Science of the Total Environment 414 (2012) 364–372

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Science of the Total Environment

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Heavy metal sensitivity and bioconcentration in oribatid mites (Acari, Oribatida)Gradient study in meadow ecosystems

Piotr Skubała a,⁎, Tomasz Zaleski b

a Department of Ecology, University of Silesia, Bankowa 9, 40-007 Katowice, Polandb Department of Soil Science and Soil Protection, Agricultural University in Krakow, Mickiewicza 21, 31-120 Cracow, Poland

⁎ Corresponding author. Tel.: +48 32 359 11 48; faxE-mail address: piotr.skubala@us.edu.pl (P. Skubała)

0048-9697/$ – see front matter © 2011 Elsevier B.V. Alldoi:10.1016/j.scitotenv.2011.11.006

a b s t r a c t

a r t i c l e i n f o

Article history:Received 11 August 2011Received in revised form 31 October 2011Accepted 1 November 2011Available online 30 November 2011

Keywords:Heavy metalsOribatidaBioconcentrationPollutionMeadow soils

In this study we aimed to identify different reactions of oribatid species to heavymetal pollution and tomeasureconcentrations of cadmium, zinc and copper in oribatid species sampled along a gradient. Oribatid mites weresampled seasonally during two years in five meadows located at different distances from the zinc smelterin the Olkusz District, southern Poland. Oribatids were shown to withstand critical metal concentrationand established comparatively abundant and diverse communities. The highest abundance and speciesrichness of oribatids were recorded in soils with moderate concentrations of heavy metals. Four differentresponses of oribatid species to heavy metal pollution were recognized. Heavy metals (Zn, Pb, Cd, Ni) andvarious physical (bulk density, field capacity, total porosity) and chemical (Kav, Pav, N, C, pH) factors wererecognized as the structuring forces that influence the distribution of oribatid species. Analysis by atomicabsorption spectrophotometry revealed large differences in metal body burdens among species. None ofthe species can be categorized as accumulators or non-accumulators of the heavy metals — the pattern dependson themetal. The process of bioconcentration of the toxicmetal (regulated) and essential elements (accumulated)was generally different in the five oribatid species studied.

© 2011 Elsevier B.V. All rights reserved.

1. Introduction

Soil organisms may play an important role in the transfer of metalsthrough the ecosystem in metal-polluted environments (Janssen et al.,1991). A number of field studies have described the reaction ofmicroar-thropods on heavymetal pollution (e.g. Bengtsson and Rundgren, 1988;Hågvar and Abrahamsen, 1990; Rabitsch, 1995; Russell and Alberti,1998). Oribatid mites (the most numerous group of microarthropodsin many soils) form a group that is still rarely considered in heavymetal research. Additionally, knowledge on response of oribatid faunato contamination and the body burden in oribatid species is still greatlylacking. This contrasts with their great diversity and abundance. They arenot passive inhabitants of ecosystems; rather they are strong interactors,important indicators of disturbance in ecosystems andmajor componentsof biological diversity. Generally saprophagous species are considered assuitable metal accumulators for monitoring studies (e.g. Hopkin, 1989)andoribatidmites, as edaphic animals feeding on “metal-enriched” fungalmycelia (Roth, 1992), are especially interesting to study in terms of theconcentrations of essential and potentially toxic metals in their bodies.

Authors have emphasized that oribatidmitesweremore sensitive toheavy metals than other soil arthropods (Bengtsson and Tranvik, 1989;Steiner, 1995; Strojan, 1978; Van Straalen et al., 1989a, 1989b). Many

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authors have shown that oribatids easily accumulate heavy metals,but there is a great variation among species (Ludwig et al., 1991;Siepel, 1995; Skubała and Kafel, 2004; Zaitsev, 1999; Zaitsev and VanStraalen, 2001). Oribatid mites are especially diverse in forest soilsand most studies on oribatids in contaminated soils have been con-ducted in these habitats (e.g. Ivan and Vasiliu, 2009; Khalil et al.,2009; Kratzmann et al., 1993; Seniczak et al., 1997; Skubała and Kafel,2004; Strojan, 1978; Van Straalen et al., 2001; Weigmann, 1995;Zaitsev and Van Straalen, 2001). We decided to investigate the reactionof oribatid fauna on heavy metal contamination in meadow soils.

This study investigated the effects of increasing levels of heavymetal contamination on the oribatid mite communities in meadowsoils. Furthermore, the influence of other physico-chemical parametersof meadow soils on mite communities was analyzed. We tested thehypothesis that moderate levels of heavy metal pollution increasethe abundance and species diversity of oribatid mites. Moreover, toestimate bioavailability of cadmium, zinc and copper in the studyarea and its mobility, bioconcentration values were investigated infive dominant oribatid species. We investigated whether nutritionalmetals (e.g. Zn and Cu) or xenobiotics (e.g. Cd) accumulate differentlyin the bodies of oribatid species.

2. Site description

The heavily industrialized vicinity of the town of Olkusz, southernPoland, an area rich in non-ferrous ores, where a metal pollution

Table 1List of methods used, with some remarks on physical and chemical analyses of the soil.

Propertiesof the soil

Method References

Content of Cd, Zn,Cu, Pb and Ni

AAS method, PU 9100xmodel of apparatus

Ostrowska et al. (1991)

K and P available Egner-Riehm's method Lityński et al. (1976)Mg available Schachtschabel's method Lityński et al. (1976)Total nitrogencontent

Kjeldahl's method Lityński et al. (1976)

Organic carbon Tiurin's method Lityński et al. (1976)Field capacity Determined in Richards

chambers on porous platesKlute (1986)

Bulk density Determined in soil cores (naturalsystem was preserved) sampledinto 100 cm3 volume cylinders

Klute (1986)

pHKCl Potentiometric method Lityński et al. (1976)

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gradient can be demarcated easily, was selected for the study. Sampleswere collected at five meadow sites situated along a gradient of heavymetal pollution running 32 km northeast from Olkusz. Four of themare situated in the vicinity of the town of Olkusz (approx. 50°17′ N,19°31′ E). For comparison, a reference site was studied as well (50°32′N/19°39′ E). Chosen sites were the same as those investigated byteams studying other species in parallel (Łagisz et al., 2002; Łaszczycaet al., 2004; Stone et al., 2001). The results on oribatids in forestsalong this gradient were presented in Skubała and Kafel (2004). Miningactivity in these areas has been carried out since Medieval Ages. Themain sources of pollution are a mining-metallurgic smelter and miningplants, all situated in close vicinity of each other. The main pollutantsare heavy metals (Pb, Zn, Cd, and Cu) from natural sources (zinc- andlead-containing ores) and from industry.

Site I represents a xerothermic meadow on sandy and initial soilsfrom the class Koelerio glaucae–Corynephoretea canescentis Klika inKluka et Novak 1941. Other meadows and the reference site representgenerally the alliance Arrhenatherion elatioris (Br.–Bl. 1925) Koch, 1926.Site II was the low-intensity management grassland with some speciesof thermophile forest fringes. The third meadow (site III) is a species-rich grassland under moderate intensity management practices onrecent mineral soils. The fourth meadow (site IV) represents grasslandwith some species characteristic of thermophile forest fringes and palefescue grassland. The reference site (V) is a grassland of A. elatioriswiththe admixture of ecotone species from the class Festuco–BrometeaBr.–Bl. et R. Tx. 1943. For additional information on localities, floristiccharacterization and soil descriptions see Łaszczyca et al. (2004) andsee Augustyniak et al. (2005) for lists of dominant grasses on thestudy sites.

3. Materials and methods

3.1. Sampling, extraction and species identification

At five sampling sites six random soil samples of topsoil (0–7.5 cm)were taken using a corer of 4.8 cm diameter. The topsoil layer includedthe litter layer. Soil samples were taken from a representative quadrat(10×10 m) at each site. Sampling was done seasonally in 2000–2002(15.05, 10.07, 08.10.2000, 12.01, 18.05, 13.07, 11.10.2001 and 16.01.2002)— a total of 30 samples per date, and a grand total of 240 samples.The representatives of mesofauna were separated from the soil usingthe Tullgren method. Mites extracted for heavy metal determinationswere preserved in amixture ofwater and glycerol with addition of alco-hol (approximately 5%) and kept in a refrigerator to avoid evaporationand development of microflora. Adult oribatid mites were assigned tospecies. The classification proposed by Subias (2004) was followed.

3.2. Test species and analytical methods

Five species which occurred in high numbers at the most contami-nated site (over 5% in the total number of oribatids), were chosen tostudy differences in Cd, Zn and Cu concentration between species.There was only one species (Tectocepheus velatus) which occurred atall sites in high numbers with high frequency. The species was chosento investigate trends of metals accumulation in oribatids at differentdistances from the smelter.

A group of 50 specimens was used in the analysis of metals. Theanimals were pooled together and weighed three times to establishtheir weight accurately. They were weighed on a AG-245 (MettlerToledo) balance with readability of ±0.01 mg, repeatability of ±0.02 mg and linearity of ±0.03 mg. Then they were dried and digestedwith concentrated nitric acid (Suprapur grade, Merck) and diluted withdistilled and deionized H2O. Determination of metal concentration wasby flame atomic absorption with flame (zinc) or electrothermal atomi-zation (cadmium and copper), using a Solar 939 spectrophotometer(background correction of deuterium). The operating conditions of

measurement were as follows. The wavelengths for zinc, cadmiumand copper were 213.9 nm, 228.8 nm and 324.8 nm, respectively. Theatomizing temperature was 2400 °C (cadmium) or 2600 °C (copper).The injected sample volume into graphite cuvette was 15 μl. The slitwidth was constantly 0.5 mm and the recording time was 3 s. Theanalyses of metals were repeated three times for each digest. Otherdetails concerning analysis of metals in the body of oribatid speciesare described in Skubała and Kafel (2004).

The bioconcentration factor (BCF) was calculated according to theformula: concentration of the metal in organism/concentration of themetal in soil. We used the term “accumulator” for species with theBCF higher than 1, and “non-accumulator” or “deconcentrator” fororibatids characterized by the BCF lower than 1.

3.3. Soil analysis

Analyses were carried out of the physical and chemical properties ofthe soils, which were thought to be of importance in the pedogenesis ofthe sites and of possible significance to themite fauna. All environmentalfactors have been determined from soil cores, which have been taken inclose vicinity to the cores used for mesofauna extraction.

Themethods and appropriate authors used in chemical and physicalanalyses of the soil are listed in Table 1. Five samples were collectedfrom each horizon (0–7.5 cm depth) for chemical analyses (volume —

250 cm3) and physical one (volume — 100 cm3). The determination ofsoil characteristics was carried out on pooled material collected fromeach of the soil horizons that were investigated.

Total porosity was determined according to the following formula:

p ¼ D–d=D½ �

where D — solid particle density and d — bulk density.

3.4. Statistics

The populations of species and the oribatid communities werecharacterized by the following indices: abundance, species richness,dominance, Shannon index of diversity (H′) and equitability (J). Thedifferences in abundance between sites, between collection date (sea-sons) and site by date interactions were tested by two-way analysis ofvariance (ANOVA). Because of their non-normal distribution, oribatidnumberswere transformed to log(x+1) prior to an analysis of variance.When a statistically significant difference (pb0.05) was noted differingpairs were identified with the Tukey test.

Correlation between metal body burdens in oribatid species andconcentrations ofmetals in soil or the abundance of specieswas calculat-ed with the Pearson's product–moment correlation test. Prior to the

Table 3Maximum acceptable concentrations (mg∙kg−1) of heavy metals by different authors.

Heavy metals Polish system ofsoil standardsa

Uncontaminated soilsb MACc CMCd

Cd 4 1 1 10–50Zn 300 100 150 b500Cu 30 30 50 b100Pb 50 50 50 100–200Ni 35 50 30 –

a Source: Regulation by the Minister of Environment.b Source: Kabata-Pendias and Pendias (2001).c European Economic Community for Maximum Acceptable Concentration (MAC) in

agricultural soils, Source: CEC (1986).d Critical Metal Concentration (that will cause no adverse effects), Source: Bengtsson

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analysis, the data, which did not meet the assumptions of normality,were log-transformed.

To test whether the oribatid community composition was affectedby metal pollution and to determine which other environmental vari-ables influenced oribatid fauna a multivariate data analysis techniquewas employed. A DCA was first carried out to determine whether thespecies matrix had a linear or a unimodal response. The length of thegradient for the first axis was above 3 and as a consequence, CCA wassuitable as direct ordination analysis (Ter Braak and Šmilauer, 2002).To avoid an excessive amount of noise in the data matrix, which couldobscure some data features, all species present as singletons wereremoved from the analysis. All statistical calculations for this researchwere carried out using STATISTICA 9.1 and CANOCO 4.5 software.

and Tranvik (1989).

4. Results

4.1. Soil analysis

The sequence of heavymetal concentration (mg/kg) in themeadowsoils subject of this research was: Zn>Pb>Cu>Cd>Ni. The distributionof cadmium, zinc and lead in the uppermost topsoil decreased withthe distance from the smelter (Table 2). These metals were recordedat elevated concentrations in the soil of meadow I, II and III comparedto the concentrations in normal and non-polluted soils (see Table 3).The differences between site I–III and site IV–Vwere statistically signif-icant (Tukey test). The content of these metals was the highest at site Ibeing 2.5 (Cd) to 4.5 (Zn) times higher than maximum acceptableconcentration in agricultural soils. The copper content of the soilprofiles did not exceed the maximum acceptable concentration insoil; however, site I to IV can be regarded as slightly contaminated(see Tables 2, 3). The highest absolute value for Cu was recorded atsite II; however, no significant differences were noted between sites.The distribution of nickel showed a more irregular pattern over thestudy area, being the highest at site IV and the lowest at site III. Weclassified meadow soils as highly polluted (site I and II), moderatelypolluted (site III and IV) and reference, based on the Polish and othersystems of soil standards for cadmium, zinc and copper (Table 3).

The available K, P and Mg varied between meadow soils, however,it is always highest in meadow I. Only with regard to available P, therewere no statistically significant differences between sites. The meanvalues of total nitrogen content, organic carbon and C-to-N ratio werehighest at site III (Table 2).

Field capacity, which is an indicator of the water-holding capacityof soil, was progressively higher from site I to III. The lowest value was

Table 2General characteristics of soil at five sampling locations in the Olkusz area. Means and standardeach other at the pb0.05 level according to the Tukey test.

Properties of soil Units Meadow I Meadow I

Cd mg∙kg−1 13.56±1.32c 10.96±Zn mg∙kg−1 1337.00±43.72c 1067.25±Cu mg∙kg−1 31.58±1.08a 40.35±Pb mg∙kg−1 418.02±20.97b 331.07±Ni mg∙kg−1 4.55±0.54c 1.71±K available [Kav] mg∙kg−1 1825.85±875.55c 28.67±P available [Pav] mg∙kg−1 224.72±42.25a 170.78±Mg available [Mgav] mg∙kg−1 307.27±67.19c 105.22±Total nitrogen content [N] g∙kg−1 1.89±0.30a 1.99±Organic carbon [C] g∙kg−1 17.81±2.46a 16.60±C-to-N ratio [C/N] 9.45±0.33c 8.42±Field capacity [fc] m3∙ m−3 0.35±0.04a 0.36±Bulk density [bd] mg∙m−3 1.13±0.06b 1.16±Total porosity [tp] m3∙ m−3 0.57±0.02a 0.55±pHKCl [pH] 6.12±0.18b 5.71±

In brackets: codes of soil properties.

observed at the reference site. Similarly total porosity, which expressesthe amount of soil spaces, was the highest at site III and significantlylower at other sites (being lowest at the reference site). With regardto bulk density, it varied from 0.71 mg∙m−3 at site III to 1.32 mg∙m−3

at the reference site. Soil pHKCl values ranged from 4.92 (meadow III)to 7.05 (reference site). A Tukey multiple range test (pb0.05) revealeddifferences in the mean value of pH between site III and other sites(Table 2).

4.2. Gradient study

In total, 4511 specimens and 58 species of oribatid mites, belongingto 43 genera, were found at different sites in the study area.

The two-way ANOVA revealed significant differences in oribatidabundance among sites. As regards differences between seasonsthey were significant for juvenile oribatids (Table 4). Furthermore,significant differences within the interaction of these two variables(pb0.05) for adults, juveniles and all oribatids were observed. Theabundance of oribatids increased from site I to site III (over threetimes higher than at site I). Meadow III had the highest total abundanceof oribatids; however, it was not statistically different from theabundance at the reference site. The abundance of adults followedthe same pattern. As regards the abundance of juveniles, it increasedfrom site I to site V (Table 4).

Differences in species richness were also pronounced betweensites. The highest number of species was recorded at site III, whereit was over two times higher than at site I. At the reference site,

deviations of five replicates. Means with identical letters are not significantly different to

I Meadow III Meadow IV Meadow V

6.69c 6.36±0.86b 2.73±0.69a 1.68±0.83a

498.76c 552.13±81.93b 221.16±60.49a 126.75±59.13a

12.31a 31.21±2.09a 33.97±3.26a 23.87±3.68a

192.21b 289.40±44.52b 83.56±28.37a 41.88±30.36a

1.21b 0.11±0.19a 15.90±4.58d 10.59±4.83d

7.77a 170.80±66.89b 183.26±27.06b 130.59±42.19b

183.13a 101.85±8.92a 146.46±28.90a 115.11±76.73a

43.41a 288.33±115.94b 169.12±59.45a/b 102.60±68.29a

0.91a 4.79±0.94b 2.89±0.43a 2.90±0.75a

6.68a 45.81±10.87b 20.34±1.51a 16.87±1.96a

1.62b/c 9.49±0.55c 7.14±0.95a/b 6.05±1.18a

0.50a 0.47±0.04b 0.39±0.01a 0.34±0.03a

0.17b 0.71±0.09a 1.25±0.12b 1.32±0.06b

0.06a 0.70±0.04b 0.51±0.04a 0.49±0.02a

0.09b 4.92±0.09a 5.89±0.43b 6.50±0.44b

Table 4General characteristic of oribatid mite communities and mean abundances of other groups of mesofauna in meadows. Abundance of oribatids (± S.E. and n=48) is tested by two-way analysis of variance (ANOVA). Mean abundances (indiv./m2) are compared by the Tukey method to test for differences between sites. Tests are carried out on the log (x+1)transformed date.

Meadow I Meadow II Meadow III Meadow IV Meadow V Two-way ANOVA

F-ratio p

Abundance of adults Sites 3924±733a 6620±972b, c 13,206±1889d 5023±733a, b 8160±839c, d 14.67 0.000Seasons 0.27 0.85Sites×seasons 1.81 0.04

Abundance of juveniles Sites 1076±389 a 1852±333b 2975±606b 3380±700b 5995±1189c 16.97 0.000Seasons 17.04 0.000Sites×seasons 5.08 0.000

Abundance in general Sites 5000±944a 8472±1105b 16,181±2333c 8403±1244b 14,155±1594c 17.63 0.000Seasons 1.98 0.12Sites×seasons 2.60 0.003

Number of species 18 21 39 24 25Shannon index (H′) 2.099 1.694 2.858 2.077 1.924Equitability (J) 0.726 0.557 0.780 0.654 0.598

The results of the Tukey method are given by letters. Means sharing a common letter (a, b, c or d) do not differ significantly at the 5% level from other means.

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twenty-five species were recorded (Table 4). There was a trend thatmore species were present at sites with the highest total abundance.The correlation coefficient between log-transformed total abundanceand number of species was not significant (r=0.82, p=0.08). It canbe seen from Appendix 1 that 27 species (46%) were restricted toone site. All sites had two (reference site) to fourteen (meadow III)species that were limited to that same site. There were only six speciescommon to all sites (e.g. T. velatus, Microppia minus, Oppiella (O.) nova,Suctobelbella (S.) subcornigera).

Site III was characterized by the highest species diversity, whilethe lowest value of the Shannon index was found at site II. Resultsregarding equitability (J) among all sites followed the same trendsas the Shannon index (Table 4).

The distribution of dominant oribatid species across sites is shownin Table 5. In total, 17 species were dominant (over 5% in the totalnumber) at the study sites. Six dominant species were observed atsite I and III, however, the proportion of species was higher and lessproportional at site I than site III. Five dominant species were notedat the reference site and four at site II and IV. One species at site II(T. velatus) reached disproportionally high percentage in the totalnumber of oribatids (>54%). Similarly, Scheloribates (S.) laevigatus wasnoted to have a very high dominance index (>43%) at the reference

Table 5Dominant species (D>5%) in oribatid mite communities from meadow habitats.

Species Codes Meadow

I II III IV V

Berniniella (B.) serratirostris hauseri Bhau – – 7.1 1.4 –

Dissorhina ornata Dorn – – 7.4 – –

Eupelops tardus Etar – – 5.3 1.4 3.1Fosseremus laciniatus Flac – 0.2 – 0.7 7.7Lauroppia fallax Lfal – 7.3 – – 0.4Liochthonius (L.) lapponicus Llap 10.0 4.7 0.4 1.4Metabelba (M.) papillipes Mpap – – – 14.7 –

Microppia minus Mmin 0.3 1.6 15.9 3.9 2.3Oppiella (O.) nova Onov 2.4 10.0 1.0 22.1 8.6Oribatula (O.) tibialis Otib 9.7 0.3 0.4 – –

Peloptulus phaeonotus Ppha 9.4 – 0.6 0.5 –

Punctoribates (P.) punctum Ppun 26.8 – 1.3 1.2 –

Scheloribates (S.) laevigatus Slae – – 7.7 25.3 43.3Scutovertex sculptus Sscu 10.0 0.3 1.5 – 1.7Suctobelbella (S.) subcornigera Ssub 1.8 10.1 2.6 0.2 0.6Tectocepheus velatus Tvel 22.4 54.4 19.0 19.1 18.4Trichoribates (Latilamellobates) incisellus Tinc – 0.2 1.2 0.5 6.9

Bold type indicates dominant species at particular site.Values are percentages of the total number of oribatids collected at each site.

site. Among the dominant group of oribatids, only T. velatuswas observedat all sites. Two species (Dissorhina ornata,Metabelba (M.) papillipes)wereeach observed at single site. Most species dominated at one site andwereobserved in low numbers at other sites (Table 5).

Data for oribatid mites were analyzed by means of CCA analysis(Fig. 1). The eigenvalues of axes 1 and 2 were high: 0.505 and 0.438, re-spectively. The cumulative percentage of variance explained by the firsttwo canonical axes accounted for 65.5% (35.1 and 30.4%, respectively forthe first and second axes) of the species-environmental relations. CCAordination distinguished the highest-polluted plus moderately pollutedsites (the right side of the graph) from the less or non-polluted ones (theleft side). The second axis of the CCA separated the moderately pollutedsite (meadow III) fromother sites. According to their correlationwith theaxes, the environmental variables determining the gradients in CCAdiagrams were Cd, Zn, Kav, Pb, Pav for axis 1 and C/N and bd, C, tp,fc, pH and N for axis 2 (Table 6).

The scatter of species and sites may be divided into three distinctbranches. Branch A is composed of species (e.g. Liochthonius (L.) lappo-nicus; Oribatula (O.) tibialis; Peloptulus phaeonotus; Punctoribates (P.)punctum; Scutovertex sculptus) that occurred abundantly only in mead-ow I. The species were mainly affected by factors associated with thefirst axis, e.g. zinc, cadmium and available phosphorus and potassium(Fig. 1). Branch B is composed of species connected with the moderatelycontaminated site (meadow III). Berniniella (B.) serratirostris hauseri,D. ornata, Eupelops tardus andM. minuswere noted in this group. Thespecies are ordinated in the positive part of the second axis. Theywere affected by several environmental factors, of which field capacity,organic carbon, total nitrogen and total porositywere themost importantones. Branch C consists of species typical of the meadow IV and thereference site. The following species were associated with these

Fig. 1. Concentrations (μg/g) of cadmium, zinc and copper contents in Tectocepheusvelatus from contaminated meadow soils and the reference site.

Table 6Intraset correlations between environmental variables and constrained site scores.

Properties of soil Axis 1 Axis 2 Properties of soil Axis 1 Axis 2

Cd 0.878 0.058 N −0.226 0.889Zn 0.876 0.004 C 0.030 0.956Cu 0.292 0.082 C/N 0.672 0.686Pb 0.843 0.397 Fc −0.003 0.932Ni −0.487 −0.766 Bd −0.237 −0.957Kav 0.862 −0.338 Pv 0.291 0.945Pav 0.691 −0.641 pH −0.139 −0.931Mgav 0.578 0.613

Codes of environmental variables see Table 3.

Table 7Bioconcentration factors (BCF) of the selected oribatid species.

Species Cadmium Zinc Copper

Tectocepheus velatus 0.18 (I) 1.52 (I) 9.10 (I)0.18 (II) 1.94 (II) 3.88 (II)0.13 (III) 2.17 (III) 3.18 (III)0.34 (IV) 2.20 (IV) 5.58 (IV)0.61 (V) 4.15 (V) 10.46 (V)

Punctoribates (P.) punctum 0.48 (I) 0.07 (I) 0.51 (I)Scutovertex sculptus 0.15 (I) 0.05 (I) 44.1 (I)Oribatula (O.) tibialis 0.14 (I) 0.44 (I) 5.95 (I)Peloptulus phaeonotus 0.40 (I) 0.11 (I) 2.32 (I)

Bold type indicates values higher than 1.0.

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sites: Fosseremus laciniatus; M. papillipes; S. laevigatus; Trichoribates(Latilamellobates) incisellus. Several factors, e.g. nickel, bulk densityand pH were the most important (Fig. 1).

4.3. Metal accumulation by oribatids

T. velatus was chosen to study metal body burden in oribatidsalong the gradient. The body burden of cadmium, copper (site I)and zinc (site II) in T. velatus were highest close to the smelter, andthen declined with distance. However, metal concentrations at thereference site were slightly higher than in meadow IV or III. In generalthe content of heavy metals in the body of the species at the mostcontaminated site was two times (Cd), four times (Zn) and 20%(Cu) higher than at the reference site (Fig. 2). The bioconcentrationfactors in T. velatus were high (over 1.0) for zinc and copper andlow for cadmium content (Table 7).

The abundance of the species decreased when the cadmium andcopper contents are increased in that same species. However, therelationship was not significant (r=−0.56, p=0.93 for cadmium

Fig. 2. Ordination of sampling sites and oribatid species on the CCA triplot. Only dominantoribatid species are depicted. Codes of species and environmental variables (see Tables 5and 2, respectively.

and r=−0.82, p=0.09 for copper). As regards zinc, the correlationwas positive but very weak (r=0.38, p=0.53). The cadmium andzinc contents in the body of T. velatus correlated significantly withmetal content in soil (r=0.91, pb0.03 for Cd and r=0.97, pb0.005for Zn). A non-significant negative correlation between the coppercontent of T. velatus and soil was detected (r=−0.50, p=0.39).

Concentrations of cadmium in five oribatid species were relativelylow (Table 8). The highest concentration was found in P. punctum andthe lowest in O. tibialis. Zinc and copper were accumulated to differentdegrees in oribatid species. The highest average concentration of zincwas observed in T. velatus. The lowestwas found in S. sculptus. Similarly,copper accumulation varied between species. The greatest concentra-tions of copperwere observed in S. sculptus and the lowest in P. punctum(Table 8).

It is notable that different oribatid species have quite differentconcentration capacities for certain metals (Table 7). The biocon-centration factor was low for cadmium for all species. A similar trendcould be observed for zinc. The only exception was the zinc load inT. velatus at all study sites. The greatest concentration factors werefound for copper in all species investigated. BCF for copper varied from2.32 (P. phaeonotus) to 10.46 (T. velatus at the reference site). The onlyexception was P. punctum with the bioconcentration factor lower than1 (0.51).

5. Discussion

5.1. Oribatid communities in gradient study

Typical heavy-metal vegetation types have been distinguished forplant assemblages on heavy-metal soils throughout the world (Ernst,1974). Indications for a specific metal-fauna equivalent to metal-vegetation, are lacking (Posthuma and Van Straalen, 1993). However,as regards soil mites (andmany other soil animals), they can establishedpermanent, stable communities on even extremely contaminated soils.

The abundance of oribatids in the highly contaminated meadow Iwas about three times lower than at the reference site and in meadowIII. We found 18–39 species of oribatid mites per site and 58 over allfive sites. This is somewhat lower than what would be expected frommeadow soils in Poland (Niedbała et al., 1981; Petrov, 1997; Rajski,1961; Żyromska-Rudzka, 1976). The authors recorded the abundance

Table 8Content of heavy metals (μg/g of fresh weight) in the body of selected oribatid speciesfrom the most contaminated site (meadow I).

Species Cd Zn Cu

Tectocepheus velatus 2519 2038.21 307.34Punctoribates (P.) punctum 6554 98.53 16.16Scutovertex sculptus 2089 64.00 1392.00Oribatula (O.) tibialis 1.925 584.72 187.80Peloptulus phaeonotus 5396 142.00 73.30

Bold type indicates the highest value of a particular metal for a species.

369P. Skubała, T. Zaleski / Science of the Total Environment 414 (2012) 364–372

of oribatids in most meadows between 20 and 160 thousands/m2. Thenumber of species varied from 18 to 38 species. Skubała (2004) notedsimilar abundance (from 7 to 15 thousands/m2) and number of species(ranged from 22 to 52) for meadows neighboring post-industrialdumps in Upper Silesia. However, it is noteworthy that in our study,the difference in abundance between contaminated meadows andthe reference meadow was not remarkable. Furthermore, the num-ber of oribatid species at the reference site was only slightly higherthan that recorded in the most contaminated meadow.

Reduction of the abundance and species richness of oribatid mitesin soils close to a smelter is a well known phenomenon (Bengtssonand Rundgren, 1984; Skubała and Kafel, 2004; Strojan, 1978; Zaitsevand Krivolutskij, 1999). Some authors underlined that oribatids gen-erally seemed to be more susceptible to heavy metals than most ofthe other arthropods (Bengtsson and Rundgren, 1988; Hågvar andAbrahamsen, 1990; Strojan, 1978). One of the important reasons forthe reduction in abundance and species richness of Oribatida at highlycontaminated sites may be explained by toxic effects through uptakeof heavy-metal loaded fungi (Hågvar and Abrahamsen, 1990). Oribatidsare known to ingest fungal hyphae (Siepel and de Ruiter-Dijkman,1993) and fungi accumulate heavy metals efficiently (Khan et al.,2000; Valix et al., 2001). However, in our study, the Oribatida commu-nities in contaminated meadow soils were neither very rich nor verypoor, as indicated by abundance and species richness.

The Shannon index and equitability were higher at the mostcontaminated site than at the reference site. This seems surprising.Surely, in highly contaminated soils the dominant species would beexpected to decrease, without disappearing, which, paradoxically,may increase the index. This phenomenon, and the precaution thatdiversity indices should be used carefully, was underlined by Cortetet al. (1999).

Some structural parameters of the oribatid community at the mostcontaminated site (e.g. the reduced number of species and their lowabundances, the lowest proportion of oribatids in the general numberof Acari) might indicate that this community is a less labile one, withreduced self-regulation possibilities. However, the differences wereonly slight in comparison with the other meadows that were part ofthe study and the control.

The oribatid community at site III (moderately polluted) was char-acterized by the highest abundance, species richness and diversityamong studied sites. The values of these factors were even higherthan in the reference meadow. One explanation of this phenomenonmay be the intermediate disturbance hypothesis (Connell, 1978;Connell and Slatyer, 1977). The hypothesis predicts the highestdiversity in sites with intermediate levels of disturbance. However,as emphasized by Minor and Cianciolo (2007), some authors havenot confirmed this phenomenon, while studying other factors ofdisturbance.

Another explanation may be stimulatory effect of small doses ofheavy metals. The stimulation of low concentration of heavy metalson the rate of reproduction is recognized and is called hormesis.Denneman and Van Straalen (1991) described that both copper andlead stimulated reproduction in the low concentration range. Thisphenomenon was previously observed by some authors. Seniczak etal. (1997), studying mite communities polluted by a copper smeltingworks, observed increased abundance and species richness of Oribatidaat low copper concentrations. Similar stimulatory effects of heavy metalson oribatids have been foundbyBengtsson et al. (1985), El-Sharabasy andIbrahim (2010), Migliorini et al. (2005) and Stamou and Argyropoulou(1995).

5.2. Species response analysis

For Oribatida, species-specific differences in heavy metal suscepti-bility have been reported, resulting in decreasing abundances of certainspecies along pollution gradients, whereas other species maintain or

even increase their populations in contaminated areas (Khalil et al.,2009; Skubała and Kafel, 2004). This is to be expected because Oribatidaare highly diversified, both taxonomically and ecologically (VanStraalen, 1998). The mechanisms behind these responses are poorlyunderstood. One possible explanation is a direct toxic effect of metalson a population of a species. However, changes in trophic interactionsshould also be taken into account.

The results of the multivariate analysis (CCA) and the analysis ofdominance in the polluted meadows and the control one allow usto distinguish four abundance response types for dominant oribatidspecies in the gradient study. The first one includes species tolerantand favored by strong heavy metal pollution. Their abundance wasthe highest at the most polluted sites. The following species wereincluded in this group: L. lapponicus,O. tibialis, P. phaeonotus, P. punctumand S. sculptus. Metal-resistant oribatid species, which, profiting frommetal-induced disturbance, are characterized by relatively high fecun-dity and short life cycles (Luxton, 1981) and are often found in disturbedor early successional habitats (Maraun et al., 2003; Scheu and Schulz,1996; Skubała, 2004). It is evident that these species have an innate orevolved (physiological) resistance to heavy metals that allows them tomaintain their populations in even highly contaminated soils. Thecontent of heavy metals (Zn, Pb and Cd) and available potassium andphosphorous played a major role in the distribution that was observedfor species occurring at the most contaminated site.

The second group comprises species sensitive to heavy metals.These predominate at the reference site or the least contaminatedsite, e.g. F. laciniatus, M. papillipes, S. laevigatus and T. (Latilamellobates)incisellus. Bulk density, pH and content of nickel were identified asthe most important variables for the occurrence of above speciesand organization of an oribatid community in less polluted soils.The third group includes species indifferent to heavy metals thatoccurred at highly and less polluted sites, e.g. Lauroppia fallax, O.nova, S. subcornigera and T. velatus. None of the environmental factorsthat were investigated was selected as the most important for theoccurrence of the species.

Furthermore, a bell-shaped curve was observed in the distributionof four species (B. serratirostris hauseri, D. ornata, E. tardus and M.minus) along the pollution gradient. These species seem to be favoredby an increase in the metals content of the topsoil but this favorableeffect declined at the highest concentration of the metals. A similarbell-shaped distribution of tolerant species has been observed inother metal-polluted sites (Bengtsson and Rundgren, 1984, 1988;Dunger, 1986; Gillet and Ponge, 2003). Nitrogen and carbon contents,field capacity and total porosity were recognized as themost importantenvironmental factors that influenced the occurrence of the species inthis study.

5.3. Metals in T. velatus along the heavy metal gradient

To date, metal concentrations along a contamination gradienthave been estimated in few oribatid species (e.g. Skubała and Kafel,2004; Zaitsev and Van Straalen, 2001). In the current study, T. velatuswas seen to bioaccumulate large quantities of copper and zinc,whereas the bioconcentration factor for cadmium was below 1. Thespecies was indifferent to metal concentrations in its body at thelevel found in our research. The same phenomenon was observedfor T. velatus and most of the oribatid species that were investigatedby Skubała and Kafel (2004) or Zaitsev (1999). The internal Cd andZn concentrations in T. velatus increased with the elevated doses ofthese metals in soil. This phenomenon is well known and describedby Heikens et al. (2001) for Pb, Cd and Cu in most taxonomic groupsof terrestrial invertebrates. The internal Zn concentration has usuallybeen observed to be independent of the concentration in soil(Heikens et al., 2001; Skubała and Kafel, 2004), which is in contrastto our study.

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T. velatus has appropriate ecological attributes to live in highlycontaminated sites. It is considered an opportunistic herbofungivorousspecies, meaning a species which is able to digest cellulose in litter andcell-walls of living green plants and trehalose in fungi (Siepel, 1995).Siepel (1995) mentioned that representatives of this feeding guildtend to be more numerous in polluted sites. T. velatus is well knownfor being parthenogenetic, with a relatively rapid life cycle (Luxton,1981). According to Siepel (1995) thelytokous species, present inheavy metal polluted areas are resistant to the pollutant, or able toavoid it, andmay reproducemore effectively than sexually reproducingspecies. It has a cosmopolitan distribution occurring in a wide range ofdifferent habitats (Schatz, 1983). Skubała and Kafel (2004) also foundT. velatus occurring at all sites along a heavy metal gradient, reachingthe highest proportion at the most contaminated site. However,Seniczak et al. (1997) classified the species as sensitive to high copperand lead, although tolerant to moderate levels of these metals. Fromour study T. velatus can be classified as species able to persist in awide range of heavy metal pollution.

5.4. Metals in dominant species in highly contaminated meadow soils

Oribatid mites are now known as animals with a remarkable abilityto accumulate metals (Khalil et al., 2009; Lebrun and Van Straalen,1995; Skubała and Kafel, 2004; Van Straalen et al., 2001). In the currentstudy, large differences were found for zinc and copper concentrations,whereas cadmium showed little variation in the five species studied.The interspecific variation in heavy metal contents is well known inoribatid species (Janssen, 1988; Skubała and Kafel, 2004; Van Straalenand Van Wensem, 1986; Zaitsev, 1999; Zaitsev and Van Straalen,2001) and some authors have shown that it is much higher in oribatidsthan inmost other soil arthropods (Janssen, 1988; Van Straalen and VanWensem, 1986).

The bioconcentration factors show that different elements areconcentrated to different extents. For example, in S. sculptus the bio-concentration factor of Zn was found to be 0.05. At the same timeBCF for the same metal in T. velatus was 1.52. The overall trend ofthe bioconcentration of heavy metals in different oribatid specieswas Cu>Zn>Cd. Copper was accumulated especially efficiently inmost species, followed by Zn (T. velatus accumulates zinc in highquantities), whereas Cd was the most efficiently regulated metal(none of the species accumulated cadmium). However, a differentranking was found for each metal, namely:

Cd: P. punctum>P. phaeonotus>T. velatus>S. sculptus>O. tibialisZn: T. velatus>O. tibialis>P. phaeonotus>P. punctum>S. sculptusCu: S. sculptus>T. velatus>O. tibialis>P. phaeonotus>P. punctum.

Bioconcentration of Cd, Zn and Cu in the five studied oribatid mitesis due to their essentiality versus non-essentiality to the organism.Nutritional metals, such as Zn and Cu are accumulated and xenobiotics,like Cd are regulated. Van Straalen et al. (1987) underlined that somedata suggest that animals are able to regulate their body levels of nutri-tional metals over a broad range of environmental concentrations,while xenobiotics are accumulated. However, this is not a general rulefor terrestrial animals, e.g. invertebrates which contain hemocyanin intheir blood (Laskowski and Hopkin, 1996).

Low accumulation of cadmium in the bodies of all species studiedmay be surprising, as previous authors have reported a bioconcentrationfactor higher than one for cadmium in some oribatid species. Janssen andHogervorst (1993) recorded, for Platynothrus peltifer, a cadmium a con-centration factor over 1.5. Similarly, Zaitsev (1999) revealed the highestconcentration factors for cadmium followed by zinc and copper. El-Sharabasy and Ibrahim (2010) recorded the highest bioconcentra-tion factors for cadmium in all species they studied. However,Skubała and Kafel (2004) noted very low bioconcentration factors

for almost all oribatid species while studying oribatid fauna in forestsoils along the heavy metal gradient. In the current study low bio-concentration factors for cadmium showed that the oribatid speciesinvestigated are able to prevent high internal cadmium concentrations,possible by low uptake through the gut wall or by rapidly excretingcadmium.

A high bioconcentration factor for coppermay be expected in specieswhich use hemocyanin (Roth, 1992) as an oxygen carrier, such as snails,isopods and some arachnids (Janssen andHogervorst, 1993). As oribatidsdo not possess hemocyanin (Krantz and Walter, 2009), high copperconcentrations may indicate the presence of other substances, whichare capable of accumulating copper or the crucial role of this elementin the metabolism of oribatids. High copper concentrations have beenfound in animals which do not possess hemocyanin, e.g. diplopods orcollembolans (Janssen and Hogervorst, 1993) and oribatids (Skubałaand Kafel, 2004).

Zinc is an essential element, required in different enzymes (Taylor andSimkiss, 1984; Rainbow, 1988). Only one species (T. velatus) accumulatedthis element to quantities higher than were recorded in the soil (thebioconcentration factor ranged from 1.5 to over 4), while other speciesdid not. Similarly Skubała and Kafel (2004) did not record accumulationof zinc in any of nine oribatid species.

This study showed that it is difficult to categorize oribatid speciesas accumulators or non-accumulators of heavy metals — the patterndepends on the metal. The species exploring similar food resources(e.g. P. punctum and O. tibialis — both are fungivorous grazers orT. velatus and S. sculptus— opportunistic herbofungivores) showconsid-erable differences in bioconcentration of certain elements. Some authorshave emphasized this in the past (Khalil et al., 2009; Skubała andKafel, 2004) and it was evident from our study, that, in field studies,oribatids must always be identified to the species level since eachspecies responded differently.

6. Conclusions

• Some oribatid mite species can withstand critical metal concentration,e.g. Cd, Zn and Pb, and established comparatively abundant anddiversecommunities.

• Small concentrations of heavy metals positively influenced the abun-dance of oribatids. This observation fitted well with the intermediatedisturbance hypothesis and the concept ‘hormesis’.

• The content of Zn, Pb, Cd, K, P (for tolerant species), bulk density,pH, content of Ni (for sensitive species) and the content of N, C,field capacity and total porosity (for species characterized by thebell-shaped curve) were recognized as the structuring forces thatinfluence the distribution of oribatid species, thus representingone of the abundance response types.

• In the oribatid species that were more intensely studied, the processof concentration of the toxic metal was regulated, while the essentialelements were accumulated.

• T. velatus was found to be able to persist in a wide range ofheavy metal pollution. The species was indifferent to metal con-centrations in its body. The body burden of Cd and Zn in T. vela-tus increased with the increasing concentrations of these metalsin soil.

• Five of the oribatid species studied were deconcentrators ofcadmium.

Acknowledgments

The study was supported by a grant (Project No. 6 P04G 011 18)from the Polish State Committee for Scientific Research. I wish tothank Dr. P. Whelan of University College Cork, Ireland for his kindlinguistic and stylistic review of the manuscript.

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Appendix 1

Check-list of oribatid species found at the contaminated meadowsoils and the reference site.

Meadow

I II III IV V

Hypochthonius rufulus rufulus Koch, 1835 + +Liochthonius (L.) lapponicus (Trägårdh, 1910) + + + +Liochthonius (L.) propinquus Niedbała, 1972 +Liochthonius (L.) sellnicki (Thor, 1930) + +Sellnickochthonius cricoides (Weis-Fogh, 1948) +Sellnickochthonius immaculatus (Forsslund, 1942) + + + + +Acrotritia ardua (Koch, 1841) + +Microtritia minima (Berlese, 1904) +Nothrus anauniensis Canestrini y Fanzago, 1876 + +Heminothrus (Platynothrus) peltifer (Koch, 1839) +Metabelba (M.) papillipes (Nicolet, 1855) +Metabelba (M.) pulverulenta (Koch, 1839) +Adoristes (A.) ovatus poppei (Oudemans, 1906) +Liacarus (L.) coracinus coracinus (Koch, 1841) +Fosseremus laciniatus (Berlese, 1905) + + +Pantelozetes paolii (Oudemans, 1913) + +Autogneta (A.) longilamellata (Michael, 1885) +Microppia minus (Paoli, 1908) + + + + +Berniniella (B.) serratirostris hauseri (Mahunka, 1974) + +Dissorhina ornata (Oudemans, 1900) +Lauroppia fallax (Paoli, 1908) + +Oppiella (O.) nova (Oudemans, 1902) + + + + +Quadroppia (Q.) maritalis Lions, 1982 +Quadroppia (Q.) quadricarinata (Michael, 1885) + + + +Suctobelba trigona (Michael, 1888) +Suctobelbella (S.) acutidens (Forsslund, 1941) + + +Suctobelbella (S.) acutidens sarekensis (Forsslund, 1941) + + + + +Suctobelbella (S.) perforata (Strenzke, 1950) +Suctobelbella (S.) subcornigera (Forsslund, 1941) + + + + +Suctobelbella (S.) subcornigera vera (Moritz, 1964) + + +Suctobelbella (Flagrosuctobelba) alloenasuta Moritz, 1971 +Suctobelbila tuberculata Aoki, 1970 + +Carabodes (C.) labyrinthicus (Michael, 1879) +Tectocepheus minor Berlese, 1903 +Tectocepheus velatus (Michael, 1880) + + + + +Bipassalozetes (B.) perforatus (Berlese, 1910) +Scutovertex sculptus Michael, 1879 + + + +Eupelops tardus (Koch, 1835) + + +Peloptulus phaeonotus (Koch, 1844) + +Achipteria (A.) coleoptrata coleoptrata (Linnaeus, 1758) + +Tectoribates ornatus (Schuster, 1958)* +Ceratozetella (C.) sellnicki (Rajski, 1958) +Ceratozetes (C.) gracilis (Michael, 1884) + +Euzetes globulus (Nicolet, 1855) +Trichoribates (Latilamellobates) incisellus (Kramer, 1897) + + + +Chamobates (Xiphobates) voigtsi (Oudemans, 1902) +Punctoribates (P.) punctum (Koch, 1839) + + +Oribatula (O.) tibialis (Nicolet, 1855) + + +Oribatula (Zygoribatula) exilis (Nicolet, 1855) +Liebstadia (L.) pannonica pannonica (Willmann, 1951) + + +Liebstadia (L.) similis (Michael, 1888) +Scheloribates (S.) laevigatus (Koch, 1835) + + +Scheloribates (S.) pallidulus latipes (Koch, 1844) + + + +Protoribates (P.) capucinus capucinus Berlese, 1908 +Galumna (G.) obvia (Berlese, 1914) +Galumna (G.) rossica Sellnick, 1926* +Pergalumna nervosa (Berlese, 1914) +Pilogalumna tenuiclava (Berlese, 1908) + +

The species marked with asterisks (*) are new species for the Upper Silesian region.

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