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Metal pollution
and the functioning of ecosystems
Bioavailability and effects of heavy metals on
the structure and functioning of detritivores in
former floodplain soils in the Biesbosch, the
Netherlands
P.H.F. Hobbelen
September 20, 2005, Vrije Universiteit,
Amsterdam
promotors: prof.dr. N.M. van
Straalen and prof.dr. S.A.L.M. Kooijman
copromotor: dr. ir. C.A.M. van Gestel
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Summary and Conclusions
Due to anthropogenic emissions, concentrations of heavy
metals in water of the rivers Rhine and Meuse reached peak
levels during the late 1960s and early 1970s
(www.waterbase.nl).
Deposition of polluted particles resulted in high
concentrations of heavy metals in river sediments and areas
flooded by these rivers. Although metal concentrations in
the rivers decreased again as a result of stricter
environmental government policies, metal concentrations in
sediments of flooded areas remain high until today. The
Biesbosch in the Netherlands, which is the delta area of the
rivers Rhine and Meuse, is one of the most polluted areas.
The aim of this thesis was to determine the consequences of
metal pollution for the structure and functioning of soil
fauna in the Biesbosch.
Soil animals that belong to the detritivores or decomposers,
feed on dead organic matter and are important for the
completion of element cycles in ecosystems, because they
contribute to the mineralization of carbon and other
elements like nitrogen and phosphate in organic matter,
making them available again for uptake by plants (Seastedt,
1984). This study focuses on decomposers that belong to the
group of shredders or litter transformers, because they
fragment litter by feeding on it. Shredders include groups
such as earthworms, enchytraeids, isopods and millipedes,
large mites, molluscs and insect larvae (Brussaard et al.,
1997). Shredders can positively as well as negatively
influence the mineralization of litter. They contribute
directly to the mineralization of litter by respiration of
CO2 and by excretion of nutrients as waste products. They
may also indirectly influence the litter decomposition by
changing the microbial community (Anderson and Bignell,
1980; Schönholzer et al., 1999) and its activity
(Tsakala, 1994) and by changing the accessibility of litter
fragments for microbes (Lavelle et al., 1998; Bossuyt et
al., 2005).
Having entered the body of organisms, heavy metals can
affect shredders in different ways. Literature data show
negative effects of heavy metals on e.g. growth,
reproduction and survival of shredders (Spurgeon and Hopkin,
1999; Ma, 1988; Spurgeon et al., 2000; Donker and Bogert,
1991; Hopkin and Hames, 1994; Donker et al., 1998). However,
data on the effects of heavy metals on the biodiversity of
shredders and on their contribution to the decomposition of
litter are scarce. Therefore, the general research questions
of this thesis were to determine:
- the effects of heavy metal
pollution on the structure of detritivore
communities
- the effects of heavy metals on the
functioning of detritivores.
In this thesis I tried to answer these
questions for a specific habitat and, as mentioned above,
for detritivores belonging to the shredders. The habitat
studied in this thesis consisted of former floodplains in
the Brabantsche Biesbosch, dominated by a vegetation of
stinging nettles (Urtica dioica) and reed
(Phragmites australis). For practical reasons, it was
not possible to study all groups of shredders and all
metals. Previous studies in the Biesbosch showed that
concentrations of Cu and Zn, two essential metals, and Cd
and Pb, two non-essential metals, were higher than
intervention values. Intervention values are used by the
Dutch government to determine if the risk for the
environment, posed by heavy metal pollution, is that high
that cleaning or removal of the soil is necessary. It was
decided to focus on these four metals. Next, a
pilot-experiment was conducted to determine which groups of
primary detritivores were present in the study area and
which of the metals Cd, Cu, Pb and Zn could possibly affect
these primary detritivores (Chapter 2). Results showed that
earthworms, isopods and millipedes were important
detritivore groups in the study area. Because no unpolluted
areas could be found in the Biesbosch, it was decided to
include a literature search for reference concentrations of
heavy metals in different soil fractions, in tissues of
detritivores and in plant leaves. Comparison of the data
found in the literature with the measured metal
concentrations in the Biesbosch showed that Cd, Cu and Zn
concentrations in earthworms and Cu concentrations in
millipedes were increased compared to concentrations in
reference areas, while metal levels in isopod species were
always similar to concentrations in non-polluted areas.
Therefore, it was decided to focus on the heavy metals Cd,
Cu and Zn and on earthworms, isopods and millipedes during
the following studies.
Having decided which metals and detritivore groups should be
studied, it was tried to answer the general research
questions. A large field experiment was set up, including 15
field sites in the Biesbosch that constituted a gradient of
Cd, Cu and Zn pollution (Chapter 4). At each field site, the
structure of the community consisting of earthworms, isopods
and millipedes was determined and metal concentrations in a
number of soil fractions were measured to determine if they
affected community structure (research question 1). Litter
bags and bait-lamina sticks were laid out in the field sites
to determine feeding activities of earthworms, isopods and
millipedes and these were also related to measured metal
concentrations to see if they were affected by heavy metal
pollution (research question 2). Results show that metal
pollution was not a dominating factor determining the
structure of the detritivore community, although the biomass
of the earthworm Lumbricus rubellus was positively
and significantly correlated to Zn concentrations in pore
water and 0.01 M CaCl2
extracts of the soil. No effects of metal pollution were
found on the feeding activity of soil fauna as indicated by
the bait-lamina method, but significant correlations were
found between litter decomposition and 0.01 M
CaCl2
extractable Cd concentrations. However, the use of two types
of litter bags to account for litter consumption by other
organisms than earthworms, isopods and millipedes and the
similarity in the amount of variation in the litter
consumption explained by the biomass of Lumbricus
rubellus and the total detritivore biomass, suggest that
Lumbricus rubellus is the most important factor
determining the consumption of litter rather than the 0.01 M
CaCl2
extractable Cd concentrations. The positive relationship
between the biomass of Lumbricus rubellus and the Zn
concentrations in pore water and 0.01 M
CaCl2
extracts of the soil is probably not a causal one, because
these Zn levels in the Biesbosch were similar to background
levels. So, based on this field experiment it can be
concluded that despite the very high total concentrations in
soil, effects of heavy metals on the structure and
functioning of detritivore communities were not detectable
in former floodplain soils in the Brabantsche Biesbosch.
Possible reasons could be adaptation of the earthworms,
isopods and millipedes to heavy metal pollution or the
presence of other more important factors such as differences
in the degree of isolation, organic matter content and
perhaps occasional flooding between the field sites.
The field experiment described above was conducted only
once. Species densities and concentrations of heavy metals
in plant leaves, animal tissues and in the soil solution may
show a seasonal fluctuation. Next to this, results from both
the pilot-experiment (Chapter 2) and the field experiment,
mentioned above (Chapter 4), showed that metal
concentrations in earthworms were increased. Therefore, a
laboratory experiment was conducted to determine effects of
the heavy metals Cd, Cu and Zn on the litter consumption by
Lumbricus rubellus (research question 2; Chapter 5).
To be able to extrapolate the results of the laboratory
experiment to earthworms in the Biesbosch, Lumbricus
rubellus and soil were collected from the twelve
Biesbosch field sites and earthworms were kept in their
native soil. Results showed that the internal Zn and Cd
concentrations in Lumbricus rubellus positively
affected the litter consumption per biomass of this
earthworm. Possible explanation for this positive
relationship could be the result of an increased demand for
energy, needed for the production of enzymes and processes
involved in the regulation and detoxification of heavy
metals. However, more research is needed to verify this
assumption.
The study above focused on the effect of heavy metals on the
food consumption by individual adult earthworms for a
limited period of time. To predict the litter consumption by
populations of earthworms, one should be able to describe
the food consumption by individual earthworms from birth to
death as a function of abiotic factors and exposure to
toxicants. Therefore, in Chapter 6, the influence of
temperature and food density on the effect of Cu on the
litter consumption by Lumbricus rubellus was studied
(research question 2), using Dynamic Energy Budget (DEB)
modeling. Cu was chosen, because data on growth of
Lumbricus rubellus at different exposure levels to
this metal species were available in the literature. A
DEB-model describes the energy fluxes through and within an
organism in time. This study used the mechanistic DEB-model
developed by Kooijman (2000), which is based on
physiological assumptions. The qualitative effects of
temperature on growth, as predicted by the DEB-model, were
in agreement with most data on the same or other earthworm
species that could be found in the literature. Few data were
available on the effect of temperature on the litter
consumption by earthworms and these data were contradictory.
Assuming that the DEB-model can describe the food
consumption by most earthworm species as a function of their
internal Cu concentration and as a function of temperature
and food density, model predictions showed that the effect
of Cu on the litter consumption by earthworms is larger at
higher temperatures for both constant and seasonally
fluctuating temperature regimes, but that it does not matter
if temperature fluctuates or not. Fluctuation of the food
density and increasing the average food density, increased
the effect of Cu on the litter consumption by earthworms.
The modeling approach based on dynamic energy budgets seems
to be a useful tool to integrate literature data and to
predict effects of environmental variables and toxicants
that are difficult to measure experimentally, but relevant
in the field.
The results of the pilot-experiment (Chapter 2) and the
field experiment (Chapter 4) showed that despite high total
soil concentrations of heavy metals, concentrations in pore
water and 0.01 M CaCl2
extracts were similar to background levels. Because it was
reported in the literature that earthworms predominantly
take up heavy metals in a soluble form and because pore
water concentrations and 0.01 M
CaCl2
extractable metal concentrations give an indication of
soluble metal concentrations, it would be expected that
internal concentrations of heavy metals in earthworms would
also be similar to background levels. This raised the
question which metal pools in the soil were responsible for
the increased bioaccumulation of heavy metals in earthworms.
Although not included in the general research questions, it
was tried to answer this question by analyzing the data
generated in the field experiment (Chapter 4) to determine
the relation between the internal metal concentrations in
the earthworms Lumbricus rubellus and Aporrectodea
caliginosa and the metal concentrations in different
soil fractions (Chapter 3). Results of this analysis showed
that Cd and Cu concentrations in earthworms were positively
and significantly correlated to pore water concentrations.
This supports the importance of the uptake of soluble metals
from the pore water. However, variation in Cd concentrations
in Lumbricus rubellus and Cu concentrations in
Lumbricus rubellus and Aporrectodea caliginosa
could best be explained by total soil concentrations. This
suggests that ingestion of Cd and Cu attached to soil and
organic matter particles also contributes to the uptake of
these metals by earthworms. None of the determined metal
fractions seemed to influence the Zn concentrations in
Lumbricus rubellus and Aporrectodea
caliginosa. It can be concluded that taking the total
soil concentration into account in predicting the internal
metal concentration of earthworms is useful for soils with
high total soil concentrations, but low soluble metal
concentrations.
Despite the high total soil concentrations of heavy metals
in the Biesbosch soils, the combination of high pH and a
high clay, organic matter and inorganic carbon content in
these soils results in soluble metal concentrations that are
comparable to background levels. Therefore, only those soil
animals that ingest polluted soil particles or that are able
to desorb heavy metals from clay and organic matter may be
at risk. From the organisms studied in this thesis,
earthworms seem to be most at risk, based on their increased
internal metal concentrations. Results presented in this
thesis show that internal Zn and Cd concentrations in
Lumbricus rubellus affected the litter decomposition
by this earthworm, which is an important species for the
litter decomposition in the study areas, but that these
effects were positive instead of negative. As mentioned
above, a possible explanation for this positive relationship
could be the result of an increased demand for energy,
needed for the production of enzymes and processes involved
in the regulation and detoxification of heavy metals. No
effects of heavy metals were found on the structure and
functioning of primary detritivores at the community level.
So, it can be concluded that heavy metal pollution is not a
dominating factor determining the structure and functioning
of primary detritivore communities in former floodplain
soils in the Biesbosch.
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