusek and Marshall, 2000). Numbers
and diversity of microbial communities can decrease as a response
to pollution, which tends to precede changes in the collembolan
community composition by affecting groups that primarily feed on
soil fungi and bacteria (Cole et al., 2001). Although soil microbial
parameters were not investigated in this study, red mud does not
necessarily decrease bacterial populations; on the contrary, Garau
et al. (2007) found signicant increase in their number in red mud
amended soil experiments.
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Fig. 5. Ordination biplot of canonical correspondence analysis (CCA) with mean abundances of Collembola species and selected soil variables (Som: soil organic matter
content; hy : hygroscopicity; pH of H2 O; Na content) in the polluted and control area (FRM : red mud polluted forest; FC : control forest; MRM : red mud polluted meadow; MC :
control meadow). Collembola species name abbreviations consist of the initial letter of the genus name followed by the rst three letters of species.
4.2. Collembola diversity and abundance

Soil pollution by a wide range of contaminants can affect
Collembola species richness, diversity and total abundance, and
can determine the presence or absence and dominance of certain
species (e.g. Filser et al., 1995; Kuznetsova and Potapov, 1997; Cole
et al., 2001; Fountain and Hopkin, 2004a; Santamara et al., 2012).
Among the most important factors inuencing community structures, changes in food resources and in competition patterns merit
special mention (Hgvar, 1990; Rusek and Marshall, 2000; Gillet
and Ponge, 2003), along with the direct toxicity effects already
discussed.
As expected, the two surveyed habitat types (forest and grassland) have shown distinct differences in collembolan community
characteristics, and community responses to red mud pollution as
a result also showed differences. The contrast between Collembolan communities in forest and open habitats is well documented
(e.g. Pozo et al., 1986; Ponge, 1993; Setala et al., 1995; Ponge
et al., 2003, 2008; Winkler and Tth, 2012); however, the unfortunate red mud accident has raised the important question as to
how do these different communities change in a forest-grassland
habitat mosaic in response to the same pollution source. Higher
species richness (both observed and estimates) was associated
with the riverine forests versus meadows but after the pollution accident it decreased in both habitats, especially in the
meadows.
The Shannon and Simpson indices showed lower diversity
in the forests, although the intersections observed between the
community diversity proles (Fig. 2) of the sampled forests and

meadows indicated that open and forest areas contain very different collembolan communities that are not comparable solely
based on diversity (Tthmrsz, 1997). Decrease in diversity was
found in the polluted areas, both in forests and in meadows. Nevertheless, the diversity proles of communities from the paired
control-polluted habitats, especially concerning the forest sites, run
close to each other, suggesting no fundamental change in diversity. Nonetheless, other studies have revealed that there is not
necessarily an evident relationship between Collembolan diversity and soil pollution and thus species diversity indices should be
used with caution when evaluating toxicity (Van Straalen, 1997;
Cortet et al., 1999; Fountain and Hopkin, 2004a,b; Santorufo et al.,
2012).
Total community abundance changed differently in the open
habitat and in the forest. Its value dropped by 45% in the polluted
meadows (8000 ind./m2 ), while almost tripled in the polluted
forests reaching a value higher than 90,000 ind./m2 . The collected
data on community-level abundance in the polluted forests roughly
correspond to those obtained by Gillet and Ponge (2003) from
poplar forest sites heavily polluted by metals. The low species
richness and abundance in the polluted meadow sites might be
explained, among other factors, by the different, less complex
habitat structure, and in consequence, by the lower patchiness in
soil, which is essential for the survival of species in polluted sites
(Bengtsson, 1997; Filser et al., 2000; Niklasson et al., 2000)
By analysing the species abundance distribution, marked difference was observed only between the forest and meadow
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ARTICLE IN PRESS
communities, but no particular change occurred in abundance

distribution after the red mud pollution. Species abundance distribution was in agreement with the geometric series in both the
polluted and control forests, signifying high community dominance
and low evenness. This type of distribution, with a few dominants and the majority of species at relatively low numbers, often
reects soil degradation such as chemical or physical soil degradation (Hgvar, 1994; Fountain and Hopkin, 2004a). A light degree of
physical soil degradation, mainly caused by wild boar (Sus scrofa)
activities, was noticeable in the forest area, which could have had
an effect on community abundance structure prior to the red mud
disaster, as reected in the abundance structure of the control forest. Abundance distributions in the polluted and control meadows
exhibited a close t to MacArthurs broken stick model with evenly
high evenness in both communities and with no species showing
extreme dominance. Although there were species (e.g. B. parvula)
that could benet from the disappearance or abundance decrease of
other competitor species following the red mud pollution, limited
resources in soil or lack of free microhabitats prevented them from
becoming more abundant and eudominant.
Abundance or change in abundance of certain Collembola species
may reveal information about the pollution status of the soil (e.g.
Filser et al., 1995; Smit and van Gestel, 1996; Fountain and Hopkin,
2004a) as well as about soil acidity (Hgvar and Abrahamsen, 1980,
1984; Van Straalen and Verhoef, 1997; Van Straalen, 1998). There
are species that, based on the abundance data, were seemingly not
affected by the red mud pollution (H. vernalis, P. gisini) while others
(e.g. Allacma fusca, S. aureus, S. aviceps) were completely missing
from the polluted area. In certain cases, low abundance data was
insufcient to draw any safe conclusions about sensitivity of certain
species, while in other cases species were abundant and frequent
enough to evaluate the approximate effect of the red mud pollution
on these organisms.
Isotomid species F. manolachei and F. quadrioculata were most
abundant in the polluted forest plots; their number has tripled compared to the control. These two species are known to occur both in
acid and neutral soils (Ponge, 1993), and their ability to colonise or
recolonise polluted soils is a widely described phenomenon (Filser
and Hlscher, 1997; Filser et al., 2000; Chauvat and Ponge, 2002;
Gillet and Ponge, 2004). In the acid control forest soil, the species
P. notabilis; classied as alkalophilous by Hgvar and Abrahamsen
(1980) and Van Straalen and Verhoef (1997); occurred in low abundance but showed a more than tenfold increase in abundance in the
highly alkaline polluted forest soil. It should be noted that P. notabilis was found to be sensitive to heavy metals by several authors
(Tranvik et al., 1993; Bruus Pedersen et al., 1999; Gillet and Ponge,
2003), which conrms the hypothesis that heavy metals do not represent a serious risk for this group of species in red mud polluted
soils as of yet. These same three species were also present as subdominant species in the meadows, but conversely, their abundance
showed a slight decrease in the polluted plots of this open habitat,
which might be explained by the limited food resources in comparison to the forest soil with higher organic matter content. Generally,
it has been shown that the higher the organic matter contents of a
soil, the lower the toxicity of pollutants is to soil organisms, including those of the Collembola (Martikainen and Krogh, 1999; Bur et al.,
2010; Domene et al., 2010).
The sminthuridid species, S. pumilis was present in both habitat types where it was found at both, the polluted and control
plots as well. Similarly to P. notabilis, following the pollution, this
species also exhibited a reverse pattern of abundance in the open
(decreasing) and forest (increasing) habitats. In their study, Gillet
and Ponge (2003) revealed that S. pumilis can survive soil pollution by moving to deeper soil layers and thereby changing their
diet characteristics. As it was observed in the eld, the ood of red
sludge primarily affected the upper 510 cm of the soil layer. In
open areas, the effect of the ood was more severe compared to
the forests where the presence of a thick leaf litter cover moderated the impact of pollution, thereby most likely facilitating the
survival of S. pumilis. After the ood was over specimens from their
temporary endogeic microhabitat could seemingly quickly populate the empty niches in the forest, while survival in the meadow
soil proved to be less successful.
The case of B. parvula and Lepidocyrtus cyaneus merits particular attention. Both species are known as preferential inhabitants
of open environments (Pozo et al., 1986; Ponge, 1993; Auclerc
et al., 2009). B. parvula is reportedly able to colonise previously
disturbed open areas rapidly (Shaw, 1997) and it is also proved
to be well adapted to alkaline soils (Eitminaviciute et al., 2005;
Eitminaviciute, 2006). Its occurrence in relatively high abundance
in the red mud polluted meadow is therefore not surprising. More
interesting, however, is its presence in the polluted forest soil. L.
cyaneus was collected at both control habitats in roughly the same
abundance. While this species was completely absent from the polluted meadow soil, its abundance was found to be increased in
the polluted forest. Based on pH preference, L. cyaneus was classied as a weakly sub-neutral species, occurring also at pH 9 (Van
Straalen and Verhoef, 1997), which corresponds with the results
of CCA in this study. It was therefore expected that this species
would be able to survive in the polluted area. Nevertheless, Cole
et al. (2001) detected signicant abundance decrease of L. cyaneus in agricultural land upon application of sewage-sludge rich
in heavy-metals, which may also somewhat explain its absence
from the studied red mud polluted meadow. Gillet and Ponge
(2003) observed its presence in poplar stands, most probably as
a consequence of canopy opening caused by severe metal pollution. Red mud pollution had no such affect on tree canopies
and for that reason; light levels of the forest understorey were
unchanged. The abundance increase of L. cyaneus in the polluted
forest site may at least partly be explained by the lack of competitor species such as L. tomosvaryi or P. cf. bohemica. Since L.
cyaneus is a motile species, it could have theoretically moved
from the meadowforest edge ecotones towards the safer forest
environment.
In this study, abundance increase of some surface dwelling
Entomobrids (Orchesella avescens, Orchesella multifasciata, O.
spectabilis) in the polluted forest might conrm their resistance
to ooding (Hopkin, 1997). Certain Collembola species can avoid
becoming waterlogged by climbing up the tree trunk to drier bark.
These tend to be larger species mainly from the genera Entomobrya and Orchesella, yet climbing of the trees for survival has been
described for several other species (Bowden et al., 1976; Bauer,
1979; Farrow and Greenslade, 1992; Zettel et al., 2000). Tree trunks
can therefore be considered as ecological Noahs Arks providing
protection for some Collembola species, which, after the red sludge
ood receded, could re-colonise the surface and upper soil layers
quickly.
The broad difference in soil pH levels between the red mud
polluted and control areas gave us the opportunity to collect additional data on species pH tolerance in the eld. Heteromurus nitidus
was more abundant in the polluted forest plots than in the control forests on acid soil. In culture experiments by Salmon and
Ponge (1999) this species preferred acid soils, while in another
experiment, Salmon et al. (2002) also demonstrated its attraction
to an alkaline buffer solution rich in Na. Both phenomena were
conrmed in the course of this eld investigation. Although the
species M. pygmaea is known for his strong afnity to acid soils
(Hgvar and Abrahamsen, 1980, 1984; Hgvar, 1984; Ponge, 1993),
its presence was also observed at neutral pH in laboratory experiments (Gillet and Ponge, 2003). This species was collected from
both the acid soil of the control forests; as well as, from the strongly
alkaline soil of the red mud polluted forests, which indicate a
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10
ARTICLE IN PRESS
high tolerance to both soil environments, acidity and alkalinity

alike.
5. Conclusion
The present study demonstrated that despite of the unprecedented environmental disaster that occurred in Hungary and the
high toxicity risk associated with this accident, no adverse effect
has been observed in Collembola abundance; and red mud polluted
areas clearly show signs of soil fauna revitalisation and recolonisation. Due to the considerably increased pH levels, trace metal
components are tightly bound and thus their limited bioavailability does not represent a high risk in the short-term. Nevertheless,
as a consequence of soil re-acidication, re-mobilisation of xed
metals in the red mud polluted soil may occur in the long-term,
constituting to a potential risk for soil organisms, including Collembola.
Acknowledgements
I would like to thank Gyrgy Traser for his help in taxonomic
identication and for his invaluable professional support; dm
Erdo and Istvn Harta for their assistance in eld work; the Institute
of Soil Site Survey for soil analyses and Dalma Btkay for providing
language help. I am greatly indebted to the two anonymous reviewers for their valuable suggestions highly improving the manuscript.
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APSOIL-1892; No. of Pages 11

Contents lists available at ScienceDirect

Applied Soil Ecology

Collembolan response to red mud pollution in Western Hungary

Tel.: +36 70 3170807; fax: +36 99 518350.

which became known as the red mud incident in international

related to alkalinity, heavy metal content and radioactive material

Fig. 1. Study area, location of sampling plots.

(1966) evenness index. The Shannon indices were compared

D. Winkler / Applied Soil Ecology xxx (2013) xxxxxx

habitats (control and polluted) had lower number of species; 28

Metaphorura riozoi Castano-Meneses,

Allacma fusca (Linnaeus, 1758)

variance: 63.84%; axis 2: eigenvalue: 0.193; explained variance:

D. Winkler / Applied Soil Ecology xxx (2013) xxxxxx

potential toxicity of heavy metals in soils depends on not only

4.2. Collembola diversity and abundance

community diversity proles (Fig. 2) of the sampled forests and

communities, but no particular change occurred in abundance

high tolerance to both soil environments, acidity and alkalinity

soil substrate as inuenced by pH and organic matter. Appl. Soil Ecol. 5,

Domene, X., Alcaniz,

Stefanovits, P. 1992. Talajtan. Mezogazda

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