Effects of microelements on soil nematode assemblages seven ...
Effects of microelements on soil nematode assemblages seven ...
Effects of microelements on soil nematode assemblages seven ...
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Science <str<strong>on</strong>g>of</str<strong>on</strong>g> the Total Envir<strong>on</strong>ment 320 (2004) 131–143<br />
<str<strong>on</strong>g>Effects</str<strong>on</strong>g> <str<strong>on</strong>g>of</str<strong>on</strong>g> <str<strong>on</strong>g>microelements</str<strong>on</strong>g> <strong>on</strong> <strong>soil</strong> <strong>nematode</strong> <strong>assemblages</strong> <strong>seven</strong><br />
years after c<strong>on</strong>taminating an agricultural field<br />
a, a b c a a<br />
Peter ´ Nagy *, Gabor ´ Bak<strong>on</strong>yi , Tom B<strong>on</strong>gers , Imre Kadar ´ ´ , Miklos ´ Fabian ´ ´ , Istvan ´ Kiss<br />
a Department <str<strong>on</strong>g>of</str<strong>on</strong>g> Zoology and Ecology, Szent Istvan ´ University, Godollo, ¨ ¨ ¨ Pater ´ K. u. 1 H-2103, Hungary<br />
bLaboratory<br />
for Nematology, Wageningen University, P.O. Box 8123, Wageningen 6700 ES, The Netherlands<br />
Research Institute for Soil Science and Agricultural Chemistry <str<strong>on</strong>g>of</str<strong>on</strong>g> the Hungarian Academy <str<strong>on</strong>g>of</str<strong>on</strong>g> Sciences, Herman O. u. 15,<br />
Budapest H-1025, Hungary<br />
c<br />
Abstract<br />
Received 28 January 2003; accepted 13 August 2003<br />
L<strong>on</strong>g-term effects <str<strong>on</strong>g>of</str<strong>on</strong>g> Cd, Cr, Cu, Se and Zn were studied 7 years after artificially c<strong>on</strong>taminating plots <str<strong>on</strong>g>of</str<strong>on</strong>g> an<br />
agricultural field <strong>on</strong> a calcareous chernozem <strong>soil</strong>.<str<strong>on</strong>g>Effects</str<strong>on</strong>g> <str<strong>on</strong>g>of</str<strong>on</strong>g> three to four different c<strong>on</strong>taminati<strong>on</strong> levels (originally<br />
y1 y1<br />
10, 30, 90 and 270 mg kg ) were studied.Nematode density was significantly reduced by 90 and 270 mg kg Se<br />
y1 y1<br />
as well as by 270 mg kg Cr, while 90 and 270 mg kg Se also reduced <strong>nematode</strong> generic richness.Maturity<br />
Index values (calculated for c-p 2–5 <strong>nematode</strong>s) c<strong>on</strong>sistently decreased with increasing Cr and Se c<strong>on</strong>centrati<strong>on</strong> and<br />
to a lesser extent in Zn plots as well.Structure Index showed decreasing trends in increasing Cr, Se and (to a lesser<br />
extent) in Zn treatments, while in Cd it shows a moderate increase.Distributi<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> c-p groups was negatively affected<br />
by the increasing Cr and Se c<strong>on</strong>centrati<strong>on</strong>, while in Zn plots, this decrease was not significant.Resp<strong>on</strong>se <str<strong>on</strong>g>of</str<strong>on</strong>g> feeding<br />
groups to polluti<strong>on</strong>s was similar to other parameters: Cr and Se caused significant changes toward the loss <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
variability.The proporti<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> the most sensitive omnivorous and predatory <strong>nematode</strong>s decreased clearly as a<br />
c<strong>on</strong>sequence <str<strong>on</strong>g>of</str<strong>on</strong>g> Cr and Se treatments.Zn polluti<strong>on</strong> also resulted in a slight decrease in this group, while Cd caused<br />
an increase.Nematode diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles showed a significant decrease in the plots <str<strong>on</strong>g>of</str<strong>on</strong>g> increased Cr and Se<br />
c<strong>on</strong>centrati<strong>on</strong>s, while increased c<strong>on</strong>centrati<strong>on</strong>s <str<strong>on</strong>g>of</str<strong>on</strong>g> Cu and Zn resulted in ambiguous effects.Besides providing evidence<br />
<strong>on</strong> the harmful effects <str<strong>on</strong>g>of</str<strong>on</strong>g> Cr and Se <strong>on</strong> a <strong>soil</strong> <strong>nematode</strong> assemblage, our results suggest that simultaneous analysis <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
Maturity Index, Structure Index and diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles provide a promising tool in nematological indicati<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> <strong>soil</strong><br />
polluti<strong>on</strong>.<br />
2003 Elsevier B.V. All rights reserved.<br />
Keywords: Soil polluti<strong>on</strong>; Microelement c<strong>on</strong>centrati<strong>on</strong> gradients; Nematodes; Maturity index; Structure index; Diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles;<br />
Heavy metals<br />
1. Introducti<strong>on</strong><br />
Increasing anthropogenic polluti<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> ecosystems<br />
by heavy metals and <str<strong>on</strong>g>microelements</str<strong>on</strong>g> means<br />
*Corresp<strong>on</strong>ding author.Fax: q36-28-410804.<br />
E-mail address: nagypeterdr@freemail.hu (P.Nagy).<br />
0048-9697/04/$ - see fr<strong>on</strong>t matter 2003 Elsevier B.V. All rights reserved.<br />
doi:10.1016/j.scitotenv.2003.08.006<br />
a growing hazard to living organisms, including<br />
mankind.In spite <str<strong>on</strong>g>of</str<strong>on</strong>g> this fact, data <strong>on</strong> l<strong>on</strong>g-term<br />
effects <str<strong>on</strong>g>of</str<strong>on</strong>g> heavy metals <strong>on</strong> <strong>soil</strong> biota are scarce to<br />
find.A unique l<strong>on</strong>g-term field experiment in Hungary<br />
has been providing opportunities since 1991<br />
to study l<strong>on</strong>g-term effects <str<strong>on</strong>g>of</str<strong>on</strong>g> plant micr<strong>on</strong>utrients,
132 P. Nagy et al. / Science <str<strong>on</strong>g>of</str<strong>on</strong>g> the Total Envir<strong>on</strong>ment 320 (2004) 131–143<br />
including heavy metals <strong>on</strong> <strong>soil</strong> biota, crops and<br />
their c<strong>on</strong>sumers (Kadar, ´ ´ 1994).<br />
Various crops grown at this site in previous<br />
years gave different resp<strong>on</strong>ses to the c<strong>on</strong>taminati<strong>on</strong><br />
(Kadar, ´ ´ 1995).As a general trend, high Se exposure<br />
had a str<strong>on</strong>g phytotoxic effect <strong>on</strong> all grown<br />
crop species (maize, carrot, potato, peas, beet,<br />
spinach, winter wheat and sunflower) and this<br />
effect did not disappear since the start <str<strong>on</strong>g>of</str<strong>on</strong>g> the<br />
experiment.Deleterious effects <str<strong>on</strong>g>of</str<strong>on</strong>g> Se <strong>on</strong> nodulati<strong>on</strong>,<br />
nitrogen-fixati<strong>on</strong> and arbuscular endomycorrhizal<br />
col<strong>on</strong>isati<strong>on</strong> were also detected 4 years after<br />
the applicati<strong>on</strong> (Biro´ et al., 1998).Cr proved to<br />
be toxic for plants in the first 6 years <str<strong>on</strong>g>of</str<strong>on</strong>g> the<br />
experiment.Thereafter, no toxic effect was found.<br />
Cd was not toxic during the first 4 years, but<br />
significantly decreased plant producti<strong>on</strong> from the<br />
5th year <str<strong>on</strong>g>of</str<strong>on</strong>g> the experiment until 2002.It is not<br />
clear whether this result is due to the increased<br />
toxicity <str<strong>on</strong>g>of</str<strong>on</strong>g> Cd or to the planting <str<strong>on</strong>g>of</str<strong>on</strong>g> more Cdsensitive<br />
plant species during these years.Cu and<br />
Zn caused no phytotoxic effects at all.<br />
Nematodes are <str<strong>on</strong>g>of</str<strong>on</strong>g>ten used as indicators <str<strong>on</strong>g>of</str<strong>on</strong>g> envir<strong>on</strong>mental<br />
disturbances, including heavy metal polluti<strong>on</strong><br />
(e.g.: Zullini and Peretti, 1986; Samoil<str<strong>on</strong>g>of</str<strong>on</strong>g>f,<br />
1987; B<strong>on</strong>gers, 1990; Korthals et al., 1996a).<br />
There are, however, <strong>on</strong>ly a limited number <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
studies <strong>on</strong> plant <str<strong>on</strong>g>microelements</str<strong>on</strong>g> under c<strong>on</strong>diti<strong>on</strong>s at<br />
least partly comparable to the present study regarding<br />
c<strong>on</strong>taminati<strong>on</strong> effects <strong>on</strong> <strong>nematode</strong> <strong>assemblages</strong>.In<br />
a microcosm study, Parmelee et al.<br />
(1993) found Cu to decrease <strong>nematode</strong> density in<br />
y1<br />
c<strong>on</strong>centrati<strong>on</strong>s above 200 mg kg .In a microplot<br />
experiment, no remarkable reducti<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> <strong>nematode</strong><br />
density was found in <strong>soil</strong>s polluted with 12 various<br />
<str<strong>on</strong>g>microelements</str<strong>on</strong>g>, except in the V plot, where the<br />
density was 25% <str<strong>on</strong>g>of</str<strong>on</strong>g> the c<strong>on</strong>trol (D.Sturhan,<br />
pers<strong>on</strong>al communicati<strong>on</strong>).<br />
More recently, Korthals et al. (1996b) carried<br />
out an experiment <strong>on</strong> the short-term toxic effects<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> Cd, Cu, Ni and Zn <strong>on</strong> <strong>nematode</strong> <strong>assemblages</strong><br />
in an acid sandy <strong>soil</strong> collected from a cultivated<br />
field.In their experiment, increased heavy metal<br />
c<strong>on</strong>centrati<strong>on</strong>s resulted in a significant decrease in<br />
density and Maturity Index (MI 2–5).This effect<br />
was significant at the c<strong>on</strong>centrati<strong>on</strong> level <str<strong>on</strong>g>of</str<strong>on</strong>g> 200<br />
y1 mg kg , which is comparable to the maximum<br />
initial c<strong>on</strong>centrati<strong>on</strong>s used in the present experi-<br />
ment.Cd applied in a c<strong>on</strong>centrati<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> 160 mg<br />
y1 kg as a maximum had no significant effect <strong>on</strong><br />
<strong>nematode</strong> density.In another paper, Korthals et al.<br />
(1996c) reported effects <str<strong>on</strong>g>of</str<strong>on</strong>g> an aged Cu polluti<strong>on</strong><br />
and pH levels <strong>on</strong> <strong>nematode</strong> assemblage <str<strong>on</strong>g>of</str<strong>on</strong>g> an<br />
experimental field polluted 10 years earlier.Cu<br />
effects <strong>on</strong> the Maturity Index (MI 2–5) showed a<br />
clear stepwise trend al<strong>on</strong>g a c<strong>on</strong>centrati<strong>on</strong> gradient<br />
y1<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> 250, 500, 750 kg ha and were largely<br />
enhanced by decreasing <strong>soil</strong> pH within a range <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
3.9–5.5.<br />
In a field site c<strong>on</strong>taminated l<strong>on</strong>g before sampling,<br />
Weiss and Larink (1991) found adverse<br />
effects <str<strong>on</strong>g>of</str<strong>on</strong>g> a mixture <str<strong>on</strong>g>of</str<strong>on</strong>g> heavy metals (am<strong>on</strong>g which<br />
Cd, Cr, Cu and Zn were also involved in this<br />
study) and sewage sludge.In terms <str<strong>on</strong>g>of</str<strong>on</strong>g> density,<br />
<strong>nematode</strong>s gave a positive reacti<strong>on</strong> to this interventi<strong>on</strong>,<br />
due to the high numbers <str<strong>on</strong>g>of</str<strong>on</strong>g> enrichment<br />
opportunists.However, c<strong>on</strong>taminati<strong>on</strong> markedly<br />
decreased omnivorous <strong>nematode</strong>s.In another study<br />
<strong>on</strong> applicati<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> sewage sludge c<strong>on</strong>taminated with<br />
various heavy metals, Georgieva et al. (2002)<br />
found Cu and Zn to have a negative effect <strong>on</strong><br />
various parameters <str<strong>on</strong>g>of</str<strong>on</strong>g> a <strong>nematode</strong> assemblage <strong>on</strong><br />
a sandy loam in England.Cu, Zn and ZnqCu<br />
decreased tax<strong>on</strong> richness and MI, affected c-p<br />
group and feeding group distributi<strong>on</strong>.<br />
In our previous study (Nagy, 1999), certain<br />
elements were found to affect <strong>nematode</strong> <strong>assemblages</strong><br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> the same experimental field.Cr and<br />
especially Se had a negative influence while Zn<br />
appeared to stimulate <strong>nematode</strong>s in terms <str<strong>on</strong>g>of</str<strong>on</strong>g> density,<br />
generic richness and Maturity Index 6 years<br />
after the c<strong>on</strong>taminati<strong>on</strong>.No effects were found,<br />
however, for Al, As, Ba, Cu, Hg, Mo, Ni, Pb and<br />
Sr.Regarding l<strong>on</strong>g-term observati<strong>on</strong>s (Bak<strong>on</strong>yi et<br />
al., 2003), Cr and especially Se showed harmful<br />
effects even 10 years after the c<strong>on</strong>taminati<strong>on</strong>,<br />
while the advantageous effects <str<strong>on</strong>g>of</str<strong>on</strong>g> Zn disappeared.<br />
However, remarkable fluctuati<strong>on</strong>s have been found<br />
in the compositi<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> <strong>nematode</strong> assemblage am<strong>on</strong>g<br />
the studied years.<br />
The aim <str<strong>on</strong>g>of</str<strong>on</strong>g> our study was to evaluate whether<br />
different doses <str<strong>on</strong>g>of</str<strong>on</strong>g> Cd, Cr, Cu, Se and Zn had<br />
recognisable effects <strong>on</strong> the structure <str<strong>on</strong>g>of</str<strong>on</strong>g> the <strong>nematode</strong><br />
<strong>assemblages</strong> in the calcareous chernozem <strong>soil</strong><br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> an agricultural field 7 years after applicati<strong>on</strong>.<br />
Particular emphasis was given to applying coen-
P. Nagy et al. / Science <str<strong>on</strong>g>of</str<strong>on</strong>g> the Total Envir<strong>on</strong>ment 320 (2004) 131–143<br />
ological methods in order to see whether various<br />
nematological indicators, such as tax<strong>on</strong> richness,<br />
MI, SI, c-p group distributi<strong>on</strong> and feeding dominance<br />
lead to similar c<strong>on</strong>clusi<strong>on</strong>s regarding the<br />
given disturbance.<br />
2. Materials and methods<br />
Soil samples were collected from the experimental<br />
field <str<strong>on</strong>g>of</str<strong>on</strong>g> Research Institute for Soil Science<br />
and Agricultural Chemistry (RISSAC) <str<strong>on</strong>g>of</str<strong>on</strong>g> the Hungarian<br />
Academy <str<strong>on</strong>g>of</str<strong>on</strong>g> Sciences at Nagyhorcsok, ¨ ¨ Hungary<br />
(UTM-code: CT 00).Soil characteristics and<br />
experimental design are detailed by Kadar ´ ´ (1994,<br />
1995).Therefore, <strong>on</strong>ly some <str<strong>on</strong>g>of</str<strong>on</strong>g> the most important<br />
<strong>soil</strong> characteristics are menti<strong>on</strong>ed here.The <strong>soil</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
the experimental plots is a calcareous loamy chernozem<br />
with medium to deep humus layer formed<br />
<strong>on</strong> loess.Exchangeable cati<strong>on</strong>s comprise <str<strong>on</strong>g>of</str<strong>on</strong>g> 80%<br />
Ca, 16% Mg, 3% K, 1% Na.Ss40 meqy100 g,<br />
water soluble saltss1 meqy100 g, pH s7.4.<br />
KCl<br />
( )<br />
Particle distributi<strong>on</strong> in percentage <str<strong>on</strong>g>of</str<strong>on</strong>g> mineral c<strong>on</strong>tent<br />
was as follows.Coarse sand: 0.8%, fine sand:<br />
15.7%, silt: 60.4%, clay: 23.1%. Soil organic<br />
matter c<strong>on</strong>tent was approximately 3%, with a C:N<br />
ratio <str<strong>on</strong>g>of</str<strong>on</strong>g> 8–8.5. Experimental plots were polluted<br />
with single <str<strong>on</strong>g>microelements</str<strong>on</strong>g> given as CdSO ,<br />
4<br />
K CrO , CuSO , Na SeO and ZnSO , respective-<br />
2 4 4 2 3 4<br />
ly.C<strong>on</strong>taminants were ploughed into the <strong>soil</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
the plots in April 1991.Initial total element doses<br />
y1<br />
were 90, 270 and 810 kg ha .These doses were<br />
y1 y1<br />
roughly equal to 30 mg kg , 90 mg kg and<br />
y1<br />
270 mg kg , respectively, based <strong>on</strong> the typical<br />
<strong>soil</strong> density value <str<strong>on</strong>g>of</str<strong>on</strong>g> 1.5 and the average plough<br />
layer <str<strong>on</strong>g>of</str<strong>on</strong>g> 0.2 m. In the case <str<strong>on</strong>g>of</str<strong>on</strong>g> Cd and Se, an<br />
y1<br />
additi<strong>on</strong>al treatment <str<strong>on</strong>g>of</str<strong>on</strong>g> 10 mg kg in total c<strong>on</strong>-<br />
centrati<strong>on</strong> was also applied.Fertilisers were given<br />
y1 y1<br />
at c<strong>on</strong>centrati<strong>on</strong>s <str<strong>on</strong>g>of</str<strong>on</strong>g> Ns100 kg ha year (as<br />
y1 y1<br />
NH4NO 3), P2O5s100 kg ha year , Ks100<br />
y1 y1<br />
kg ha year .P, K and half <str<strong>on</strong>g>of</str<strong>on</strong>g> the N dose were<br />
applied before the autumn tillage, while the sec<strong>on</strong>d<br />
half <str<strong>on</strong>g>of</str<strong>on</strong>g> N was applied in early spring.The above<br />
treatments are aimed to assess the effects <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
<str<strong>on</strong>g>microelements</str<strong>on</strong>g> <strong>on</strong> crops grown under c<strong>on</strong>diti<strong>on</strong>s<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> regular cropping systems.No pesticides were<br />
applied, weed c<strong>on</strong>trol was performed by manual<br />
cultivati<strong>on</strong>.Experimental units were arranged in a<br />
split-plot design encompassing an area <str<strong>on</strong>g>of</str<strong>on</strong>g> 21 m2 133<br />
per plot.Each plot was surrounded by paths <str<strong>on</strong>g>of</str<strong>on</strong>g> 1<br />
m width.The two replicates were set up as two<br />
adjacent blocks <str<strong>on</strong>g>of</str<strong>on</strong>g> plots.Both replicates <str<strong>on</strong>g>of</str<strong>on</strong>g> each<br />
treatment and two c<strong>on</strong>trol plots were sampled <strong>on</strong><br />
30 June 1998, 7 years after the c<strong>on</strong>taminati<strong>on</strong>.<br />
The NH4-acetateqEDTA soluble (mobile) fracti<strong>on</strong><br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> element was determined according to Lak-<br />
anen and Ervio ¨ (1971).These analyses were<br />
performed in 1991, 1992, 1994 and 1997.Sunflower<br />
(Helianthus annuus L.) was grown in the<br />
experimental field in 1998.By the date <str<strong>on</strong>g>of</str<strong>on</strong>g> sampling<br />
it was close to flowering.<br />
For nematological analysis composite samples<br />
(20 subsampleyplot) <str<strong>on</strong>g>of</str<strong>on</strong>g> approximately 300–400 g<br />
<strong>soil</strong> were taken using a <strong>soil</strong> corer <str<strong>on</strong>g>of</str<strong>on</strong>g> 2 cm in<br />
diameter.The top 10 cm <str<strong>on</strong>g>of</str<strong>on</strong>g> <strong>soil</strong> was sampled.<br />
Nematodes were extracted from <strong>soil</strong> using Cobb’s<br />
decanting and sieving method (modified according<br />
to s’Jacob and van Bezooijen, 1984), and enumerated<br />
(typically approx.20% <str<strong>on</strong>g>of</str<strong>on</strong>g> the obtained suspensi<strong>on</strong>).Then<br />
after fixing with 80–90 8C hot<br />
formalin (cc.8%), samples were stored until further<br />
processing, during which at least 150 specimens<br />
per sample were identified, possibly to genus<br />
level.This process resulted in <strong>nematode</strong> tax<strong>on</strong><br />
richness values (i.e. number <str<strong>on</strong>g>of</str<strong>on</strong>g> <strong>nematode</strong> taxa)<br />
and coenological data for each sample. (In cases<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> the maximum c<strong>on</strong>centrati<strong>on</strong> Se treatment where<br />
this amount <str<strong>on</strong>g>of</str<strong>on</strong>g> <strong>nematode</strong>s was not available, samples<br />
were processed totally.) As a result, c-p group<br />
distributi<strong>on</strong> patterns and Maturity Index values<br />
were calculated for <strong>nematode</strong> <strong>assemblages</strong> in each<br />
sample according to B<strong>on</strong>gers (1990).Korthals et<br />
al. (1996a) indicated that omitting c-p 1 <strong>nematode</strong>s<br />
that results in a ‘MI (2–5)’ value gives a much<br />
better resp<strong>on</strong>se to disturbances than the MI<br />
(including c-p 1).The reas<strong>on</strong> for this is that taxa<br />
in c-p 1 group react to <strong>soil</strong> organic enrichment as<br />
well.When calculating c-p distributi<strong>on</strong>, intermediate<br />
taxa <str<strong>on</strong>g>of</str<strong>on</strong>g> c-p 3 were assigned to the c<strong>on</strong>glomerate<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> c-p 4–5 (persister <strong>nematode</strong>s).However,<br />
representatives <str<strong>on</strong>g>of</str<strong>on</strong>g> the c-p 3 group occurred in <strong>on</strong>ly<br />
27% <str<strong>on</strong>g>of</str<strong>on</strong>g> the samples where their average proporti<strong>on</strong><br />
was as low as 0.75%. Structure Index (SI) values<br />
(Ferris et al., 2001) were also computed.SI is a<br />
measure <str<strong>on</strong>g>of</str<strong>on</strong>g> the stabile and structured status <str<strong>on</strong>g>of</str<strong>on</strong>g> a<br />
<strong>soil</strong> <strong>nematode</strong> community.It is based <strong>on</strong> the<br />
proporti<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> feeding types combined with their
134 P. Nagy et al. / Science <str<strong>on</strong>g>of</str<strong>on</strong>g> the Total Envir<strong>on</strong>ment 320 (2004) 131–143<br />
appropriate guild weightings.High value shows a<br />
more structured community, while low SI is a sign<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> ‘basal c<strong>on</strong>diti<strong>on</strong>s’, i.e. previous disturbance.<br />
Nematode taxa were assigned to feeding types<br />
sensu Yeates et al. (1993).<br />
Data were analysed using <strong>on</strong>e-way ANOVA to<br />
discover significant differences in <strong>nematode</strong> density<br />
as well as <strong>nematode</strong> generic richness values.<br />
For density values, correlati<strong>on</strong> was also calculated<br />
al<strong>on</strong>g the c<strong>on</strong>centrati<strong>on</strong> gradient.The significant<br />
differences in c-p group distributi<strong>on</strong>s were tested<br />
2<br />
with standard Pears<strong>on</strong> x test.<br />
Most <str<strong>on</strong>g>of</str<strong>on</strong>g> the classical diversity indices have the<br />
serious disadvantage <str<strong>on</strong>g>of</str<strong>on</strong>g> varying in sensitivity to<br />
the density <str<strong>on</strong>g>of</str<strong>on</strong>g> the comm<strong>on</strong> and rare species.To<br />
overcome this problem, Patil and Taillie (1979)<br />
suggested the use <str<strong>on</strong>g>of</str<strong>on</strong>g> the community diversity<br />
pr<str<strong>on</strong>g>of</str<strong>on</strong>g>ile.The community diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>ile outlines<br />
scale-dependent diversity <str<strong>on</strong>g>of</str<strong>on</strong>g> a community.Some<br />
values <str<strong>on</strong>g>of</str<strong>on</strong>g> the diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>ile are related to classical<br />
diversity indexes, namely at as0 equal to<br />
lgS, where Ssnumber <str<strong>on</strong>g>of</str<strong>on</strong>g> species in the community,<br />
at as1 equal to the value <str<strong>on</strong>g>of</str<strong>on</strong>g> the Shann<strong>on</strong><br />
index etc.Tothmeresz ´ ´ ´ (1993) developed new<br />
diversity functi<strong>on</strong> families and the computer program<br />
package DivOrd.In this study, DivOrd 1.50<br />
was used to calculate diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles.Diversity<br />
pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles between scale parameters 0–40 <str<strong>on</strong>g>of</str<strong>on</strong>g> all plots<br />
were generated.The low values refer to the rare<br />
taxa, while the higher scale parameters depict the<br />
status <str<strong>on</strong>g>of</str<strong>on</strong>g> the more frequent <strong>on</strong>es.Above as4, the<br />
curves were more or less parallel to each other,<br />
therefore, diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles between as0 and 4<br />
are presented.Significant differences can be found<br />
am<strong>on</strong>g 2 curves when these do not cross each<br />
other and Renyi ´ diversity values for the points <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
the curves differ at Ps5%.In this study, curves<br />
have been compared with an increment <str<strong>on</strong>g>of</str<strong>on</strong>g> 0.5<br />
al<strong>on</strong>g the range <str<strong>on</strong>g>of</str<strong>on</strong>g> as0–4.<br />
3. Results<br />
The mobile fracti<strong>on</strong>s <str<strong>on</strong>g>of</str<strong>on</strong>g> the target element in<br />
the studied plots are shown in Table 1.These data<br />
show that the actual available values differed<br />
(<str<strong>on</strong>g>of</str<strong>on</strong>g>ten remarkably) from the originally added total<br />
values (depending <strong>on</strong> the pollutant).However, a<br />
trend <str<strong>on</strong>g>of</str<strong>on</strong>g> increasing c<strong>on</strong>centrati<strong>on</strong>s over the dose<br />
gradient was still well recognisable 6 years after<br />
the c<strong>on</strong>taminati<strong>on</strong>.<br />
In general, increased microelement c<strong>on</strong>centrati<strong>on</strong>s<br />
decreased <strong>nematode</strong> density in all cases<br />
except Cu.Nematode density was significantly<br />
lower than the c<strong>on</strong>trol in the Se treatments at 90<br />
y1<br />
and 270 mg kg c<strong>on</strong>centrati<strong>on</strong> and in the plots<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> the highest Cr c<strong>on</strong>taminati<strong>on</strong>, 270 mg kgy1 (Table 2).There were significant correlati<strong>on</strong>s<br />
between microelement c<strong>on</strong>centrati<strong>on</strong> and <strong>nematode</strong><br />
density in Cr, Se and Zn treatments (P-0.05).<br />
Nematode tax<strong>on</strong> richness values were decreased<br />
y1<br />
significantly by the 90 and 270 mg kg Se<br />
treatment (Table 3).The increasing c<strong>on</strong>centrati<strong>on</strong>s<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> the other elements did not correlate with this<br />
parameter.However, this could be due to the<br />
relatively low richness and high S.D. values in<br />
certain cases (Cr, Cu).<br />
Nematode MI (2–5) values (Table 4) were<br />
c<strong>on</strong>sistently lower in the Cr treatments <str<strong>on</strong>g>of</str<strong>on</strong>g> the 270<br />
y1 mg kg c<strong>on</strong>centrati<strong>on</strong> and in the Se treatments<br />
y1<br />
from 30 mg kg <strong>on</strong>wards, according to a clear<br />
dose-related pattern.The low number <str<strong>on</strong>g>of</str<strong>on</strong>g> <strong>nematode</strong>s<br />
y1<br />
extracted from the 270 mg kg Se-plots made it<br />
impossible to calculate MI for this treatment.For<br />
Zn, a slight decrease appeared with the increasing<br />
c<strong>on</strong>centrati<strong>on</strong>, while in Cd samples there was a<br />
little increase in MI toward the highest treatment<br />
investigated.No trend could be observed in Cutreated<br />
samples.<br />
The c-p group distributi<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> samples was also<br />
significantly affected by Cr and Se polluti<strong>on</strong> levels<br />
(Table 5).Cu c<strong>on</strong>taminati<strong>on</strong> induced no c<strong>on</strong>sistent<br />
resp<strong>on</strong>se.This parameter was not sensitive to Cd<br />
and Zn treatment.The c-p 3–5 <strong>nematode</strong>s occurred<br />
y1<br />
in relatively high proporti<strong>on</strong> in 270 mg kg Cd<br />
and Cu samples.<br />
Structure Index (SI) values are displayed in<br />
Table 6.This parameter shows clear decreasing<br />
trends in Cr, Se and (to a lesser extent) in Zn<br />
treatments, while in Cd it shows a moderate<br />
increase.In the values <str<strong>on</strong>g>of</str<strong>on</strong>g> the Cu treatments there<br />
is no obvious trend.<br />
Feeding group dominance data are shown in<br />
Table 7.Regarding bacterial feeders, Cr and Se<br />
more or less increased, Cd, Cu and Zn decreased<br />
this parameter compared to the c<strong>on</strong>trol.Fungal<br />
feeders were enhanced by all treatments, except
P. Nagy et al. / Science <str<strong>on</strong>g>of</str<strong>on</strong>g> the Total Envir<strong>on</strong>ment 320 (2004) 131–143<br />
Table 1<br />
The NH4-acetateqEDTA soluble (mobile) c<strong>on</strong>centrati<strong>on</strong> values al<strong>on</strong>g the microelement gradients as measured in the subsequent<br />
analyses<br />
Element, year C<strong>on</strong>trol 10 mg kg y1 30 mg kg y1 90 mg kg y1 270 mg kg y1<br />
Cd<br />
1991 – 14.0 27.0 96.0 270.0<br />
1992 – 0 18.0 62.0 228.0<br />
1994 – 0 14.0 44.0 164.0<br />
1997 – 0 26.8 84.7 190.0<br />
2000<br />
Cr<br />
– 0 14.0 44.0 124.0<br />
1991 0 – 1.0 3.0 9.0<br />
1992 0 – 2.0 5.0 10.0<br />
1994 0 – 1.0 2.0 4.0<br />
1997 0.2 – 0.45 0.77 1.4<br />
2000<br />
Cu<br />
0 – 0.4 0.9 1.6<br />
1991 9.0 – 29.0 47.0 200.0<br />
1992 4.0 – 34.0 94.0 270.0<br />
1994 4.0 – 23.0 65.0 192.0<br />
1997 6.0 – 19.4 54.1 133.0<br />
2000<br />
Se<br />
4.0 – 20.0 44.0 128.0<br />
1991 – 1.0 6.0 34.0 84.0<br />
1992 – 0 7.0 66.0 81.0<br />
1994 – 0 8.0 33.0 89.0<br />
1997 – 0.5 1.56 9.32 36.0<br />
2000<br />
Zn<br />
– 0 2.0 4.0 11.0<br />
1991 1.0 – 22.0 66.0 120.0<br />
1992 3.0 – 29.0 68.0 213.0<br />
1994 1.0 – 19.0 44.0 147.0<br />
1997 2.0 – 22.0 53.0 143.0<br />
2000 2.0 – 16.0 37.0 85.0<br />
–: no such treatment.<br />
Table 2<br />
y1<br />
<str<strong>on</strong>g>Effects</str<strong>on</strong>g> <str<strong>on</strong>g>of</str<strong>on</strong>g> pollutant c<strong>on</strong>centrati<strong>on</strong> gradients <strong>on</strong> <strong>nematode</strong> density; average specimenU100 g <strong>soil</strong> ("S.D.)<br />
Element 0mgkg y1 10 mg kg y1 30 mg kg y1 90 mg kg y1 270 mg kg y1<br />
C<strong>on</strong>trol 1275.0 ("1104) – – – –<br />
Cd – x 1105.0 ("824) 937.5 ("735) 815.0 ("613)<br />
Cr x – 1055.0 ("754) 834.5 ("724) 484.5 ("267)*<br />
Cu x – 981.0 ("501) 1184.0 ("945) 1063.0 ("987)<br />
Se – 1160.0 ("587) 954.0 ("861) 422.5 ("370)* 20.0 ("3.5)**<br />
Zn x – 1150.0 ("1033) 1021.0 ("648) 882.5 ("628)<br />
–: no such treatment, x: not sampled, *: significant decrease in respective values, P-0.05, **: significant decrease in respective<br />
value, P-0.01.<br />
135
136 P. Nagy et al. / Science <str<strong>on</strong>g>of</str<strong>on</strong>g> the Total Envir<strong>on</strong>ment 320 (2004) 131–143<br />
Table 3<br />
<str<strong>on</strong>g>Effects</str<strong>on</strong>g> <str<strong>on</strong>g>of</str<strong>on</strong>g> pollutant c<strong>on</strong>centrati<strong>on</strong> gradients <strong>on</strong> <strong>nematode</strong> tax<strong>on</strong> richness; average values ("S.D.)<br />
Element 0mgkg y1 10 mg kg y1 30 mg kg y1 90 mg kg y1 270 mg kg y1<br />
C<strong>on</strong>trol 19.0 ("2.8) – – – –<br />
Cd – x 22.5 ("2.1) 17.0 ("y) 18.0 (0)<br />
Cr x – 20.5 ("0.7) 16.0 (0) 15.0 ("2.8)<br />
Cu x – 21.0 ("1.4) 15.5 ("0.7) 17.5 ("5.0)<br />
Se – 16.5 ("2.1) 16.0 ("2.8) 12.5 ("2.1)* 3. 0 ("1.4)*<br />
Zn x – 18.5 ("2.1) 18.5 ("0.7) 18.5 ("2.1)<br />
–: no such treatment, x: not sampled, y: no data available, *: significant decrease in respective values, P-5%.<br />
the maximum Se level.As for predators and<br />
omnivores, this group was very sensitive to high<br />
Cr and Se levels, while in other treatments showed<br />
ratios comparable to the c<strong>on</strong>trol.<br />
Bacterial feeders and fungal feeders being differently<br />
sensitive to heavy metal and microelement<br />
polluti<strong>on</strong>, BFyFF ratio was displayed separately in<br />
Table 8.Based <strong>on</strong> this parameter, bacterial feeders<br />
became dominant under higher Se c<strong>on</strong>centrati<strong>on</strong>s<br />
y1<br />
(90 and 270 mg kg ), while increasing Cd and<br />
Cu levels favoured fungal feeders.<br />
Diversity-pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles for <strong>nematode</strong> samples were<br />
obviously affected by some <str<strong>on</strong>g>of</str<strong>on</strong>g> the treatments.Cd<br />
polluti<strong>on</strong> did not result in a clear trend <str<strong>on</strong>g>of</str<strong>on</strong>g> diversity<br />
pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles (Fig.1).The lowest level <str<strong>on</strong>g>of</str<strong>on</strong>g> Cr seemed<br />
to have slightly stimulated <strong>nematode</strong> diversity<br />
while the two highest <strong>on</strong>es resulted in a significant<br />
decrease, though there was an adverse trend<br />
between these latter: the highest level <str<strong>on</strong>g>of</str<strong>on</strong>g> c<strong>on</strong>taminant<br />
was more depressive for the rare taxa than<br />
for the most comm<strong>on</strong> <strong>on</strong>es (Fig.2).In the Cu<br />
treated plots, the highest level treatment resulted<br />
in lower diversity values than the others (except<br />
for the rare taxa) and there was an overall trend<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> decrease with increasing c<strong>on</strong>centrati<strong>on</strong> (Fig.3).<br />
Table 4<br />
<str<strong>on</strong>g>Effects</str<strong>on</strong>g> <str<strong>on</strong>g>of</str<strong>on</strong>g> pollutant c<strong>on</strong>centrati<strong>on</strong> gradients <strong>on</strong> Maturity Index (2–5); average values ("S.D.)<br />
For Se treatments, a slight to moderate polluti<strong>on</strong><br />
y1<br />
(up to 90 mg kg ) kept diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles around<br />
y1<br />
the c<strong>on</strong>trol level and <strong>on</strong>ly 270 mg kg caused a<br />
massively significant decrease in diversity (Fig.<br />
4).The Zn levels resulted in a remarkable pattern:<br />
no significant differences were found for the whole<br />
diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>ile for most treatments, but the highest<br />
c<strong>on</strong>centrati<strong>on</strong> slightly increased diversity compared<br />
to the two lowest <strong>on</strong>es for rare taxa, while<br />
the frequent taxa appeared to become much less<br />
diverse (Fig.5).<br />
4. Discussi<strong>on</strong><br />
<str<strong>on</strong>g>Effects</str<strong>on</strong>g> <str<strong>on</strong>g>of</str<strong>on</strong>g> Cd <strong>on</strong> <strong>soil</strong> <strong>nematode</strong>s were not<br />
significant in terms <str<strong>on</strong>g>of</str<strong>on</strong>g> most parameters.Only BFy<br />
FF ratio was decreased by the increasing c<strong>on</strong>centrati<strong>on</strong><br />
and the diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>ile seemed to benefit<br />
y1<br />
from the 30 mg kg treatment, i.e. LOEC (Low-<br />
est Observable Effect C<strong>on</strong>centrati<strong>on</strong>) value <str<strong>on</strong>g>of</str<strong>on</strong>g> Cd<br />
under present c<strong>on</strong>diti<strong>on</strong>s should be above the<br />
y1<br />
theoretical level <str<strong>on</strong>g>of</str<strong>on</strong>g> 270 mg kg applied as max-<br />
imum rate (In available c<strong>on</strong>centrati<strong>on</strong> it was equal<br />
y1<br />
to approx.190 mg kg ).This finding is in<br />
agreement with Kammenga et al. (1994) who<br />
Element 0mgkg y1 10 mg kg y1 30 mg kg y1 90 mg kg y1 270 mg kg y1<br />
C<strong>on</strong>trol 2.45 ("0.11) – – – –<br />
Cd – x 2.25 ("0.13) 2.3 ("y) 2.57 ("0.09)<br />
Cr x – 2.33 ("0.13) 2.22 ("0.18) 2.03 ("0.04)<br />
Cu x – 2.34 ("0.1) 2.11 ("0.06) 2.42 ("0.18)<br />
Se – 2.52 ("0.06) 2.19 ("0.08) 2.05 ("0.01) n.c.<br />
Zn x – 2.42 ("0.05) 2.39 ("0.04) 2.33 ("0.13)<br />
–: no such treatment, x: not sampled, y: no data available, n.c.: not calculable due to the too low <strong>nematode</strong> density.
P. Nagy et al. / Science <str<strong>on</strong>g>of</str<strong>on</strong>g> the Total Envir<strong>on</strong>ment 320 (2004) 131–143<br />
Table 5<br />
<str<strong>on</strong>g>Effects</str<strong>on</strong>g> <str<strong>on</strong>g>of</str<strong>on</strong>g> pollutant c<strong>on</strong>centrati<strong>on</strong> gradients <strong>on</strong> the c-p group distributi<strong>on</strong> patterns <str<strong>on</strong>g>of</str<strong>on</strong>g> n<strong>on</strong>-plant feeding <strong>nematode</strong>s; average values<br />
Element 0mgkg y1 10 mg kg y1 30 mg kg y1 90 mg kg y1 270 mg kg y1<br />
C<strong>on</strong>trol<br />
c-p 1(%) 3. 5 – – – –<br />
c-p 2(%) 79.7 – – – –<br />
c-p 3–5(%)<br />
Cd<br />
16.9 – – – –<br />
c-p 1(%) – x 4.0 2.4 1.1<br />
c-p 2(%) – x 85.8 87.2 79.2<br />
c-p 3–5(%) – x 10.1 10.4 19.9<br />
P-<br />
Cr<br />
n.s. n.s. n.s.<br />
c-p 1(%) x – 2.0 0.7 0.7<br />
c-p 2(%) x – 86.0 90.0 98.8<br />
c-p 3–5(%) x – 12.3 9.0 0.8<br />
P-<br />
Cu<br />
n.s. 0.01 0.001<br />
c-p 1(%) x – 1.7 1.3 0.9<br />
c-p 2(%) x – 85.9 94.8 83.0<br />
c-p 3–5(%) x – 12.2 4.3 16.1<br />
P-<br />
Se<br />
n.s. 0.001 n.s.<br />
c-p 1(%) – 0.8 1.3 6.0 n.c.<br />
c-p 2(%) – 81.2 92.6 92.6 n.c.<br />
c-p 3–5(%) – 18.2 5.9 1.5 n.c.<br />
P-<br />
Zn<br />
n.s. 0.01 0.001<br />
c-p 1(%) x – 0.9 1.4 1.6<br />
c-p 2(%) x – 83.9 84.6 86.3<br />
c-p 3–5(%) x – 15.2 14.2 12.0<br />
P- n.s. n.s. n.s.<br />
–: no such treatment, x: not sampled, n.c.: not calculable due to the too low <strong>nematode</strong> density, P-significance level compared<br />
2<br />
to the c<strong>on</strong>trol resulting from the x test, n.s.: n<strong>on</strong>-significant.<br />
found <strong>nematode</strong>s to be relatively insensitive to Cd,<br />
compared to other <strong>soil</strong> animals.Though the cited<br />
study was carried out in vitro with a short-term<br />
Table 6<br />
<str<strong>on</strong>g>Effects</str<strong>on</strong>g> <str<strong>on</strong>g>of</str<strong>on</strong>g> pollutant c<strong>on</strong>centrati<strong>on</strong> gradients <strong>on</strong> SI; average values ("S.D.)<br />
Element 0mgkg y1 10 mg kg y1 30 mg kg y1 90 mg kg y1 270 mg kg y1<br />
C<strong>on</strong>trol 52.69("7.8) – – – –<br />
Cd – x 35.04 ("13.3) 40.59 ("y) 59.42 ("4.2)<br />
Cr x – 42.64 ("11.3) 31.01 ("20.7) 10.12 (0)<br />
Cu x – 47.24 ("10.3) 26.52 ("6.0) 49.58 ("13.3)<br />
Se – 56.93("3.6) 28.58 ("9.4) 9.12 ("0.8) n.c.<br />
Zn x – 50.60 ("3.7) 48.49 ("2.0) 43.16 ("10.8)<br />
–: no such treatment, x: not sampled, y: no data available, n.c. not calculable due to the too low <strong>nematode</strong> density.<br />
137<br />
aspect, it included 12 <strong>nematode</strong> species <str<strong>on</strong>g>of</str<strong>on</strong>g> various<br />
feeding and life-strategy groups, which made its<br />
c<strong>on</strong>clusi<strong>on</strong>s more realistic than usual single-species
138 P. Nagy et al. / Science <str<strong>on</strong>g>of</str<strong>on</strong>g> the Total Envir<strong>on</strong>ment 320 (2004) 131–143<br />
Table 7<br />
<str<strong>on</strong>g>Effects</str<strong>on</strong>g> <str<strong>on</strong>g>of</str<strong>on</strong>g> pollutant c<strong>on</strong>centrati<strong>on</strong> gradients <strong>on</strong> feeding group ratios; average percentage values<br />
Element 0mgkg y1 10 mg kg y1 30 mg kg y1 90 mg kg y1 270 mg kg y1<br />
C<strong>on</strong>trol<br />
BF 34.4 – – – –<br />
FF 21.9 – – – –<br />
PqO 9. 1 – – – –<br />
PF<br />
Cd<br />
34.6 – – – –<br />
BF – x 42.5 36.0 28.7<br />
FF – x 30.3 29.1 35.2<br />
PqO – x 6.5 6.3 13.8<br />
PF – x 20.7 28.6 22.3<br />
P- 0.01 n.s. 0.01<br />
Cr x –<br />
BF x – 32.8 47.2 43.2<br />
FF x – 34.3 36.9 41.1<br />
PqO x – 7.2 5.0 0.6<br />
PF 25.7 10.9 15.0<br />
P-<br />
Cu<br />
0.05 0.001 0.001<br />
BF – 34.2 29.1 22.5<br />
FF x – 30.0 32.5 33.9<br />
PqO x – 7.6 2.7 7.2<br />
PF x – 28.2 35.7 36.3<br />
P-<br />
Se<br />
n.s. 0.05 0.05<br />
BF – 32.3 39.8 56.2 n.c.<br />
FF – 27.1 30.6 30.6 n.c.<br />
PqO – 12.1 4.1 1.0 n.c.<br />
PF – 28.4 25.5 12.2 n.c.<br />
P-<br />
Zn<br />
n.s. 0.05 0.001<br />
BF x – 21.2 26.8 20.0<br />
FF x – 31.8 31.7 31.1<br />
PqO x – 7.2 7.9 6.0<br />
PF x – 39.7 33.7 42.9<br />
P- 0.05 n.s. 0.01<br />
BF: bacterial feeders, FF: fungal feeders, PqO: predatorsqomnivores, PF: plant feeders, –: no such treatment, x: not sampled,<br />
2<br />
n.c.: not calculable due to the too low <strong>nematode</strong> density, P-significance level compared to the c<strong>on</strong>trol resulting from the x test,<br />
n.s.: n<strong>on</strong>-significant.<br />
laboratory tests.Korthals et al.(1996b) also found<br />
<strong>nematode</strong> fauna uneffected by Cd up to 160 mg<br />
y1 kg (though in a short-term study).<br />
<str<strong>on</strong>g>Effects</str<strong>on</strong>g> <str<strong>on</strong>g>of</str<strong>on</strong>g> Cr <strong>on</strong> <strong>nematode</strong> <strong>assemblages</strong> have so<br />
far been paid little attenti<strong>on</strong> to.Yeates et al.(1995)<br />
presented results <strong>on</strong> mixed effects <str<strong>on</strong>g>of</str<strong>on</strong>g> As, Cr and<br />
Cu but their data are hard to compare with ours<br />
due to the different approach (multi- vs.singleelement<br />
treatment).In his study D.Sturhan (per-<br />
s<strong>on</strong>al communicati<strong>on</strong>) showed an MI-decrease for<br />
Cr.In our present experiment, Cr had still a<br />
negative impact <strong>on</strong> <strong>nematode</strong> <strong>assemblages</strong>, similarly<br />
to earlier results (Nagy, 1999).Increasing<br />
c<strong>on</strong>centrati<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> this element affected most <str<strong>on</strong>g>of</str<strong>on</strong>g> the<br />
parameters applied to indicate disturbance <strong>on</strong> <strong>nematode</strong><br />
assemblage.Density, tax<strong>on</strong> richness, MI, SI,<br />
PqO ratio and proporti<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> c-p 3–5 <strong>nematode</strong>s<br />
all clearly decreased al<strong>on</strong>g the c<strong>on</strong>centrati<strong>on</strong> gra-
P. Nagy et al. / Science <str<strong>on</strong>g>of</str<strong>on</strong>g> the Total Envir<strong>on</strong>ment 320 (2004) 131–143<br />
Table 8<br />
<str<strong>on</strong>g>Effects</str<strong>on</strong>g> <str<strong>on</strong>g>of</str<strong>on</strong>g> pollutant c<strong>on</strong>centrati<strong>on</strong> gradients <strong>on</strong> bacterial feederyfungal feeder ratios; average values ("S.D.)<br />
Element 0mgkg y1 10 mg kg y1 30 mg kg y1 90 mg kg y1 270 mg kg y1<br />
C<strong>on</strong>trol 1.90 ("1.4) – – – –<br />
Cd – x 1.52 ("0.6) 1.24 ("y) 0.82 ("0.1)<br />
Cr x – 1.00 ("0.3) 1.29 ("0.2) 1.14 ("0.5)<br />
Cu x – 1.14 ("0.2) 0.92 ("0.3) 0.66 ("0.0)<br />
Se – 1.19 ("0.46) 1.36 ("0.2) 1.95("0.6) n.c.<br />
Zn x – 0.68 ("0.1) 0.85 ("0.2) 0.64 ("0.0)<br />
–: no such treatment, x: not sampled, y: no data available, n.c. not calculable due to the too low <strong>nematode</strong> density, BF: bacterial<br />
feeders, FF: fungal feeders.<br />
Fig.1.Diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles for the Cd treatment.Cd 2:30 mg<br />
y1 y1 y1<br />
kg , Cd 3:90 mg kg , Cd 4:270 mg kg .<br />
Fig.2.Diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles for the Cr treatment.Cr 2:30 mg<br />
y1 y1 y1<br />
kg , Cr 3:90 mg kg , Cr 4:270 mg kg .<br />
139<br />
Fig.3.Diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles for the Cu treatment.Cu 2:30 mg<br />
y1 y1 y1<br />
kg , Cu 3:90 mg kg , Cu 4:270 mg kg .<br />
dient.Moreover, the diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles also showed<br />
a significant decrease as a c<strong>on</strong>sequence <str<strong>on</strong>g>of</str<strong>on</strong>g> the 90<br />
y1 mg kg level.Therefore, it can be c<strong>on</strong>cluded that<br />
LOEC value for Cr is approximately 0.5 mg<br />
y1 kg available c<strong>on</strong>centrati<strong>on</strong> (expressed in NH4- acetateqEDTA soluble).In the higher treatments<br />
y1<br />
(90 and 270 mg kg ), where the remaining<br />
y1<br />
available Cr in 1997 was 0.77 mg kg and 1.4<br />
y1 mg kg , respectively, all parameters showed a<br />
c<strong>on</strong>siderable depressi<strong>on</strong>.It is difficult, however, to<br />
quantify what proporti<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> available Cr acts in<br />
the <strong>soil</strong> as the more toxic Cr(VI) form.<br />
In case <str<strong>on</strong>g>of</str<strong>on</strong>g> the Cu gradients, no obvious resp<strong>on</strong>se<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> <strong>nematode</strong>s could be observed based <strong>on</strong> the most<br />
parameters.Only diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles showed a more<br />
or less c<strong>on</strong>sistent stepwise difference suggesting<br />
y1<br />
that 90 and 270 mg kg c<strong>on</strong>centrati<strong>on</strong>s might
140 P. Nagy et al. / Science <str<strong>on</strong>g>of</str<strong>on</strong>g> the Total Envir<strong>on</strong>ment 320 (2004) 131–143<br />
Fig.4.Diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles for the Se treatment.Se 1:10 mg<br />
y1 y1 y1<br />
kg , Se 2:30 mg kg , Se 3:90 mg kg , Se 4:270 mg<br />
kg . y1<br />
have an unfavourable effect <strong>on</strong> <strong>nematode</strong><br />
<strong>assemblages</strong>.<br />
Korthals et al. (1996c) observed several clear<br />
effects <strong>on</strong> <strong>nematode</strong> trophic structure <str<strong>on</strong>g>of</str<strong>on</strong>g> a field<br />
c<strong>on</strong>taminated with a Cu c<strong>on</strong>centrati<strong>on</strong> gradient 10<br />
years prior to sampling.In the most comparable<br />
case, where actual pH was 5.5 (originally 6.1)<br />
total numbers were similar al<strong>on</strong>g the whole c<strong>on</strong>centrati<strong>on</strong><br />
gradient.Bacterial feeders slightly, fungal<br />
feeders remarkably increased with higher Cu<br />
levels.Plant <strong>nematode</strong>s showed no c<strong>on</strong>sistent reacti<strong>on</strong>.Omnivorous<br />
and carnivorous <strong>nematode</strong>s<br />
decreased al<strong>on</strong>g the c<strong>on</strong>centrati<strong>on</strong> gradient.These<br />
Fig.5.Diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles for the Zn treatment.Zn 2:30 mg<br />
y1 y1 y1<br />
kg , Zn 3:90 mg kg , Zn 4:270 mg kg .<br />
results are partly in line with our findings: fungal<br />
feeders seemed to slightly benefit from the increasing<br />
Cu levels and the BFyFF ratio decreased.Also,<br />
plant feeders fluctuated around basically the same<br />
percentage value.However, in our study there was<br />
no systematic decrease in the number <str<strong>on</strong>g>of</str<strong>on</strong>g> omnivorous<br />
and carnivorous <strong>nematode</strong>s and bacterial feeders<br />
rather decreased than increased in their<br />
proporti<strong>on</strong>.The probable main reas<strong>on</strong>s for the<br />
partly dissimilar findings can be the different pH<br />
values and <strong>soil</strong> type.Under present c<strong>on</strong>diti<strong>on</strong>s,<br />
<strong>nematode</strong>s did not appear to be particularly sensitive<br />
to Cu up to an available c<strong>on</strong>centrati<strong>on</strong> level<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> approximately 130 mg kg . y1<br />
The relatively high proporti<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> c-p 3–5 nem-<br />
y1<br />
atodes in 270 mg kg Cd and Cu samples may<br />
be due to the insensitivity <str<strong>on</strong>g>of</str<strong>on</strong>g> this group <str<strong>on</strong>g>of</str<strong>on</strong>g> persister<br />
<strong>nematode</strong>s to the given metals or an increase in<br />
algal growth in the upper millimetres <str<strong>on</strong>g>of</str<strong>on</strong>g> the <strong>soil</strong>,<br />
where the heavy metals had been washed out.<br />
The most expressed effects <strong>on</strong> target parameters<br />
in this experiment were observed in the Se treat-<br />
y1<br />
ments.The first c<strong>on</strong>centrati<strong>on</strong> level (10 mg kg )<br />
slightly increased <strong>nematode</strong> MI, while the two<br />
y1<br />
higher c<strong>on</strong>centrati<strong>on</strong>s (30 and 90 mg kg ) result-<br />
ed in a clearly detectable decrease in all the studied<br />
<strong>nematode</strong> parameters.In the plots <str<strong>on</strong>g>of</str<strong>on</strong>g> highest dose<br />
y1<br />
(270 mg kg ) there were not enough <strong>nematode</strong>s<br />
to calculate indices.It should also be pointed out,<br />
however, that the remarkable negative effects <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
Se might partly be due to the almost complete<br />
y1<br />
lack <str<strong>on</strong>g>of</str<strong>on</strong>g> vegetati<strong>on</strong> in the 270 mg kg plots.This<br />
assumpti<strong>on</strong> is supported by the observati<strong>on</strong>s that<br />
terrestrial <strong>nematode</strong>s are without respect to their<br />
feeding types, closely c<strong>on</strong>nected to vegetati<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
a field (Freckman and Caswell, 1985; Yeates,<br />
1987).It requires further studies to discriminate<br />
between direct and indirect (plant-mediated) toxic<br />
effects <str<strong>on</strong>g>of</str<strong>on</strong>g> high Se loads.<br />
Zn has apparently lost its previously shown<br />
(Nagy, 1999) favourable character for the <strong>soil</strong><br />
<strong>nematode</strong> assemblage by the time <str<strong>on</strong>g>of</str<strong>on</strong>g> the present<br />
experiment.N<strong>on</strong>e <str<strong>on</strong>g>of</str<strong>on</strong>g> the c<strong>on</strong>centrati<strong>on</strong> levels had<br />
any significant effect <strong>on</strong> any <str<strong>on</strong>g>of</str<strong>on</strong>g> the parameters <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
the studied <strong>soil</strong> invertebrate group.The <strong>on</strong>ly indicati<strong>on</strong><br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> its earlier positive effect was that the<br />
diversity <str<strong>on</strong>g>of</str<strong>on</strong>g> the rare taxa was higher in plots <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
high than <str<strong>on</strong>g>of</str<strong>on</strong>g> low Zn levels.Diversity <str<strong>on</strong>g>of</str<strong>on</strong>g> the
P. Nagy et al. / Science <str<strong>on</strong>g>of</str<strong>on</strong>g> the Total Envir<strong>on</strong>ment 320 (2004) 131–143<br />
frequent taxa showed, however, an opposite trend.<br />
Nematode density, MI, SI values showed, though<br />
not significantly, a decrease with the increasing<br />
c<strong>on</strong>centrati<strong>on</strong>s <str<strong>on</strong>g>of</str<strong>on</strong>g> Zn.These findings appear to be<br />
in line with the results <str<strong>on</strong>g>of</str<strong>on</strong>g> Korthals et al. (1996b)<br />
who found Zn to depress <strong>nematode</strong>s in a c<strong>on</strong>cen-<br />
y1trati<strong>on</strong><br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> 200 mg kg during a short-term exper-<br />
iment.In our l<strong>on</strong>g-term study performed under<br />
more favourable <strong>soil</strong> c<strong>on</strong>diti<strong>on</strong>s, Zn doses <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
approximately 140 ppm available c<strong>on</strong>centrati<strong>on</strong> in<br />
plots <str<strong>on</strong>g>of</str<strong>on</strong>g> the maximum treatment gave the first<br />
signs <str<strong>on</strong>g>of</str<strong>on</strong>g> destructi<strong>on</strong> for the <strong>nematode</strong> fauna.In a<br />
recent paper, Georgieva et al. (2002) reported<br />
several negative effects <str<strong>on</strong>g>of</str<strong>on</strong>g> Zn, Cu and ZnqCu<br />
treatments <strong>on</strong> <strong>nematode</strong>s in an English agroecosystem<br />
<strong>on</strong> a sandy loam treated with sewage<br />
sludge.The metal levels applied by them extended<br />
to a higher level (e.g. for Zn: 160–600 mg kg y1<br />
in total c<strong>on</strong>centrati<strong>on</strong>) than in our case.It should<br />
be pointed out, however, that repeated sewage<br />
sludge applicati<strong>on</strong> means a more realistic, but less<br />
c<strong>on</strong>trollable treatment than ploughing in a given<br />
amount <str<strong>on</strong>g>of</str<strong>on</strong>g> metal salt at the start <str<strong>on</strong>g>of</str<strong>on</strong>g> the experiment;<br />
the latter is easily washed out and biologically<br />
more available.<br />
Density decreased significantly by Cr and Se<br />
c<strong>on</strong>centrati<strong>on</strong> gradient, while in Cd and Zn plots,<br />
it showed a n<strong>on</strong>-significant decline.The former<br />
can be attributed to a severe destructi<strong>on</strong>, since<br />
pure <strong>nematode</strong> density is a rather insensitive<br />
parameter (B<strong>on</strong>gers, 1990).<br />
Richness <str<strong>on</strong>g>of</str<strong>on</strong>g> <strong>nematode</strong> taxa is a more sensitive<br />
parameter <str<strong>on</strong>g>of</str<strong>on</strong>g> activity <str<strong>on</strong>g>of</str<strong>on</strong>g> nemat<str<strong>on</strong>g>of</str<strong>on</strong>g>auna as well as<br />
<strong>soil</strong> nitrogen status and decompositi<strong>on</strong> functi<strong>on</strong><br />
(Ekschmitt et al., 1999).In our study, richness<br />
was slightly decreased by increasing Cr and<br />
remarkably decreased by the subsequent steps <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
Se treatment.The other pollutants did not generate<br />
any clear effect.<br />
The clear stepwise resp<strong>on</strong>se <str<strong>on</strong>g>of</str<strong>on</strong>g> Maturity Index<br />
and Structure Index to Cr and Se treatments also<br />
underlines the destructive character <str<strong>on</strong>g>of</str<strong>on</strong>g> these pollutants.The<br />
c-p distributi<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> samples shows very<br />
clearly the sensitivity <str<strong>on</strong>g>of</str<strong>on</strong>g> the ‘persisters’ to Cr and<br />
Se polluti<strong>on</strong>.The c-p 3 <strong>nematode</strong>s being very rare,<br />
the apparent trends in this parameter can be attributed<br />
to the sensitivity <str<strong>on</strong>g>of</str<strong>on</strong>g> the K-strategist <strong>nematode</strong>s<br />
(in this case bel<strong>on</strong>ging mostly to the order Dory-<br />
141<br />
laimida).This is in accordance with B<strong>on</strong>gers<br />
(1990, 1999).Zullini and Peretti (1986) found a<br />
similar phenomen<strong>on</strong> for lead (Pb) polluti<strong>on</strong>.<br />
Regarding distributi<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> feeding groups: the<br />
percentage dominance bacterial feeders (chiefly<br />
Acrobeloides, Chiloplacus and Heterocephalobus)<br />
clearly increase al<strong>on</strong>g the c<strong>on</strong>centrati<strong>on</strong> gradients<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> Cr and Se.In the light <str<strong>on</strong>g>of</str<strong>on</strong>g> other parameters, this<br />
indicates the relative insensitivity <str<strong>on</strong>g>of</str<strong>on</strong>g> this group to<br />
the given disturbances.It is remarkable how dominant<br />
Chiloplacus is in the 90 and 270 ppm Seplots.This<br />
indicates a c<strong>on</strong>siderable tolerance for<br />
Se, at least compared to other <strong>nematode</strong> taxa that<br />
occur in the studied area.This phenomen<strong>on</strong> has<br />
also been observed earlier, except the stepwise<br />
resp<strong>on</strong>se (Nagy, 1999). Proporti<strong>on</strong> <str<strong>on</strong>g>of</str<strong>on</strong>g> fungal feeding<br />
<strong>nematode</strong>s remains stable (Zn) or slightly<br />
increases (Cd, Cr, Cu), but even in case <str<strong>on</strong>g>of</str<strong>on</strong>g> Se, it<br />
decreases str<strong>on</strong>gly <strong>on</strong>ly in the highest treatment<br />
level.In the latter case, the low value is based <strong>on</strong><br />
the (probably random) occurrence <str<strong>on</strong>g>of</str<strong>on</strong>g> a single<br />
Tylencholaimus.This shows that fungivorous <strong>nematode</strong>s<br />
(dominated by Aphelenchus, Aphelenchoides<br />
and Ditylenchus) were quite insensitive to<br />
most polluti<strong>on</strong>s.This is in agreement with D.<br />
Sturhan (pers<strong>on</strong>al communicati<strong>on</strong>) and Korthals et<br />
al. (1996c), who found Aphelenchoides to tolerate<br />
heavy metal (including Cu) stress.The proporti<strong>on</strong><br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> omnivorous and predatory <strong>nematode</strong>s decreased<br />
clearly as a c<strong>on</strong>sequence <str<strong>on</strong>g>of</str<strong>on</strong>g> Cr and Se treatments.<br />
Zn also resulted in a slight decrease, while to Cd<br />
this group reacted with an increase.Since dominant<br />
representatives <str<strong>on</strong>g>of</str<strong>on</strong>g> this group were in this study<br />
basically the same as the c-p 4–5 <strong>nematode</strong>s, these<br />
results underline the harmful effects <str<strong>on</strong>g>of</str<strong>on</strong>g> Cr and Se<br />
dem<strong>on</strong>strated by the above menti<strong>on</strong>ed parameters<br />
as well.<br />
In general, MI (and the closely related c-p<br />
distributi<strong>on</strong>), SI values and diversity pr<str<strong>on</strong>g>of</str<strong>on</strong>g>iles gave<br />
basically similar indicati<strong>on</strong>s <str<strong>on</strong>g>of</str<strong>on</strong>g> the effects <str<strong>on</strong>g>of</str<strong>on</strong>g> the<br />
studied elements.While for Cr and Se, a clear<br />
depressi<strong>on</strong> could be dem<strong>on</strong>strated and for Zn a<br />
weak depressi<strong>on</strong> appears, Cd generated no sensitivity<br />
and Cu treatments showed no obvious patterns.The<br />
fact that the above parameters <str<strong>on</strong>g>of</str<strong>on</strong>g><br />
different theoretical nature led to comparable c<strong>on</strong>sequences<br />
shows the robustness <str<strong>on</strong>g>of</str<strong>on</strong>g> the present<br />
results.The combined use <str<strong>on</strong>g>of</str<strong>on</strong>g> these tools may be a
142 P. Nagy et al. / Science <str<strong>on</strong>g>of</str<strong>on</strong>g> the Total Envir<strong>on</strong>ment 320 (2004) 131–143<br />
relevant method in field toxicity studies, <str<strong>on</strong>g>of</str<strong>on</strong>g>fering<br />
several advantages compared to single indices.<br />
Such advantages <str<strong>on</strong>g>of</str<strong>on</strong>g> diversity ordering are the firm<br />
background built <strong>on</strong> various diversity indices and<br />
the suitability <str<strong>on</strong>g>of</str<strong>on</strong>g> clear graphic interpretati<strong>on</strong>.However,<br />
the Maturity Index and Structure Index are<br />
easy-to-calculate measures <str<strong>on</strong>g>of</str<strong>on</strong>g> highly relevant<br />
nematological basis (B<strong>on</strong>gers and B<strong>on</strong>gers, 1998;<br />
B<strong>on</strong>gers, 1999; B<strong>on</strong>gers and Ferris, 1999; Ferris<br />
et al., 2001).<br />
In c<strong>on</strong>clusi<strong>on</strong>, both favourable <strong>soil</strong> c<strong>on</strong>diti<strong>on</strong>s<br />
and time elapsed (over 7 years) since the c<strong>on</strong>taminati<strong>on</strong><br />
as well as not very high available element<br />
c<strong>on</strong>centrati<strong>on</strong>s may explain the less pr<strong>on</strong>ounced<br />
effects <str<strong>on</strong>g>of</str<strong>on</strong>g> certain elements (Cd, Cu, Zn).However,<br />
Se and Cr still show significant l<strong>on</strong>g-term effects<br />
<strong>on</strong> terrestrial <strong>nematode</strong>s, an important comp<strong>on</strong>ent<br />
<str<strong>on</strong>g>of</str<strong>on</strong>g> the <strong>soil</strong> biota involved in a crop producti<strong>on</strong><br />
system.<br />
Acknowledgments<br />
This study was supported by a Hungarian-<br />
Flemish Intergovernmental R&D Co-operative<br />
Agreement (C<strong>on</strong>tract No.B15y97) and by the<br />
Ministry <str<strong>on</strong>g>of</str<strong>on</strong>g> Culture and Educati<strong>on</strong> (C<strong>on</strong>tract No.<br />
FKFP 0280y1999).<br />
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