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Carabid beetles (Coleoptera, Carabidae) are one of the most studied soil groups in relation to heavy metal (HM) accumulation and use for bioindication of environmental pollution. Accumulation of Zn and Cu in carabid beetles was species-, sex- and trophic group-specific. No differences were found in HM contents between omnivorous and carnivorous species. The use of carabid beetles as indicators of HM accumulation appears to be rather limited.
Heavy metals, carabid beetles, pollution, accumulation
Because of the increasing impacts of chemicals on terrestrial and soil ecosystems, assessment of environmental quality by bioindicators is of particular interest.
Carabid beetles are traditionally used as bioindicators of anthropogenic stresses for a number of reasons. They inhabit most terrestrial ecosystems. The ecology and systematics of the group are well studied. Sampling methods are simple and universal. And the data collected by different researchers are comparable.
In soil trophic webs, carabid beetles play an extremely important role as non-specialized predators and 2nd order consumers.
There are numerous publications demonstrating structural
changes in carabid communities due to different anthropogenic impacts
caused by motorways, metallurgic smelters, and recreation (see review
by
This paper reviews the literature data on heavy metal (HM) impacts on carabid beetle communities and also considers the use of carabids as indicators of HM accumulation.
Results and discussion HM contents limitsThe mean HM content in carabids decreased in the following sequence Fe > Zn > Cu > Mn > Pb > Cd (
The concentration ratios of Cd : Pb : Mn : Cu : Zn :
Fe in an average carabid beetle were 1 : 2.5 : 7 : 17 : 29.5 : 93. In
other words, an average carabid beetle may contain 93 times more Fe
than Cd and 37 times more Fe than Pb (
Variation coefficients of HM in carabids were variable and dependent on the carabid genus and type of HM (Table 1). In Carabus spp. for Pb, Zn and Cu the coefficient was 17.9% (5.2–32.5%) and in Pterostichus spp. 29.9% (6.3–48.2%). (Table 1).
The analysis of 14 HMs in 28 carabid species revealed that the variability of HM in Carabus spp. was 26% and in Pterostichus spp. 42% (
Inter-generic variability in HM contents (ppm) in carabid beetles (by different authors after
Genera | N | Heavy metals, ppm | |||||
---|---|---|---|---|---|---|---|
Cd | Cu | Fe | Mn | Pb | Zn | ||
Abax | 3 | 0.1* | 15.9 | N/A | N/A | 3.1+1.7 | 62.8 |
Agonum | 2 | 0 | 25.8+ 7.9 | 532.3 | 24.3 | 4.9+4.9 | 95.0+14.4 |
Calathus | 4 | 1.0+0.3 | 57.2+30.8 | 58.7+ 49.0 | 29.1+9.3 | 6.7+1.9 | 89.2+21.1 |
Carabus | 9 | 0.1+0.1 | 16.9+ 0.9 | 333.9 | N/A | 4.3+1.4 | 96.1+15.3 |
Harpalus | 1 | 0 | 23.3 | N/A | N/A | 0 | 130 |
Leistus | 2 | 2.9+1.1 | 30.1 | N/A | N/A | 7.8 | 118.6 |
Loricera | 1 | N/A | N/A | N/A | N/A | 1.9 | N/A |
Notiophilus | 2 | 1.7+0.3 | 27.5+ 1.3 | 117.1+109.9 | 29.2+2.8 | 1.7+0.3 | 77.9+10.5 |
Poecilus | 2 | 0.1+0.1 | 16.3 | N/A | N/A | 4.2+4.2 | 118.7+30.7 |
Pseudo-ophonus | 1 | 0 | 17.3+ 2.1 | 461.2 | N/A | 3.0+3.0 | 92.3+ 6.4 |
Pterostichus | 5 | 0 | 29.5+10.4 | 436.3+ 37.3 | N/A | 2.9+1.4 | 116.2+ 7.4 |
A positive correlation between body mass and Pb content was found in beetles of the genus Carabus (Emets and Zhulidov 1983) and three other species: Calathus melanocephalus, Notiophilus biguttatus, Notiophilus rufipes (but not for Zn or Cd) (
I subdivided the collected carabids into three groups: (1) with body mass (B) less than 15 mg (genera Agonum, Leistus, Loricera, Notiophilus, Calathus); (2) with 15<B<50 mg (genera Pseudophonus, Poecilus, Pterostichus, Abax, Harpalus) and (3) with B>50 mg (genus Carabus) (Table 2).
Mean HM content (at least for Zn, Pb and Mn) was not dependent on the mass/size of carabid beetles. Medium-sized species contained more Fe compared to small-sized species and small species contained more Cd and Cu compared to medium-sized and large species.
Heavy metal content (ppm) and dry body mass of carabid beetles (
Heavy metals | Body mass, mg | ||
---|---|---|---|
<15 | 15–50 | >50 | |
Cd | 1.4+0.6 | 0.5+0.3 | 0.1+0.1 |
Cu | 35.1+7.4 | 20.5+2.6 | 16.9+0.9 |
Fe | 236.0+149.1 | 448.7+12.4 | 333.9 |
Mn | 26.7+2.4 | 29.1 | - |
Pb | 4.6+1.2 | 2.6+0.7 | 4.3+1.4 |
Zn | 95.2+8.6 | 104.0+11.9 | 96.1+15.3 |
In most studies no clear pattern of HM contents in males or females of carabid species were observed (
In some species, males contained more metals (Pb, Zn, Cd, Cu, Mn, Fe, Co, Ni, Sr, Cr, Al) than females (
Sex-specific differences were found in six carabid species (Poecilus cupreus, Pterostichus melanarius, Pterostichus niger, Pseudophonus rufipes, Carabus nemoralis and Carabus granulatus), while females contained more Zn than males (
Microelement (Na, Mg, K, Ca) concentrations were higher in females compared to males in populations of Agonum dorsale and Agonum sexpunctatum (
No regular pattern was found in studies of HM contents in dozens of carabid species published by numerous authors (reviewed by
Omnivorous species (Harpalus spp., Amara spp.) contained more Cu but less Zn than carnivorous species (Pterostichus spp., Carabus spp.) in roadside ecosystems (Butovsky 1995).
The effects of feeding ecologies were evident only for the essential elements: carnivores (Calathus spp., Pterostichus cupreus, Pterostichus melanarius) had significantly higher contents of Zn, Cu and Mn than omnivores (Harpalus spp., Pterostichus rufipes). No differences were found for Pb and Cd (
Seasonal differences in abundance, species
composition, and age structure of invertebrates may lead to high
variability in HM contents in carabid beetles, and the highest
variability can be expected at highly polluted sites (
Seasonal changes in Cd contents were not found for Notiophilus biguttatus, but higher concentrations were observed in Calathus melanocephalus in autumn, likely due to a peak of reproductive activity (
I found a decrease of Zn and Cu contents in the dominant species Pterostichus cupreus and Pterostichus melanarius in roadside ecosystems of the Moscow region at the end of the season (
In roadside populations of Pterostichus oblongopunctatus the Zn contents of over-wintered beetles was higher than in newly hatched ones (
In ten carabid species, Zn and Cu contents during
the spring were higher than in autumn. The authors speculated that in
the period of increased feeding activity (spring), the elements were
stored in body fat, while during sexual activity and wintering they
were mobilized and excreted. The composition of a population with
regards to the fraction of juvenile specimens, active feeders, or
reproducing individuals may have a considerable effect on the seasonal
dynamics of the metals (
Carabids are relatively poor accumulators of heavy metals, particularly the most toxic ones, such as cadmium or lead (
In contrast, the highest concentrations of
non-essential metals (Cd and Pb) were found in carnivorous carabid
beetles together with earthworms and oribatid mites in the vicinity of a
metallurgic smelter (
In putative trophic chains, carabids as non-specialized predators accumulated less copper and zinc (Cf = 0.54 and 0.21 respectively) than specialized predators (like Coccinellidae, Syrphidae) (0.67 and 0.99 respectively) and specialized parasitoids (Alloxystidae, Pteromalidae)
(1.07 and 2.08 respectively). These differences probably reflected the
increase of trophic adaptation to elevated concentrations of HM in
non-specialized predators, specialized predators and parasitoids (
As in other holometabolic insects, carabid beetles
possess various detoxification systems, which can segregate metals and
turn it into inactive forms (
Compared to other groups of soil invertebrates, carabid beetles are characterized by low accumulation and high excretion rates of cadmium (Table 3).
The concentrations of Pb differed between the
exoskeleton and the soft tissues in the carabid body. Up to 63–82% of Pb
was accumulated in the exoskeleton (
Females from contaminated sites have elevated
activities of some enzymes (glutathione-S-transferase and
carboxyl-esterase), but males do not (
The fat concentration in carabids collected from polluted sites was lower when compared to reference sites. Presumably, HM excretion requires energy, thus restricting the accumulation of fat (Lindqvist and Block, 2001).
Adaptation (in terms of HM accumulation and
excretion) did not occur in carabids inhabiting chronically polluted
sites and obviously had no genetic basis (
Cd “accumulators” and “disseminators” in soil invertebrate communities (van Straalen and van Wensem 1986;
High Cd contents | Low Cd contents |
---|---|
Isopoda | Orabitida (fam. Notaspididae) |
Opiliones | Lithobiidae |
Lyniphiidae | Collembola (Entomobriidae) |
Pseudoscorpions | Carabidae |
Gamasidea | Staphylinidae |
Oribatida (fam. Camisiidae) | Gryllidae |
Geophylidae | Tettigoniidae |
Diplopoda | |
Collembola (fam. Onychiroidea) |
Carabid beetles constitute one of the most appropriate
invertebrate groups for the study of “ecological” effects of different
anthropogenic stressors of soil communities, and the changes in carabid
community dominance, diversity, abundance, sex ratio etc. have been
used as bioindicators in numerous studies (
On the other hand, carabids are relatively poor HM accumulators (being both holometabolic insects and predators). They may contain elevated amounts of HM in polluted sites compared to referent sites, but results are variable and no accurate assessments of contamination levels can be made.
Our extensive research in roadside ecosystems showed that HM contents in carabids did not correlate with their relative abundance or distance from the motorway (Butovsky 1995) or a metallurgic smelter (van Straalen et al. 2001).
More research is obviously needed on HM stress on carabids, e.g. detoxification, genetic resistance, physiology and demography.