soil invertebrates- an usefull tool in biomonitoring of heavy metal pollution. a review

12 Pages·2017·0.37 MB·English

Studia Universitatis “Vasile Goldiş”, Seria Ştiinţele Vieţii
Vol. 27 issue 4, 2017, pp 247-258
© 2017 Vasile Goldis University Press (www.studiauniversitatis.ro)

SOIL INVERTEBRATES- AN USEFULL TOOL IN BIOMONITORING OF
HEAVY METAL POLLUTION. A REVIEW

Minodora Manu

Romanian Academy, Institute of Biology Bucharest, Department of Ecology,
Taxonomy and Nature Conservation

ABSTRACT: The atmospheric pollution and its impact on human life, increased attention paid to the
invertebrates. It was determined that human intervention causes important quantitative (density) and
qualitative (diversity) changes of the invertebrate populations from the affected ecosystems in comparison
with those from natural areas. Studies concerning the invertebrates’ usage as biomonitors had been started
from 1977-1978. The lab methods became more and more modern, being used in order to determine
concentrations of heavy metals from invertebrate bodies. These modern techniques are present in this
paper. Analyzing the concentrations of heavy metals from invertebrate bodies from Europe and Russia, the
higher values of cadmium (Cd) were identified on different species of beetles, mollusks, mites-oribatids and
earthworms. High concentrations of lead (Pb) were identified on earthworms, isopods and mollusks. The
mercury (Hg) was identified only on few species of isopods and millipedes. The biomonitor groups for iron
(Fe) are earthworms and beetles; for zinc (Zn): earthworms, springtails, beetles, spiders, millipedes, mites,
pseudoscorpions and mollusks. Millipedes and mites are efficient biomonitors for copper (Cu).
Most biomonitoring studies on invertebrates were realized on species from temperate zones, many of
them being signaled also in Romania. However, the national biomonitoring studies that used invertebrates
are few, in comparison with those from Europe, being necessary many researches with this topic.

Keywords: pollution, invertebrates, monitoring, heavy metal, review.

INTRODUCTION: metals in the body of mammals. The ability of
Increasing of the economic output and the rate of terrestrial species to accumulate pollutants is different.
release of chemicals in nature has reached a level that However there is a small general classification, in
is difficult to control their impact. Use and which species are grouped into two categories: one that
transformation of over 100 000 individual chemicals, accumulates more and another that accumulates less.
whose current locations are difficult to establish, This classification was the first step toward developing
provided new research topics that have one thing in of a new research field called ecotoxicology (Moriarty,
common: joining of fields such as ecology, physiology 1983). Often chemical and analytical analyses are too
and chemistry (Market, 2007). expensive and complicated, biomonitors representing a
Exposure to chemicals can’t be fully avoided and viable and efficient solution that does not require
the determination of the low levels of pollution sophisticated laboratory equipment.
requires great efforts (Harpin et al., 2004; Reimann et The present review aims to provide information on
al., 2003). Therefore, understanding, predicting and the selection and use of invertebrate groups, as
quantifying the pollution phenomena have both biomonitors of heavy metal pollution.
scientific and practical importance.
In the last decades, heavy metal contamination of SOIL INVERTEBRATES AS BIOMONITORS
the biotic component from ecosystems attracted the The edaphic invertebrate fauna includes those
attention of many scientists. Using biological animals that spend their entire life in the soil or part of
components as bio-indicators and biomonitors is a their development cycle. The classification criteria for
cheap and viable method (Hoodaji et al., 2012). the invertebrates that live in/on the ground are: body
Studies have shown that not only plants and fungi size, the capacity to adapt to the soil humidity
are able to tolerate and accumulate heavy metals, also conditions, the type of food, the connection with soil as
invertebrates. With these biological organisms can a living place, etc. Soil invertebrate fauna has an
measure the quantities of heavy metals accumulated in important role in the decomposition processes of plant
a reasonable period of time, the economic cost being material, contributing to soil genesis (Coleman et al.,
much lower cost than if it had been used chemical, 2004). Depending on the degree to which these
analytical methods of analysis. These species are invertebrates are involved in the processes of
considered biomonitors. A biomonitor is the body (or decomposition, the most important are: earthworms
part of an organism or a community of organisms) (Oligocheta), nematodes (Nematoda), springtails
which provides quantitative information on the (Collembola) and mites (Acari).
environment (Market, 2007).
This phenomen of the bioaccumulation has been
observed on different groups of animals since 1960,
when were noticed different concentrations of heavy
Correspondence*: Manu Minodora, Romanian Academy, Institute of Biology Bucharest, Department of Ecology, Taxonomy and
Nature Conservation, street Splaiul Independenţei, no. 296, code 0603100, PO-BOX 56-53, fax [phone], tel. [phone],
Bucharest, Romania; e-mail address: [email protected].
© 2017 Vasile Goldis University Press (www.studiauniversitatis.ro)
Manu M.

Taking into account the trophic biotic components and saprophagous land snails, which live on the soil,
of the debris food web, some authors estimated that have a high bioaccumulation capacity, due to their life
over 75% of the total energy assimilated by plants is conditions. The oligochete annelids are consider also
assimilated and redistributed to the ecosystem, with biomonitors. Taking into account the depth where they
contribution of soil fauna. After some evaluations, the are found in soil, the annelids are classified as: epigeic
highest amount of necromass, before mineralization species (in litter), endogeic species (in the top 10 cm of
process, is crossing the digestive tract of soil soil) and anecic species (in the few meters of soil).
invertebrates. Between 85-95% of the organic These are common species for temperate area and
fractions ingested by soil fauna, are returning to this as migrates on short distances. There are resistant and
manure. In this way, under the action of a soil fauna, a sensitive species to the pollution. Isopods are
significant amount of necromass is passing through a bioacumulators as well.
particular phase, called coprogenous phase, the The pollutants affect the soil fauna directly and
coprolites being favorable microhabitats for intense indirectly. The direct effects are associated with the
microbial processes (Mattew & Dindal, 1987; Walter pollutant transmission through the trophic chain, from
& Dindal, 1987; Walter et al., 1988; Van Straalen, one biotic component to another. These direct effects
1998; Walter & Proctor, 2003). are: decreasing of the reproduction rate, of their life
The atmospheric pollution and its impact on human cycle and even mortality. The indirect effects are: the
life, increased attention paid to the invertebrates. It was decreasing or disappearance of the food source for
determined that human intervention causes important invertebrates (fungi, microfauna), changes in organic
quantitative (density) and qualitative (diversity) matter content and modifications of the microclimate.
changes of the invertebrate populations from the Studies concerning the invertebrates’ usage as
affected ecosystems in comparison with those from biomonitors had been started from 1977-1978,
natural areas (Steiner, 1995; Skubala & Zaleski, 2012; observing that some arthropods (mites) are more
Santamaria et al., 2012; Manu et al., 2016). sensible to the heavy metal pollution. These researches
The pollution damages the connections between had been continued, till present (Williams et al. 1977;
different biotic components of the biocenosis. Strojan, 1978; Steiner 1995; Zaitsev and Van Straalen
Invertebrates, especially those that their taxonomy, 2001; Skubala & Kafel, 2004; Migliorini et al. 2005).
biology and ecology are well known, constitute the The biomonitoring studies had been realized in Europe
test-animal, which will be used more and more to (Netherlands, Finland, France, Poland, Belgium,
highlight the functional status of soils and possible Austria, Greece, Germany, England, Italy), beginning
modifications due to the pollution (Walter & Proctor, from 1984, till present, but also in Canada and Russia
2003). (Van Straalen & van Wensem, 1986; Morgan et al.,
Taking account of the body size, invertebrates are 1986; Weigmann, 1995; Russell & Alberti, 1998;
classified as following: Cortet et al., 1999; Devkota & Schmidt, 2000; van
- microfauna (species less than 0.02 mm): Protozoa Straalen et al., 2001; Seniczak & Seniczak, 2002;
and Nematoda. These live in the interstitial water from Scheifler, 2002; Skubala & Kafel, 2004; Khalil, 2009;
the soil. These invertebrates are used in ecotoxicology Heikens et al., 2010; Gongalsky et al., 2010;
studies of the soil and have a high bioaccumulation Butovsky, 2011; Skubala & Zaleski, 2012; Owojori &
potential. Protozoa were used for microcosm tests Siciliano, 2012; Ardestani, 2014).
(Eisenbeis G., 2006). In ecotoxicology projects from Romania, the
The toxicity tests from artificial soils that have been researches that used the invertebrates as biomonitors,
used nematodes are used in order to provide additional have been started from 2007 and they have been taken
information for the study of contaminants. In situ into consideration only few groups as: isopods,
studies which use nematodes are based on the analysis chilopods, diplopods and thrips (Giurginca, 2008;
of some maturity indices that bring new information on 2010; Ion, 2008; Oromulu-Vasiliu & Bărbuceanu,
soil structure. These indices can be used for 2008).
biomonitoring of conservation state or soil degradation
(Eisenbeis G., 2006). METHODS USED FOR THE DETERMINATION
- mesofauna (species with immensions between OF HEAVY METALS FROM SOIL
0.02 mm and 4 mm): Diplura, Acari, Collembola, INVERTEBRATE BODIES
Enchytreidae. Enchytraeids, that live in the top of soil, The methods for analysis are diverse, qualitative
are the most common invertebrates, having an and quantitative. The steps required for the heavy
important ecological role in descomposing and metals determination, involves three mandatory phases:
humification. They are macrophagous species, able to - sampling from monitored areas,
process the excrement of other invertebrates - the samples preparation for analysis - which
(earthworms and microarthropods). Only a few varies depending on the requirements of laboratory
ecotoxicological studies have used these species ex instruments and the type of samples; in this stage can
situ. The springtails (Collembola) and arachnids be found the following activities: acidification or acid
(Arachnida) are the most used groups for the digestion, filtration, preconcentration, etc.
ecotoxicology studies of soil (Eisenbeis G., 2006). -the analysis, which varies depending on the used
- macrofauna (bigger than 4 mm) : Araneida, equipment.
Opiliones, Pseudoscorpiones, Chilopoda, Diplopoda,
Isopoda, Lumbricidae, Pulmonata. The phytophagous
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Soil invertebrates- an usefull tool in biomonitoring of heavy metal pollution. A review

The most known equipment for the qualitative and The lab and field methods used to determine the
quantitative evaluation of the heavy metals, are: atomic concentrations of heavy metals from organisms /
absorption spectrometry (AAS), X ray fluorescence terrestrial invertebrates’ methods are varied. The
(XRF); inductively coupled plasma-mass spectrometry collection of biological material (invertebrates) was
(ICP-MS); plasma atomic emission spectroscopy (ICP- generally performed manually: by extraction, with
AES); ion chromatograph (IC); cold vapor atomic entomological net or by using the soil core. Sorting
fluorescence spectrometry (CVAF); advanced mercury was done using the Tullgren method (Table 1). For the
analyzer (AMA 254). Besides these, they are also lab analysis the most used methods for the
used: neutron activation analysis (NAA), atomic quantification of the heavy metal content was atomic
absorption spectrometry using atomization in a absorption spectrophotometry (Table 2).
graphite furnace (spectrometer 4100ZL Perkin-Elmer), Studies regarding the usage of invertebrates as
spectrometer Aanalyst 300 Perkin-Elmer- flame atomic biomonitors for heavy metal pollution had
absorption spectrometry. demonstrated that these accumulate chemical
Over time, this methodology varied depending on substances through food (vegetable matter, fungi or
the level of equipping, which became more and more other arthropods). More, fungivore species (mites,
modern, but also on the need to find simple solutions in springtails, enchytraeids) in the polluted environment
comparison with the laborious methods of work in the with heavy metals can change their trophical
laboratory. In addition, there are some other very preferences, due to the modifications of the
important aspects concerning these modern methods: development conditions of fungi or due to the change
the high cost of equipment and reagents; their of taste / their structure.
availability to a large volume of samples and not least
their level of detection.
Table 1
Methods for collecting and sorting of invertebrate fauna
Taxa Ecosystem Pollution The collected Sampling The extraction Lab processing Referen
source body parts and method method ce
the quantity
Carabidae
Deciduos Chemical The whole body Manual Tullgren All invertebrates Van
Isopodae
forests industries collection (for method were dried and Straalen
Lumbricid
(Capinus litter) and (mixture of kept in et al.,
ae
Collembol betulus, Salix 1-2 individuals mowing with water, refrigerator. They 2001
a sp., Betula for large species entomological glycerin and have been weight
Araneae pendula, or 10-20 net. etilic alcohol). with a Sartorius
Chilopoda Alnus incana) individuals for balance, till 1 μg
those smaller. dry weight for
small
invertebrates (as
mites). For bigger
invertebrates
(worms) 1-5 mg
of biological
material was
collected.
Carabidae
Forest with Mining The whole body Manual Tullgren All invertebrates Van
Collembol
Pinus and collecting and method were dried and Straalen
a 2 individuals for
sylvestris processing selecting; (individuals kept in & Van
Araneae large species or
of Zn aspiration. were refrigerator. They Wensem
Diplura 10-20
preserved in have been weight, , 1986
Acari individuals for
glass vials till 1 μg dry
Chilopoda those smaller.
with wet weight.
Pseudosco
stoppers.
rpionida
The whole body
Acari- Meadow Mining The samples Tullgren The individuals Skubala
Oribatida and were taken method were kept in a &
processing with soil core, mixture of water, Zaleski,
of Zn with diameter glycerin and 2012
by 4,8 cm. alcohol, on
refrigerator.
Five
ecosystems
were
investigated,
six samples
from each
ecosystem.
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Manu M.

Mollusca
Deciduous Deposits The whole body Manual The The invertebrates Morgan
Diptera
forest with collecting. invertebrates were kept in the et al.,
Diplopoda
heavy were washed refrigerator. 1986
Isopoda
metals with
Chilopoda
deionized
Lumbricid
water and then
ae
introduced in
Carabidae
immersion
liquid with N
2

Table 2:
Methods and equipment used for measurements of heavy metals concentrations from invertebrates’ bodies
Equipment Accessories Reagent Method Reference
Atomic absorption Graphite Calcium lactate Total carbon and nitrogen Van Straalen
spectrometry (AAS, furnace. 12.5% (pH=7) concentrations were measured by et al., 2001
Perkin-Elmer model Atropine burning of 1 - 5 mg duplicate Burghouts et
1100B), using CaCl samples, in a stream of pure al. 1998
2
atomization in a Acid ascorbic oxygen, in combination with
graphite furnace. Molybdate column chromatography and an
elemental analyzer (Carlo Erba
Estrumentazione, Milano, model
1106), using atropine (Merck,
Darmstadt) for calibration.
Determination of phosphorus was
done after extraction with 12,5%
calcium lactate (pH 7), measuring
phosphate colorimetrically with an
autoanalyzer (Skalar model SA
5100) at 880 nm, using the scorbic
acid-molybdate reagent.
Flameless atomic Pyrex tubes 1 M NH H PO Each samples was dried and Van Straalen
4 2 4
absorption L’vop platform Ultrex- grade deposited on refrigerator, in & Van
spectrometry (PE graphite nitric and quantities by 1 μg or 0,1 μg. The Wensem, 1986
3030, HGA 400, AS furnaces perchloric acid samples digestion was made using
40)- for Cd and Pb; (7:1) adapted method of the Bengtsson
for Zn was used and Gunnarsson (1984), with Pyrex
AAS (PE 4000) tubes and with ultrex- grade nitric
and perchloric acid (7:1)
Cd and Pb were measured using
atomic absorption spectrometer (PE
3030, HGA 400, AS 40) and L’vop
platform graphite furnaces. For Zn,
AAS (PE 4000) atomic absorption
spectrometer was used; measuring
the absorption peak at 100 ml
aliquots, withdraw from a titrator.
Flame atomic Analytic Acid nitric 50 individuals were analyzed, being Skubala &
absorption balance – AG- Distilled and weights three times, using AG-245 Zaleski, 2012
spectrometry - Solar 245 (Mettler deionized water balance (Mettler Toledo), with an -
939- for Zn Toledo) accuracy of ±0.01 mg, a repetabiliy
Atomic absorption of ±0.02 mg and linearity of ±
spectrometry with 0.03 mg. Species were dried and
electrothermal digested with concentrated acid
atomization for Cd, nitric (Suprapur grade, Merck) and
Cu. diluted with distilled and deionized
water.
Determination of metal
concentration was by flame atomic
absorption with flame (Solar 939-
for zinc) or electrothermal
atomization (for Cd, Cu). The
wavelengths for Zn, Cd and Cu
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Soil invertebrates- an usefull tool in biomonitoring of heavy metal pollution. A review
were 213.9 nm, 228.8 nm and 324.8
nm. The atomizing temperature was
2400 °C (Cd) or 2600 °C (Cu). The
injected sample volume into
graphite cuvette was 15 μl.
Atomic absorbtion Hydrogen lamp „Analar” grade Wet digestion, using nitric acid. Morgan et al.,
spectrometry- used to nitric acid 1986
(Pye/Unicam SP automatically
2900; compensate for
Varian-Techtron nonatomic
AA6) absorbtion.

HEAVY METALS FROM SOIL For one gram of dry weight, the higher
INVERTEBRATE BODIES concentrations of Cd were identified on different
The content of heavy metals from invertebrates species of beetles, mollusks, mites-oribatids and
represents the balance between the environment earthworms. High concentrations of Pb were identified
takeover and their disposal. If we take into on earthworms, isopods and mollusks. The mercury
consideration the studied invertebrate groups, this was identified only on few species of isopods and
takeover vary a lot, being a great difference in the millipedes (Table 3). The biomonitor groups for Fe are
concentrations of heavy metals determined. Unlike earthworms and beetles; for Zn: earthworms,
organochlorine compounds, heavy metals do not springtails, beetles, spiders, millipedes, mites,
accumulate along the food chain, except predatory pseudoscorpions and mollusks. Millipedes and mites
species that feed on bioaccumulation organisms are efficient biomonitors for Cu (Table 4).
(Gongalsky et al, 2010; Van Straalen et al., 2001). In Romania, the study of invertebrates’ biomonitors
Heavy metals from the arthropod bodies were has been considered the impact of the airborne heavy
classified in two categories: those mentioned in law metals pollutants in urban areas. Only few invertebrate
104/2011 (Pb, Cd, Ni, As, Hg) and others (Table 3). groups were analysed: diplopods, isopods, chilopods
and thrips (Table 3, 4).

Table 3:
The heavy metals identified in invertebrates body, according to national law no. 104/2011 (Pb, Cd, Ni, As, Hg)
(d.w.= dry weight; f.w.=fresh weight)
Taxa Species Pb Cd Hg Country Reference
Lumbricus castaneus < 0,5 μg g-1 23,6 μg g-1
Oligocheta -
Lumbricus rubellus d.w d.w
Lumbricidae
Lumbricus terrestris 8,18 μg g-1 8,04 μg g-1
Aporrectodea d.w d.w
Russia
caliginosa 12,5 μg g-1 6,2 μg g-1
England
Aporrectodea rosea d.w d.w
Van
Dendrobaena 1,41 μg g-1 11,1 μg g-1
Straalen et
mammalis d.w d.w
al., 2001
Lumbricus rutellus 126 μg g-1 26,9 μg g-1
Morgan et
Allolobophora d.w d.w
al., 1986
caliginosa 502 μg g-1 60 μg g-1 d.w
d.w 66 μg g-1 d.w
696 μg g-1 157 μg g-1
d.w d.w
5335 μg g-1
d.w
Orchesella cincta 1,54 – 5,4 0,13-12,1 μg
Collembola Russia Van
Orchesella flavescens μg g-1 d.w g-1 d.w
Straalen et
Tomocerus sp. 0,75 μg g-1 0,08 μg g-1
al., 2001
Tomocerus flavescens d.w d.w
Netherlands
Lepidocyrtus cyaneus 1,79 μg g-1 0,15 μg g-1
Isotoma notabilis d.w d.w
Van
1,12 μg g-1 0,12 μg g-1
Straalen &
d.w d.w
van
24,7 mg kg-1
Wensem,
d.w.
1986
65,2 mg kg-1
d.w.
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Manu M.

Agonum assimile 59,6 μg g-1 9,16 μg g-1
Coleoptera Russia
Agonum obscurum d.w d.w
Pterostichus niger 35,2 μg g-1 2,32 μg g-1
Pterostichus d.w d.w
oblongopunctatus 12,4 μg g-1 5,16 μg g-1
Calathus melanocephalus d.w d.w

Notrophilus bigttatus 41,4 μg g-1 7,37 μg g-1
Notrophilus rufipes d.w d.w Netherlands Van Straalen et
Lathrobium brunnipes 12,3 mg kg-1 10,5 mg kg-1 al., 2001

Abax sp (3 individuals) d.w. d.w.
Agonum sp. (2 5,3 mg kg-1 18,2 mg kg-1 Russia Van Straalen &
individuals) d.w. d.w. van Wensem,
Calathus sp. (4 9,5 mg kg-1 21,2 mg kg-1 1986
individuals) d.w. d.w.
Carabus sp. (9 7,1 mg kg-1 44,3 mg kg-1 Butovsky, 2011
individuals) d.w. d.w.
Leistus sp. (2 individuals) 0,1 ppm d.w. 3,1 ppm d.w England
Loricera sp. (1 - 4,9 ppm d.w
individuals) 1 ppm d.w 6,7 ppm d.w
Nothiophilus sp. (2 0,1 ppm d.w 4,3 ppm d.w Morgan et al.,
individuals) 2,9 ppm d.w 7,8 ppm d.w 1986
Poecilus sp. (2 - 1,9 ppm d.w
individuals) 1,7 ppm d.w 1,7 ppm d.w
Pseudo-ophonus sp. (1 0,1 ppm d.w 4,2 ppm d.w
individuals) - 3 ppm d.w
Pterostichus sp. (5 - 2,9 ppm d.w
individuals) 62 μg g-1 d.w 5 μg g-1 d.w
Perostichus madidus
Isopoda Hyloniscus riparius 2,50 μg g-1 1,55 μg g-1 Russia Van Straalen et
Porcellio scaber d.w d.w England al., 2001
Philoscia muscorum 22 μg g-1 d.w 22 μg g-1 d.w Morgan et al.,
Oniscus asellus 543 μg g-1 57 μg g-1 d.w 1986
Trachelipus arcuatus d.w 72 μg g-1 d.w 0,70 μg g-1 Romania
Cylisticus convexus 813 μg g-1 0,53 μg g-1 d.w
Armadillidium vulgare d.w d.w 0,34 μg g-1 Giurgincă et al.,
2,04 μg g-1 0,20 μg g-1 d.w 2008
d.w d.w 0,33 μg g-1
7,46 μg g-1 0,26 μg g-1 d.w
d.w d.w
7,5 μg g-1
d.w
Araneae Pardosa sp. 0,61 μg g-1 1,28 μg g-1 Russia Van Straalen et
d.w d.w al., 2001
Myriapoda Centromerus sylvaticus 5 mg kg-1 176,9 mg kg-1 Netherlands Van Straalen &
d.w. d.w. van Wensem,
1986
Centromerus sylvaticus 0,99 μg g-1 0,44 μg g-1 Russia Van Straalen et
d.w d.w al., 2001
Lithobius forficatus 31,9 mg kg-1 19,9 mg kg-1 Van Straalen &
Netherlands
d.w. d.w. van Wensem,
1986
Schendyla nemorensis 2,6 mg kg-1 149,4 mg kg-1 Van Straalen &
Netherlands
d.w. d.w. van Wensem,
1986
Lithobius variegatus 480 μg g-1 52 μg g-1 d.w. England Morgan et al.,
d.w 1986
Polydesmus angustus 47 μg g-1 d.w England Morgan et al.,
1986
Megaphyllum unilineatum 9,03 μg g-1 0,08 μg g-1 0,10 μg g-1 Romania Giurgincă et al.,
d.w d.w d.w 2008
Acari-Oribatida Chamobates cuspidatus 185 μg g-1 375 μg g-1 d.w Russia Van Straalen et
d.w al., 2001
Chamobates cuspidatus 65,2 mg kg-1 Netherlands Van Straalen &
d.w. van Wensem,
1986
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Soil invertebrates- an usefull tool in biomonitoring of heavy metal pollution. A review

Tectocepheus velatus 2519 μg g-1 Poland Skubala &
f.w Zaleski, 2012

Punctoribates punctum 6554 μg g-1 Poland Skubala &
f.w Zaleski, 2012
Scutovertex sculptus 2089 μg g-1 Poland Skubala &
f.w Zaleski, 2012
Oribatula tibialis 1,925μg g-1 Poland Skubala &
f.w Zaleski, 2012
Peloptulus phaeonotus 5396 μg g-1 Poland Skubala &
f.w Zaleski, 2012
Diplura Camphodea staphylinus 141,7 mg kg-1 Netherlands Van Straalen &
d.w. van Wensem,
1986
Pseudoscorpionida Neobisium muscorum 155,2 mg kg-1 Netherlands Van Straalen &
d.w. van Wensem,
1986
Mollusca Hygromia hispida 176 μg g-1 25 μg g-1 d.w. England Morgan et al.,
d.w 1986
Deroceras caruanae 363 μg g-1 53 μg g-1 d.w. England Morgan et al.,
d.w. 1986
Deroceras reticutalum 254 μg g-1 37 μg g-1 d.w. England Morgan et al.,
d.w 1986
Diptera Tipula paludosa 439 μg g-1 33 μg g-1 d.w. England Morgan et al.,
d.w 1986
Tysanoptera Frankliniella intonsa 0,60-8,40 Romania Oromulu-
ppm d.w. Vasiliu &
Bărbuceanu,
2008
Haplothrips niger 0,80-6,17 Romania Oromulu-
ppm d.w Vasiliu &
Bărbuceanu,
2008
Bagnaliella yuccae 6,94-15,53 Romania Oromulu-
ppm d.w. Vasiliu &
Bărbuceanu,
2008

Table 4
The heavy metals identified in invertebrates body, other than those mentioned in the national law no. 104/2011 ( Co, Cr,
Cu, Fe, Mn, Zn) (d.w.= dry weight; f.w.=fresh weight).
Organism Species Fe Zn Cu Mn Co Cr Country Author
Lumbricus 909 μg 3336 19,5
Oligocheta - castaneus g-1 d.w μg g-1 μg g- Russia Van Straalen
Lumbricidae Lumbricus rubellus 825 μg d.w 1d.w England et al., 2001
Lumbricus g-1 d.w 385 μg 11 μg Morgan et
terrestris 3309 μg g-1 d.w g-1 d.w al., 1986
Aporrectodea g-1 d.w 485 μg 9,3 μg
caliginosa 390 μg g-1 d.w g-1 d.w
Aporrectodea g-1 d.s 480 10,2
rosea 374 μg μg g-1 μg g-
Dendrobaena g-1 d.s d.w 1d.w
mammalis 355 μg 15,5
Lumbricus rutellus g-1 d.w μg g-
Allolobophora 621 1d.w
caliginosa μg g-1
d.w
1187
μg g-1
d.w
1280
μg g-1
d.w
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253
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Manu M.

Collembola Orchesella cincta 699 μg 793- 6,22 Russia Van Straalen
Orchesella g-1 d.w 1100 μg g- Netherlands et al., 2001
flavescens 329 μg μg g-1 1d.w Van Straalen
Tomocerus sp. g-1 d.w d.w 4,38 & Van
T. flavescens 560 μg 587 μg μg g- Wensem,
Lepidocyrtus g-1 d.w g-1 d.w 1d.w 1986
cyaneus 490 μg 719 μg 6,95
Isotoma notabilis g-1 d.w g-1 d.w μg g-
503 μg 1d.w
g-1 d.w 5,33
700 μg g-
mg kg- 1d.w
1 d.w.
840
mg kg-
1 d.w.
Agonum assimile 59,6 μg 140 μg 32,4
Coleoptera Agonum obscurum g-1d.w g-1 d.w μg g- Russia Van Straalen
Pterostichus niger 438 μg 788 μg 1d.w Netherlands et al., 2001
P. g-1d.w. g-1 d.w 5,80 Van Straalen
oblongopunctatus 160 μg 126 μg μg g- England & van
Calathus g-1 d.w g-1 d.w 1d.w Wensem,
melanocephalus 210 μg 170 μg 13,1 1986
Notrophilus g-1 d.w g-1 d.w μg g-
bigttatus 1080 1d.w Butovsky,
Notrophilus rufipes mg kg- 15,6 2011
24.3
Lathrobium 1 d.w. μg g-
ppm Morgan et
brunnipes 1250 1d.w
d.w al., 1986
Abax sp. (3 mg kg-
29.1
indivizi) 532.2 1 d.w.
ppm
Agonum sp. (2 ppmd.w 860
d.w
indivizi) 58.7 mg kg-

Calathus sp. (4 ppm d.w 1 d.w. 15.9

indivizi) 333.9 3600 ppm
Carabus sp. (9 ppmd.w mg kg- d.w

indivizi) 1 d.w. 25.8 29.2
Harpalus sp. (1 62.8 ppm
ppm
individ) 117.1 ppm d.w
d.w
Leistus sp. (2 ppmd.w d.w 52.7

indivizi) 95 ppm
Loricera sp. (1 461.2 ppm d.w
individ) ppmd.w d.w 16.9

Nothiophilus sp. (2 436.3 89.2 ppm
indivizi) ppmd.w ppm d.w
Poecilus sp. (2 d.w 23.3

indivizi) 96.1 ppm
Pseudoophonus sp. ppm d.w
(1 individ) d.w 30.1
Pterostichus sp. (5 130 ppm
indivizi) ppm d.w

Perostichus d.w
madidus 118.6 27.5
ppm ppm

d.w d.w
16.3
77.9 ppm
ppm d.w
d.w 17.3

118.7 ppm
ppm d.w
d.w 29.5

92.3 ppm
ppm d.w
d.w
116.2
ppm
d.w
248 μg
g-1 d.w

Studia Universitatis “Vasile Goldiş”, Seria Ştiinţele Vieţii
254
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Soil invertebrates- an usefull tool in biomonitoring of heavy metal pollution. A review
Hyloniscus 732 μg 25,3 2,96 Russia Van Straalen
Isopoda riparius g-1 d.s μg g-1 μg g-1 England et al., 2001
Porcellio scaber d.s d.s Romania Morgan et
Philoscia 1005 al., 1986
muscorum μg g-1 0,06 0,012 0,22 Giurgincă et
Oniscus asellus 0,75 mg d.s 0,18 mg g- mg g-1 mg al., 2008
Trachelipus g-1 d.w. 130 μg mg g-1 1 d.w. d.w. g-1
arcuatus 1,17 mg g-1 d.s d.w. 0,083 0,018 d.w.
Cylisticus g-1 d.w. 299 μg 0,21 mg g- mg g-1 0,07
convexus 1 mg g-1 g-1 d.s mg g-1 1 d.w. d.w. mg
Armadillidium d.w. 0,22 d.w. 0,072 0,017 g-1
vulgare mg g-1 0,26 mg g- mg g-1 d.w.
d.w. mg g-1 1 d.w. d.w. 0,17
0,075 d.w. mg
mg g-1 g-1
d.w. d.w.
0,15
mg g-1
d.w.
Araneida Pardosa sp. 13,1 Russia Van Straalen
272 μg 197 μg
μg g-1 et al., 2001
g-1 d.s g-1 d.s
d.s
Centromerus Netherlands Van Straalen
4370
sylvaticus & van
mg kg-
Wensem,
1 d.w.
1986
Myriapoda Lithobius 5,51 Russia Van Straalen
582 μg 182 μg
forficatus μg g-1 et al., 2001
g-1 d.w g-1 d.w
d.w
Lithobius Netherlands Van Straalen
forficatus 2850 & van
mg kg- Wensem,
1 d.w. 1986
Lithobius 1608 England Morgan et
variegatus μg g-1 al., 1986

d.w

Schendyla Netherlands Van Straalen
6050
nemorensis & van
mg kg-
Wensem,
1 d.w.
1986
Polydesmus 406 μg England Morgan et
angustus g-1 d.w al., 1986

Lithobius muticus 16,47 31,94 mg/kg Romania Ion, 2008
μg g-1 μg g-1
d.w d.w
Lithobius lucifugus 21,68 40,07 Romania Ion, 2008
μg g-1 μg g-1
d.w d.w
Lithobius 31,7 Romania Ion, 2008
470 μg
variegatus μg g-1
g-1 d.w
d.w
Megaphyllum 0,4 Romania Giurgincă et
0,23 0,96
unulineatum 0,47 mg mg al., 2008
mg g-1 mg g-1
g-1 d.w. g-1
d.w. d.w.
d.w.
Acari-Oribatida Chamobates 37,4 Russia Van Straalen
2638 μg 545 μg
cuspidatus μg g-1 et al., 2001
g-1 d.w g-1 d.w
d.w
Chamobates Netherlands Van Straalen
cuspidatus 5580 & van
mg kg- Wensem,
1 d.w. 1986
Studia Universitatis “Vasile Goldiş”, Seria Ştiinţele Vieţii
255
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Manu M.

Tectocepheus 2038,2 307,34 Poland Skubala &
velatus μg g-1 μg g-1 Zaleski, 2012
f.w f.w
Punctoribates 98,53 16,16 Poland Skubala &
punctum μg g-1 μg g-1 Zaleski, 2012
f.w f.w

Scutovertex 64 μg 1392 Poland Skubala &
sculptus g-1 f.w μg g-1 Zaleski, 2012
f.w

Oribatula tibialis 584,72 187,80 Poland Skubala &
μg g-1 μg g-1 Zaleski, 2012
f.w f.w

Peloptulus 142 μg 73,30 Poland Skubala &
phaeonotus g-1 f.w μg g-1 Zaleski, 2012
f.w

Diplura Camphodea 3130 Netherlands Van Straalen
staphylinus mg kg- & van
1 d.w. Wensem,
1986
Pseudoscorpionida Neobisium 4880 Netherlands Van Straalen
muscorum mg kg- & van
1 d.w. Wensem,
1986
Mollusca Hygromia hispida 437 μg England Morgan et
g-1 d.w al., 1986

Deroceras 515 μg England Morgan et
caruanae g-1 d.w al., 1986

Deroceras 619 μg England Morgan et
reticutalum g-1 d.w al., 1986

Diptera Tipula paludosa 483 μg England Morgan et
g-1 d.w al., 1986

Tysanoptera Frankliniella 1,39- 7,53- Romania Oromulu-
intonsa 6,26 42,68 Vasiliu &
ppm ppm Bărbuceanu,
d.w. d.w. 2008
Haplothrips niger 2,11- 16,91- Romania Oromulu-
15,71 60,64 Vasiliu &
ppm ppm Bărbuceanu,
d.w. d.w. 2008
Bagnaliella yuccae 1,88- 34,74- Romania Oromulu-
16,62 44,08 Vasiliu &
ppm ppm Bărbuceanu,
d.w. d.w. 2008
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