Download Soil Ecosystem Toxicology Metal effects on structure and function

Soil Ecosystem Toxicology
Metal effects on structure and
function
S.A.E. Kools
March 22, 2006, Vrije Universiteit,
Amsterdam
promotor: prof.dr. N.M. van Straalen
copromotor: dr. ir. C.A.M. van Gestel
Summary
In this thesis, experiments and field studies are presented. The title, Soil Ecosystem
Toxicology, represents the different aspects that were studied; the soil harbors an
enormous diversity of organisms and several levels of this ecosystem are investigated in
systems that contain metal pollution, which might cause toxic effects. Research in this
discipline, ecotoxicology, has always searched for indicators that reflect effects on
organisms, the ecosystem structure. This thesis also presents studies that focus on
ecosystem processes and ecosystem functioning.
In the Netherlands, an enormous amount of sites is polluted (ca. 750,000). For example, in
the western part of the Netherlands, poor grassland soils were improved by using farm and
city waste from the 1600s till the mid-1900s. Soil in these large-scale areas nowadays
contains elevated concentrations of metals, such as copper (up to 160 mg/kg), lead (8001000 mg/kg) and zinc (300 mg/kg). These concentrations exceed Intervention Values, the
threshold above which immediate action is required to mitigate the risks for humans and
ecosystems. These grasslands, however, are seemingly healthy ecosystems and some
are even designated as valuable nature reserves, for which nature development plans
were developed. This thesis pays special attention to the grasslands in such a nature
reserve, fields located in the Polder Demmerik.
The first studies discuss several structural endpoints, the bacteria, nematodes,
enchytraeids and earthworms, since they are sensitive to heavy metal pollution and occur
abundantly in grasslands. Next to that, due to their abundance, these organisms might
have a major influence on functional endpoints. Chapter 2 shows high densities of
enchytraeids and earthworms. In addition, mesocosms (intact soil samples) were used to
analyze the relations between enchytraeids, earthworms and decomposition endpoints.
Heavy metals seemed to have no major effects on the abundance of the organisms by
comparing polluted and non-polluted sites. However, soil with higher metal concentrations
had reduced wheat straw decomposition rates, a functional endpoint. This chapter also
illustrates that certain functional endpoints are linked with structural aspects, for example
the consumption of bran-based bait in correlation with earthworms.
The next chapter (Chapter 3) presents detailed research on soil from the Polder Demmerik
by sampling intact soil columns, so-called Terrestrial Model Ecosystems (TMEs). These
were transported to a climate room, which enabled studying links between structure and
functioning. Multivariate statistics showed the relation between structure (enchytraeids,
nematodes and bacteria) and function (decomposer activity and nitrate from TMEs).
Furthermore, earthworms and plant yield turned out to be related. Overall, biomass was
less related to functional endpoints than biodiversity. The most sensitive to metals were
the enchytraeids, showing a reduced biomass and diversity with increasing metal
concentration. The soil pH was also an important factor, either causing direct effects on
organisms or indirect effects on the bioavailability of metals.
Having assessed some structural and functional endpoints in the previous chapters,
Chapter 4 describes a study of earthworms taken from polluted and non-polluted sites.
The field sampling campaign showed a skewed adult/juvenile ratio of the earthworm
community in the most polluted area. The zinc concentrations in metal-sensitive worms
(Allolobophora chlorotica) from polluted soils were not elevated compared to worms from
non-polluted soils. Moreover, in an acute filter paper toxicity test, the average LC50s
(concentration that killed 50% of the worms) of zinc were the highest for the animals from
non-polluted soils and the differences were not significant. Thus, zinc tolerance was not
shown for the earthworms from the polluted nature area.
Chapter 5 presents the study that assesses the zinc toxicity for soil microbial processes in
the presence and absence of enchytraeids. The soil from the most polluted area was used
for preparing microcosms, without, or inoculated with, a mixture of enchytraeid species
from that same area. Respiration, ammonium concentrations, and soil moisture levels
were increased by enchytraeids. The addition of zinc caused no increased mortality of
enchytraeids during six weeks’ incubation. Soil nitrate concentrations showed a negative
trend with increasing zinc levels, while ammonium concentrations were highest at
maximum zinc concentrations (1360 mg/kg). This indicated impairment of ammonium
oxidation. In addition to this, zinc decreased bacterial carbon biomass and caused a doserelated decrease of the respiration, but this was not observed in the presence of
enchytraeids. Therefore, these organisms have a strong effect on microbiologically driven
ecosystem processes.
The TME study in Chapter 3 showed that it is technically possible to simultaneously study
species, populations, community and ecosystem processes. The potential impact of the
elevated heavy metal concentrations on ecosystem stability was intriguing. The
experiment in Chapter 6 aims to assess the resistance to stress of polluted and less
polluted soils. For this, TMEs were sampled in the same set-up and ecosystem stability
was analyzed by applying three levels of zinc by adding ca. 2, 9 and 40 mg /L to artificial
rainwater that was watered upon the TMEs during the experiment. The gradual increase in
zinc concentrations in the top layer did not cause pronounced effects on the structure in
the less polluted soils, which was expected since these systems might not be adapted to
zinc stress. However, results of this experiment indicated that the most polluted soils were
more vulnerable, since decomposer activity (bait consumption) was decreased in the
highest soils only. Next, ammonium from the TMEs was highest in the most polluted soils,
thus indicating impairment of the nitrogen cycle, as described in the previous chapter.
In Chapter 7, a second TME experiment was performed in which a shock-type of stress
was applied, in contrast with the gradual increase in zinc described above. This
experiment showed fewer organisms in soils with higher heavy metal concentrations. Here
we applied pulse doses of zinc (4.2 g/L). This caused a similar decreased decomposition
activity, but nitrogen levels were not altered. Another group of TMEs was subjected to a
different stress treatment (heating at 40 °C for 24 h), primarily aimed at affecting bacteria
and to investigate whether the responses were different between polluted and less-
polluted soils. CO2 production and ammonium leaching were more sensitive to heat
treatment in the most polluted soils than in less polluted soils. The conclusion was that
higher polluted systems seem to be less stable.
Another important ecosystem function is the (bio)degradation of xenobiotics or the socalled purifying function of ecosystems. Chapter 8 therefore investigated whether
degradation rates of glyphosate serve as an indicator for ecosystem health. Glyphosate is
commonly used on grassland soil to kill weeds, for example as the active ingredient in
Roundup®. However, the degradation rates were not different between soils. Against
expectations, a positive correlation between glyphosate degradation rates and soil metal
pollution was observed. The conclusion was that metals have no harmful effect on bacteria
responsible for the herbicide degradation. Moreover, soil pH turned out to be important.
This herbicide tends to stick (chelate) to soil particles, especially in the presence of heavy
metals, and this asks for research into the long-term effects.
This thesis shows that grasslands in the metal polluted areas indeed have high numbers of
bacteria, nematodes, enchytraeids and earthworms, but that these were lower than nonpolluted sites. Further, functional endpoints give insight into possible effects of pollutants.
An important consideration for the use of functional endpoints is that some functional
endpoints were influenced by several factors, while others integrated only a low level of
complexity.
The polluted and less polluted grassland showed to be different across several ecosystem
levels. A multiple-line-evidence approach in this thesis points out that the metals in most
cases caused only subtle effects on organisms. Yet, the implications for ecosystems of
these subtle effects on the structure were more severe, as shown by the stress-on-stress
studies.
Ultimately, the metal pollution may have, yet unknown, effects on soil organisms that are
essential for nature development. The nature development plans in these areas must
therefore take into account the vulnerability of the polluted areas, for example by
formulating less explicit targets.