184 L.J. Cole et al. Agriculture, Ecosystems and Environment 83 2001 177–189
Fig. 2. Effect of sludge treatment on the abundance of Isotoma viridis and Lepidocyrtus cyaneus caught by suction sampling showing mean number square-root transformed. Error bars show standard deviations.
the total collembolan abundance and the abundance of I. maculatus was significantly lower in pitfalls es-
tablished in plots receiving cadmium-rich sludge than in those receiving uncontaminated sludge Table 4,
Figs. 5 and 6. This difference was not significant in the suction sampling results Table 3.
IsotomaIsotomurus juveniles and I. palustris had a significantly higher abundance in pitfalls placed in
plots receiving sludge than those placed in control plots Table 4 and Fig. 7. In agreement with the
suction results, C. denticulata occurred in its high-
Fig. 3. Effect of sludge treatment on the abundance of Isotoma anglicana and Isotomurus palustris caught by suction sampling showing mean number square-root transformed. Error bars show standard deviations.
est abundance in pitfalls established in plots receiving zinc-rich sludge Table 4 and Fig. 7.
4. Discussion
4.1. Seasonal variation in epigeal Collembola In accordance with findings by other authors, the
influence of season was species-specific Joosse, 1969; Brussaard et al., 1990. Some species reached
L.J. Cole et al. Agriculture, Ecosystems and Environment 83 2001 177–189 185
Fig. 4. Effect of sludge treatment on the abundance of Sminthurus viridis and Ceratophysella denticulata caught by suction sampling showing mean number square-root transformed. Error bars show standard deviations.
their maximum population density in April e.g. S. malmgreni, others in May e.g. I. anglicana and Iso-
tomaIsotomurus juveniles and others in August e.g. H. nitidis, I. viridis and L. cyaneus. Joosse 1969
suggested that seasonal differences in species abun- dance could be related to humidity. This hypothesis
was not supported for all species, and while some hy- drophilic species e.g. S. malmgreni peaked in April
as predicted, others i.e. I. viridis and T. longicor-
Fig. 5. Effect of sludge treatment on the abundance of total Collembola, Isotoma viridis and Lepidocyrtus cyaneus caught by pitfall trapping showing mean number square-root transformed. Error bars show standard deviations.
nis peaked in August Joosse, 1970; Fjellberg, 1980. It would therefore appear that species-specific differ-
ences in seasonal abundance could not simply be ex- plained by their humidity preference.
4.2. Effect of treatment on epigeal Collembola It is well documented that the addition of sewage
sludge can promote Collembola, and this is thought
186 L.J. Cole et al. Agriculture, Ecosystems and Environment 83 2001 177–189
Fig. 6. Effect of sludge treatment on the abundance of Heteromurus nitidis, Isotoma notabilis and Isotomurus maculatus caught by pitfall trapping showing mean number square-root transformed. Error bars show standard deviations.
to be primarily the result of an increase in food sup- ply Lübben, 1989; Pimentel and Warneke, 1989. In
this study, a higher abundance of total Collembola, H. nitidis and I. notabilis was found in plots receiving
uncontaminated sludge but not those receiving con- taminated sludge when compared to control plots. It
Fig. 7. Effect of sludge treatment on the abundance of Isotomurus palustris, IsotomaIsotomurus juveniles and Ceratophysella denticulata caught by pitfall trapping showing mean number square-root transformed. Error bars show standard deviations.
would therefore appear that while these species ben- efited from the increased nutrients in uncontaminated
sludge plots, this was not the case when the sludge was contaminated by heavy metals. Furthermore, the
species L. cyaneus and I. viridis were both less abun- dant in plots receiving cadmium-rich sludge than in
L.J. Cole et al. Agriculture, Ecosystems and Environment 83 2001 177–189 187
plots receiving uncontaminated sludge, thus indicating that these species were particularly sensitive to the
cadmium-rich sludge. It is important to note that the efficiency of several
sampling methods has been found to decrease in long grass Greenslade, 1964; Harwood, 1994. In studies
where treatment influences grass height, the possibility that treatment effects may be attributed to changes in
sampling efficiency must be considered. In this study, the lower abundance of L. cyaneus and I. viridis in
plots receiving cadmium-rich sludge could not simply be attributed to a reduced sampling efficiency in longer
grass, as grass height was actually lower in plots re- ceiving cadmium-rich sludge Table 5. It is therefore
likely that the observed decrease in these species was a true effect of treatment. Furthermore, the observed
changes in abundance found by suction sampling were largely mirrored in the pitfall data, further suggesting
that grass height did not unduly influence sampling ef- ficiency. As additional differences between the sludges
existed, we cannot however conclude that it was the high levels of cadmium in the cadmium-rich sludge
that adversely influenced these species see Table 1.
Toxicity studies conducted in the laboratory provide a useful indication as to what levels of metals could
potentially effect animals in the field. Smit and van Gestel 1996 found an EC
50
value of 185 mg kg
− 1
soil for the effect of zinc on the population size of F. candida, while Crommenruijn et al. 1993 found
an EC
50
-
reproduction
value in F. candida of 227 mg Cd kg
− 1
soil. From Table 2, it can be seen that while the soil concentration of zinc in the study site was
higher than that shown to effect F. candida in the lab- oratory, the concentration of cadmium was not. Lab-
oratory studies, however, only investigate the direct effects of a contaminant i.e. effects on growth rate,
reproduction and survival and it is possible that the indirect effects of cadmium were more pronounced
than those of zinc. Cadmium may indirectly affect Collembola through altering their habitat structure
and food Posthuma et al., 1993. It is possible that the lower grass height in the cadmium-rich plots re-
sulted in a more variable, and hence less favourable, microclimate Pimentel and Warneke, 1989. Further-
more, species that are able to digest fungal cell walls, where heavy metals are frequently accumulated, are
exposed to metal concentrations far in excess of those found in the soil Siepel, 1994.
The fact that total Collembola and I. maculatus appeared to be adversely affected by the application
of cadmium-rich sludge when sampled by pitfall trapping, but not when sampled by suction sampling,
may indicate sublethal effects of cadmium on mobil- ity. The detoxification of heavy metals is thought to
be energetically costly, and a decrease in glycogen reserves after metal exposure has been found for sev-
eral invertebrate species Richards and Ireland, 1978; Bodar et al., 1990; Reddy and Bhagyalakshmi, 1994.
The presence of metals may, therefore, be expected to reduce activity by decreasing the energy available and
isopods exposed to heavy metals have been shown to have reduced activity levels Hopkin, 1989; Sørensen
et al., 1997. Computer-automated video tracking could provide a quick and effective method of mon-
itoring metal pollution in the laboratory Sørensen et al., 1997 and the present results indicate that I.
maculata might be a suitable test species.
Sminthurus viridis was the only species to occur in its highest abundance in control plots. The abundance
of S. viridis was also higher in the plots receiving cadmium rich sludge than in the plots receiving un-
contaminated or zinc-rich sludge. It is possible that this species was adversely affected by the higher
grass yield in the zinc-rich and digested sludge plots, or was sampled less efficiently in long grass. How-
ever, as S. viridis occurred in its highest abundance in June when the grass was longest, neither explanation
is likely. It is therefore suggested that S. viridis, be- ing phytophagous, did not benefit from the increase
in micro-organisms which accompanies sludge ap- plication. The application of sludge can also favour
predatory carabid beetles and this may account for the lower abundance of S. viridis observed in uncon-
taminated sludge plots Larsen et al., 1996. As this species consumes living plant tissue, which generally
has lower concentrations of heavy metals than fungi Curry, 1994, it may actually have had a competitive
advantage over mycophagous Collembola in plots receiving cadmium-rich sludge.
4.3. Sampling protocol While suction samplers provide good quantitative
data on collembolan population density Johnson et al., 1957; Frampton, 1994, pitfall traps tend to
over-represent the most active species and, hence,
188 L.J. Cole et al. Agriculture, Ecosystems and Environment 83 2001 177–189
give poorer quantitative data Greenslade, 1964. Pit- fall traps also tend to under-represent plant climbing
species e.g. S. viridis, which are well represented in suction samples, but appear to be more effective at
catching strictly surface-active species Bruce, 1997. In this study, suction sampling and pitfall trapping
both yielded nine significant treatment effects. This indicates neither method was superior in assessing the
ecological impact of sewage sludge. Effects for some species were only detected by suction sampling e.g.
S. viridis and I. anglicana while others were only detected by pitfall trapping e.g. IsotomaIsotomurus
juveniles and I. notabilis. In agreement with other au- thors, the most effective sampling regime for epigeal
Collembola would, therefore, appear to be a combina- tion of both pitfall traps and suction samples Berbiers
et al., 1989; Frampton, 1994. Limiting resources may make such a choice unfeasible and when selecting
between methods, the efficiency of each in collect- ing specific groups of species should be considered.
For example, if a treatment predominantly effects plant-climbing species e.g. some pesticides, suction
sampling would be the preferred method as it is more efficient at sampling such species Bruce, 1997.
5. Conclusion
