Agriculture, Ecosystems and Environment 83 2001 177–189
Using Collembola to assess the risks of applying metal-rich sewage sludge to agricultural land in western Scotland
Lorna J. Cole
∗
, David I. McCracken, Garth N. Foster, Mark N. Aitken
Conservation and Ecology Department, Environment Division, SAC Auchincruive, Ayr, KA6 5HW, Scotland UK Received 6 December 1999; received in revised form 5 April 2000; accepted 19 April 2000
Abstract
The recent United Kingdom ban on the disposal of sewage sludge at sea has led to the prediction that land application of sludge will become more widespread. The positive aspect of recycling nutrients may, however, be offset by the risk of
contamination by heavy metals that are frequently present in sludge. The environmental impact of applying metal-rich sewage sludge to agricultural land was, therefore, assessed using Collembola. A combination of pitfall trapping and suction sampling
was used to monitor epigealhemiedaphic Collembola on a small plot field trial in the west of Scotland. Four sludge treatments were investigated: cadmium-rich sludge, zinc-rich sludge, uncontaminated sludge and a no-sludge control. It was found that
the abundance of Lepidocyrtus cyaneus Tullberg and Isotoma viridis Bourlet was significantly lower in plots receiving cadmium-rich sludge than those receiving uncontaminated sludge. Isotoma anglicana Lubbock was not influenced by the
presence of metals in sludge and Isotomurus palustris Müller was actually favoured by the application of metal-rich sludge. Other aspects of collembolan ecology, and the efficiency of the two sampling methods, are also discussed. © 2001 Elsevier
Science B.V. All rights reserved.
Keywords: Ecotoxicology; Sewage sludge; Heavy metals; Collembola; Agriculture
1. Introduction
Recent estimates suggest that, in the United King- dom, 500,000 t of sewage sludge are applied annually
to agricultural land Smith, 1996. However, the Com- mission of the European Communities CEC recent
ban on the disposal of sewage sludge at sea Commis- sion of the European Communities, 1991 has led to
the prediction that the recycling of sludge to agricul- tural land will become more widespread throughout
Europe Rund, 1995. Probably, the principal envi- ronmental risk posed by fertilising agricultural land
∗
Corresponding author. Tel.: +44-1292-525-291; fax: +44-1292-525-333.
E-mail address: l.coleau.sac.ac.uk L.J. Cole.
with sludge lies in the fact that it often contains sig- nificant quantities of heavy metals such as cadmium,
zinc, lead and copper Petruzzelli et al., 1994. These elements, collectively known as potentially toxic el-
ements PTEs, are persistent and will accumulate in the upper layers of the soil where they can reach
levels that are potentially toxic to plants and animals van Straalen et al., 1987.
The CEC’s 1986 Directive on The protection of the environment, and in particular the soil, when
sewage sludge is used in agricultural land addresses the problem of PTEs in sewage sludge Commission
of the European Communities, 1986. This Directive controls the amount of heavy metals entering the en-
vironment through sludge application to agricultural land by setting maximum metal levels for sludge
0167-880901 – see front matter © 2001 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 7 - 8 8 0 9 0 0 0 0 1 7 2 - 9
178 L.J. Cole et al. Agriculture, Ecosystems and Environment 83 2001 177–189
and soil. However, despite the ample information on how PTEs in sludge affect micro-organisms Brookes
and McGrath, 1984; Smith, 1996, there is com- paratively little information on how they influence
invertebrates. Risk assessment studies tend to focus on economically important pests e.g. Hemiptera:
Aphidae, polyphagous predator groups e.g. Aranae and Coleoptera and macro-decomposers e.g. earth-
worms. For example, earthworms and spiders col- lected from plots treated with contaminated sludge
were shown to have elevated metal concentrations indicating that the metals were in bio-available forms
Benninger-Truax and Taylor, 1993. Green peach aphids Appelia schwartzi Börner feeding on plants
grown on contaminated sludge were found to have decreased fecundity and longevity than those feeding
on plants grown on uncontaminated sludge Pimentel and Warneke, 1989. The metals in sludge are, there-
fore, biologically available and have the potential to reduce fitness.
When a pollutant is added to agricultural land, changes in the structure of the microbial community
tend to precede changes in the composition of the plant or invertebrate community. Groups that feed di-
rectly on soil fungi and bacteria e.g. Collembola and Acarina may, therefore, be more susceptible to metal
pollution than predatory or phytophagous groups which are further removed from the effects of the
pollutant. Previous field studies have indicated that although the addition of metal contaminated sludge
did not adversely affect the abundance of Collem- bola, it influenced the community structure Lübben,
1989; Bruce et al., 1999. Lübben 1989 found that Sminthurinus aureus Lubbock, Willemia intermedia
Mills and Isotoma notabilis Schäffer were sensitive to sewage sludge artificially contaminated with metal
salts zinc, cadmium, copper, nickel, chromium and lead, while Folsomia candida Willem and Mesapho-
rura spp. were not. Collembolan communities would therefore appear to be sensitive to metal-contaminated
sludge with species-specific differences in metal sen- sitivity occurring.
Collembola are of agronomic importance not only as a consequence of their regulatory role in decompo-
sition Seastedt, 1984, but also because they are an important source of prey for polyphagous predators
Hopkin, 1997. As Collembola live in close associa- tion with the soil micro-flora and fauna, it is likely that
they will give an earlier indication of ecosystem dis- turbance than predatory groups. Furthermore, Collem-
bola are better suited than larger more mobile inverte- brates e.g. Coleoptera in small plot agricultural field
trials.
In this study, the risks of applying metal-rich sewage sludge to agricultural land were assessed in the field
using epigeal Collembola as indicators. A sludge rich in zinc, which is an essential micro-nutrient, and a
sludge rich in cadmium, which is an ecological impu- rity, were investigated on a small-plot field trial. The
metal-rich sludges were derived from sewage treat- ment works with naturally high inputs of each specific
metal. It was considered essential to use naturally con- taminated sludge since this provided a more appro-
priate measure of exposure and, hence, risk under field conditions. The use of sludges artificially con-
taminated with metal salts was discounted as metals are more available in such sludges and they therefore
do not represent a natural situation Smith, 1996. Al- though the use of naturally contaminated sludge meant
that the sludges differed in other respects see Table 1, these were taken into account in the interpretation of
the results.
2. Materials and methods
