Review Article |
Corresponding author: Cornelis A.M. van Gestel ( kees.van.gestel@vu.nl ) Academic editor: Elisabeth Hornung
© 2018 Cornelis A.M. van Gestel, Susana Loureiro, Promoz Zidar.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
van Gestel CAM, Loureiro S, Zidar P (2018) Terrestrial isopods as model organisms in soil ecotoxicology: a review. In: Hornung E, Taiti S, Szlavecz K (Eds) Isopods in a Changing World. ZooKeys 801: 127-162. https://doi.org/10.3897/zookeys.801.21970
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Isopods play an important role in the decomposition of leaf litter and therefore are making a significant contribution to nutrient cycling and soil ecosystem services. As a consequence, isopods are relevant models in soil ecotoxicology, both in laboratory toxicity tests and in field monitoring and bioindication studies. This paper aims at reviewing the use of isopods as test organisms in soil ecotoxicology. It provides an overview of the use of isopods in laboratory toxicity tests, with special focus on comparing different exposure methods, test durations, and ecotoxicological endpoints. A brief overview of toxicity data suggests that chemicals are more toxic to isopods when exposed through soil compared to food. The potential of isopods to be used in bioindication and biomonitoring is discussed. Based on the overview of toxicity data and test methods, recommendations are given for the use of isopods in standardized laboratory toxicity tests as well as in situ monitoring studies.
Bioaccumulation, biomonitoring, indicator organisms, Isopoda , toxicity tests
Increasing human activities have caused serious effects on man and the environment. Since the industrial revolution in the 19th century, pollution from industries and metal contamination from mining activities has increased. In the 20th century, after the Second World War, the massive use of pesticides resulted in widespread environmental pollution. The first evidence of chemical pollution was shown by air pollution, for instance leading to smog episodes in cities. Air pollution was a major problem already in the 19th century and still is one of the major factors threatening human health, especially in rapidly developing industrial regions like China (see e.g.,
Apart from threatening human health, air, water and soil pollution may also affect ecosystems. By affecting major functions of natural systems, pollution can alter the so-called ecosystem services (
Pollution may damage ecosystems and by that the support ecosystems provide to (the quality of) human life. Protection of ecosystem services therefore is essential not only for safeguarding the health of our ecosystems but also for our own benefit (
Isopods play an important role in the functioning of soil ecosystems and therefore also in the ecosystem services provided by soils. They act mainly on the first processes of litter fragmentation, contributing to the input of high quality organic matter, and increasing the microbiome for further nutrient cycling in soil (
After the publication of the book Silent Spring by Rachel
Environmental chemistry provides insight into the way chemicals interact with components of the environment, determining their fate, and therefore also the exposure of organisms and ecosystems. From knowledge of persistence and partitioning, environmental chemistry enables estimating Predicted Environmental Concentrations (PEC), which are the starting point for the risk assessment of chemicals. One important issue is bioavailability: the notion that total concentration of a chemical in the environment is not indicative of its risk, because only a fraction of it may be available for uptake and therefore causing effects (
Toxicology provides insight into the interaction of chemical pollutants with molecules, tissues, and organs resulting in effects at the molecular and individual level (
Ecology provides the knowledge for the extrapolation from individual-level effects to effects on populations, communities, and ecosystems. Ecology adds knowledge about life histories of organisms, their functioning in different processes or their interactions with other species or the abiotic environment. Knowledge on life histories and other ecological properties or traits of species also helps understanding how organisms will be exposed to chemicals in the environment and how this may affect populations. The behaviour of an organism may for instance differ depending on its life stage, while it may have great influence on exposure. Again, this seems even more important in soils, where pollution is only rarely distributed homogenously. Finally, knowledge about ecological interactions between species may help translating effects to the community and ecosystem level.
Ecotoxicology may follow predictive/prospective and diagnostic/retrospective approaches (
Diagnostic approaches are applied to monitor possible effects of chemicals after introduction onto the market, e.g., as post-registration monitoring of pesticides, or to assess the actual risk of contaminated soils. Diagnostic risk assessment, for instance of contaminated soils, relies on a combination of ecological, toxicological and chemical approaches. Basically, toxicity tests (in this case usually called bioassays) are used as diagnosis tools to assess the toxicity of soil samples from the contaminated site. Results of the bioassays are considered together with those of measurements of total or available concentrations of a selected number of chemicals and ecological field observations. The added value of bioassays is that they provide information on the actual risk of bioavailable concentrations of all chemicals present in the contaminated samples; such information cannot be obtained from chemical analyses (see e.g.,
One key issue in ecotoxicological risk assessment is the selection of test species for generating the required toxicity data. For a proper risk assessment it is crucial that test species are representative of the community or ecosystem to be protected. Criteria for selection of tests and therefore also for organisms to be used in toxicity tests have been summarised by
There is no species that is most sensitive to all pollutants. Which species is most sensitive depends on the mode of action and possibly also other properties of the chemical, and the properties of the organism (e.g., presence of specific targets, physiology, etc.). It is therefore important to always test a number of species, with different life traits, functions, and position within a trophic chain. Such a battery of test species should be (according to
Once tests have been developed, accepted, and validated, they may be standardised by international organisations like the International Standardization Organization (ISO) or the Organization for Economic Co-operation and Development (OECD). Chemical registration authorities usually only accept results of tests standardised by these organisations. For the soil environment different OECD and ISO standardised tests are available (for an overview see e.g.,
The ecological relevance of isopods, their typical routes of exposure (soil, food) and life history characteristics, the possibility to determine different endpoints (see below), and the fact that they have already been used for testing for more than 30 years, make them highly suitable test organisms (
In terrestrial systems, several pollutants can reach the soils from diverse sources and can also be found in decaying organic matter. These sources can be considered as point and/or diffuse (non-point) and they will include different forms of contamination: gaseous (atmospheric), solid or liquid hazardous substances that will be mixed with soil.
Industry and commerce are two of the major economic sectors responsible for soil contamination (36 %), either by negligence or by accident (European Environment Agency (EEA); www.eea.europa.eu). This includes atmospheric emissions from production, spilling or burying chemical substances directly in the soil or through runoff from surrounding areas. Such polluted sites are common in Europe and worldwide, and are commonly named as historically-contaminated sites, where metals (37.3 %) and mineral oils (33.7 %) are the main harmful substances to be considered, followed by Polycyclic Aromatic Hydrocarbons (PAHs) (13.3 %), Aromatic Hydrocarbons (BTEX) (6 %), phenols (3.6 %), chlorinated hydrocarbons (2.4 %), and other chemical compounds (3.6 %) (EIONET priority data, EEA). Along with industrial and commercial sources, waste treatment and disposal is another main source of soil contamination (EEA; www.eea.europa.eu). Sewage sludge is often applied to agricultural fields as fertiliser. This provides a considerable input of hazardous substances to soils, some of them considered as emerging pollutants, like those in daily care products, pharmaceuticals, or nanomaterials. In addition, Phthalates (e.g., diethylhexylphthalate (DEHP), dibutylphthalate (DBP)), Octylphenols, Nonylphenols, Linear alkylbenzene sulfonates (LAS), Polychlorinated biphenyls (PCBs), PAHs and metals are amongst the substances most commonly found in sewage sludge that is applied to soils for agricultural purposes. Considering this cocktail of chemicals along with pesticides and fertilisers, agricultural soils are a major sink for contaminants. Pesticides have been introduced by man in ecosystems initially as natural compounds, by using poisonous plants or extracting chemical substances from other natural sources. Later in the 20th century, especially after the 2nd World war, anthropogenically modified or synthesised compounds have been introduced at a large scale, that nowadays represent a wide range of organic chemical groups, including organophosphates, carbamates, triazines, organochlorines, pyrethroids, neonicotinoids, sulfonylurea and biopesticides (EEA; www.eea.europa.eu).
Along with agricultural areas, urban areas have been identified as hotspots for soil contamination (
Lately emerging chemicals like nanomaterials (e.g., nanoparticles) are showing a potential risk to aquatic and terrestrial organisms as they are being used for different applications and are expected to appear in the environment, mainly through sewage sludge discharges. Recently also microplastics have been added to this list of pollutants potentially threatening the soil environment (
In addition to chemical stress, natural stress can also affect the performance of soil organisms, including isopods. Considering their evolution from water to land, terrestrial isopods have acquired several features to succeed their appearance in terrestrial environments. One limiting habitat property is moisture content, while temperature, salinity, and UV radiation increase are also of importance. These factors can become stressors on their own when tending to extremes but they can also act as joint stressors in addition to chemicals. This joint effect can be caused by the interaction of stressors in exposure media but most interestingly also inside the organisms. It is known that several environmental conditions like temperature fluctuation patterns will influence an organism’s physiology and behaviour, changing therefore the metabolism of chemicals upon exposure or affecting its behaviour, e.g., its aggregation behaviour (
In soil, chemicals may be distributed over different compartments, the soil solid phase, pore water, and air. Isopods living on and in the soil may be exposed to all three compartments, with food acting as another compartment from which chemicals may be taken up. Very little data is available on the way isopods are exposed and on what the relative importance of each route of exposure is. Likely, the relative importance of either route of exposure is dependent on the properties of the chemical, including its volatility, water solubility and sorption or soil/water partition constant, and the properties of the soil, like organic matter content, clay content, and pH. As a consequence of these factors, bioavailability and therefore exposure may be quite different for soil and food. For volatile chemicals inhalation may present another route of uptake, which again will be hard to quantify. It therefore remains hard to predict the role of either route of exposure, and this will also require knowledge of several factors related to isopod behaviour (see
In the toxicity tests described in the literature, generally two routes of exposure have been tested, usually separately: exposure to food only or to soil only (see Table
Summary of data on the toxicity of chemicals to isopods in different tests with exposures in soil or through food. For each chemical, species and endpoint, the lowest value is reported. For a more complete overview of data, it is referred to the Supporting Information.
Test compound | Species | Soil/food | Time (d) | Criterion | Endpoint | Result (mg/kg dry soil or food) | Reference |
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2-phenylethyl isothiocyanate | Porcellio scaber | food | 28 | LC50 | survival | >1000 |
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Lufa2.2 | 28 | LC50 | survival | 65.3 | |||
3-phenylpropionitrile | Porcellio scaber | food | 28 | LC50 | survival | >1000 |
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Lufa2.2 | 28 | LC50 | survival | 155 | |||
abamectin | Porcellio scaber | Lufa 2.2 | 21 | LC50 | survival | 69 |
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Lufa 2.2 | 21 | NOEC | weight loss | 3 |
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AgNO3 | Porcellionides pruinosus | food | 14 | EC50 | growth | 233 |
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Lufa 2.2 | 14 | LC50 | survival | 396 | |||
14 | EC50 | consumption | 56.7 | ||||
2 | EC50 | avoidance | 13.9 | ||||
AgNPs | Porcellionides pruinosus | food | 14 | EC50 | growth | >1500 |
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Lufa 2.2 | 14 | LC50 | survival | >455 | |||
14 | EC50 | growth | 114 | ||||
2 | EC50 | avoidance | 15.8 | ||||
benomyl | Porcellionides pruinosus | 2 Soils | 14 | LC50 | survival | >1000 |
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benzo[a]anthracene | Oniscus asellus | food | 329 | NOEC | growth | 3 |
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Porcellio scaber | food | 112 | NOEC | growth | >9.6 | ||
benzo[a]pyrene | Oniscus asellus | food | 63 | NOEC | growth | 10.6 |
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Porcellio scaber | food | 63 | NOEC | growth | 10.6 | ||
bisphenol A | Porcellio scaber | sandy soil | 112 | NOEC | growth | ≤10 |
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70 | LC50 | survival | 910 |
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carbendazim | Porcellionides pruinosus | 2 Soils | 14 | LC50 | survival | >1000 |
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Cd | Armadillidium vulgare | food | 21 | NOEC | MT/ HSP70 expression | 43.14 |
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Oniscus asellus | food | 91 | LC50 | survival | ~1600 |
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Porcellio scaber | food | 308 | LC50 | survival | 86 |
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70 | EC10 | growth/biomass | 1.35 |
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21 | LOEC | food selection | 20 |
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21 | NOEC | moulting/survival | >200 | ||||
Porcellionides pruinosus | food | 28 | EC50 | egestion ratio | 370 |
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28 | LOEC | assimilation efficiency | 19850 | ||||
chloranthraniliprole | Porcellio scaber | Lufa 2.2 | 32 | LC50 | survival | >1000 |
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32 | NOEC | growth | >1000 | ||||
chlorpyrifos | Porcellionides pruinosus | Lufa 2.2 | 14 | NOEC | biomass | ≥3 |
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Cu | Porcellio scaber | food | 28 | EC10 | growth | 45 |
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28 | LC50 | survival | 1117 | ||||
Lufa 2.2 | 28 | NOEC | growth | 500 |
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28 | LC50 | survival | 3755 | ||||
Porcellionides pruinosus | food | 28 | EC50 | consumption ratio | 1038 |
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28 | EC50 | egestion ratio | 483 | ||||
28 | LOEC | assimilation efficiency | >10500 | ||||
Lufa 2.2 | 2 | EC50 | avoidance behavior | 802 |
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dimethoate | Porcellio scaber | food | 28 | LC50 | survival | >75 |
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28 | NOEC | growth | >75 | Hornung et al. 1998 | |||
2 soils | 28 | EC10 | female gravidity | 3.8 |
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Lufa 2.2 | 28 | NOEC | growth | 10 |
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28 | NOEC | food consumption | 10 | ||||
Porcellio dilatatus | black silt | 2 | NOEC | active time | <5 |
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Porcellionides pruinosus | Lufa 2.2 | 2 | EC50 | avoidance behavior | 28.7-39.7 |
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doramectin | Porcellio scaber | Lufa 2.2 | 21 | LC50 | survival | >300 |
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endosulfan | Porcellio dilatatus | food | 21 | NOEC | glycogen / lipids | <0.1 |
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fluoranthene | Oniscus asellus | food | 329 | NOEC | growth, reproduction | >267 |
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fluorene | Oniscus asellus | food | 329 | NOEC | protein (females) | 7 |
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Porcellio scaber | 112 | NOEC | growth | >219 | |||
glyphosate | Porcellionides pruinosus | Lufa2.2 | 2 | EC50 | avoidance behavior | 39.7 | Santos et al. 2010 |
imidacloprid | Porcellio scaber | food | 14 | NOEC | growth | 5 |
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Lufa 2.2 | 28 | LC50 | survival | 7.6 |
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lambda-cyhalothrin | Porcellionides pruinosus | 2 Soils | 14 | LC50 | survival | 0.5-1.4 |
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14 | EC50 | reproduction | 0.13-0.4 | ||||
lasalocid | Porcellio scaber | Lufa 2.2 | 28 | NOEC | growth | 202 |
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2 | NOEC | avoidance behavior | <4.51 | ||||
mancozeb | Porcellionides pruinosus | Lufa 2.2 | 14 | NOEC | biomass | 176 |
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Ni | Porcellionides pruinosus | Lufa2.2 | 1-8 | NOEC | integrated biomarkers | 50 |
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parathion | Porcellio dilatatus | food | 21 | NOEC | AChE | <0.1 |
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Pb | Armadillidium vulgare | food | 21 | NOEC | MT/ HSP70 expression | 478 |
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Porcellio scaber | food | 80 | NOEC | oxygen consumption | 1178 |
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Porcellionides pruinosus | food | 28 | EC50 | egestion ratio | 14050 |
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28 | LOEC | assimilation efficiency | >42070 | ||||
28 | LOEC | growth efficiency | >31790 | ||||
phenanthrene | Oniscus asellus | food | 329 | NOEC | growth, reproduction | >235 |
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Porcellionides pruinosus | Lufa 2.2 | 14 | LC50 | survival | 110-143 |
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14 | EC50 | biomass | 16.6-31.6 | ||||
spirodiclofen | Porcellionides pruinosus | Lufa2.2 | 2 | EC50 | avoidance behavior | 0.9 | Santos et al. 2010 |
thiacloprid | Porcellio scaber | Lufa 2.2 | 28 | LC50 | survival | >32 |
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28 | EC50 | consumption | >32 | ||||
TiO2 NPs | Porcellio scaber | food | 3 | NOEC | CAT/GST | >3000 |
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tributyltin | Porcellionides pruinosus | food | 14 | NOEC | consumption rate | 1 |
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soil | 14 | LC50 | survival | 99.2 | |||
2 | EC50 | avoidance behavior | <0.2 | ||||
vinclozolin | Porcellio scaber | sandy soil | 70 | LC50 | survival | 298 |
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35 | NOEC | molt delay | 10 | ||||
Zn | Porcellio scaber | food | 72 | EC50 | growth | 1916 |
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35 | NOEC | fecal production | 1000 |
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Porcellionides pruinosus | food | 28 | EC50 | consumption ratio | 11100 |
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28 | EC50 | assimilation efficiency | 3650 | ||||
28 | EC50 | egestion ratio | 3520 | ||||
4 Soils | 14 | LC50 | survival | 1792-2352 |
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14 | EC50 | biomass | 312-1400 | ||||
ZnO non-nano | Porcellionides pruinosus | 4 Soils | 14 | LC50 | survival | 2169-2894 |
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14 | EC50 | biomass | 119-1951 | ||||
ZnO NPs (3–8 nm) | Porcellionides pruinosus | 4 Soils | 14 | LC50 | survival | 1757->3369 |
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14 | EC50 | biomass | 713-1479 |
Food can be an important route of exposure, especially in case of input from the air with freshly fallen decaying leaves containing high levels of pollution. Food exposure may also be more uncertain and more difficult to quantify due to the possibility of isopods avoiding contaminated food. It is known that isopods may be able to survive for very long time without food (
In addition, it should be noted that organisms may affect exposure by their behaviour. Feeding behaviour affects the dietary exposure, while mobility may play a role in determining the degree of contact with soil and therefore may affect soil exposure.
It will be difficult to construct an experiment that completely separates the different exposure routes. This also is not necessary when the focus is not on the mechanisms behind uptake and accumulation but rather on the consequences of exposure in terms of the toxicity. The amount of chemical accumulated instead of the concentration in the environment might provide a suitable measure of exposure and integrates aspects of bioavailability and route of exposure (
It is also not self-evident that the route of exposure will be the same under laboratory and field test conditions. In most standard laboratory tests, the test animal is kept on a relatively thin, homogeneous soil layer and is (if food is provided) forced to feed on a single food item (
The first record on relating isopods to terrestrial contamination was a study from Martin et al., in 1976, where the availability and uptake of several metals from woodland litter were recorded and described in the woodlouse Oniscus asellus. In 1977, this species was mentioned as a biomonitor of environmental cadmium (
In 1991, Armadillidium vulgare appeared as a test species in a study on the sequestration of copper and zinc in the hepatopancreas, and its relation with previous exposure to lead (
Porcellionides pruinosus has more recently been proposed as a suitable test species for ecotoxicity testing. The advantage of this species is its somewhat shorter life cycle making it easier to culture, and therefore it is more suitable for performing reproduction toxicity tests (e.g.,
Based on the above, it remains difficult to recommend one or the other species for toxicity isopod testing. A toxicity test with isopods may therefore use different species, but its duration and design may differ depending on the species chosen.
Although no standard test guidelines are available for assessing chemical toxicity to isopods, they are used as test organisms, applying different routes of exposure (food, soil), different test durations, and different endpoints. Table
1 Design of feeding inhibition tests with isopods, applying exposure through food (left) or to contaminated soil with contaminated or uncontaminated food (right). In the test with contaminated food only, the animals are kept on a net or gauze allowing also for collecting faeces produced; this will enable estimating food assimilation efficiency. By offering the animals pre-weighed disks or pieces of leaf, food consumption can easily be determined. 2 Design of an avoidance test with isopods. The test uses containers with two compartments. One compartment is filled with contaminated soil, the other one with clean soil. After two days of exposure, the position of the animals in the container is checked. By testing a range of concentrations, including a control (clean soil in both compartments), a dose-response relationship for avoidance may be obtained. The test may also be used to assess avoidance responses to field-contaminated soils, but in that case it might be more difficult to find a proper control soil. Drawing made by Paula Tourinho.
Toxicity tests with isopods in soil use either artificial soil, prepared following the methods described by
Toxicity tests with isopods have been carried out with several endpoints (Tables
Overview of isopod toxicity and bioaccumulation test methods described in the literature. References are just given as an example; in many cases several papers are available describing a more or less similar method of testing. For an overview of toxicity data generated using these methods, see Table
Toxicity test | Species | Age | Exposure time (days) | Route of exposure | Endpoints | Test validity criteria | References |
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acute toxicity | Porcellionides pruinosus | adult | 14 | soil | survival |
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growth toxicity | Porcellio scaber | juvenile | 28 | soil (artificial and natural) | survival, biomass change | control mortality <20% |
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food pellets, leaf litter | survival, biomass change | control mortality <20% | |||||
reproduction toxicity | Porcellio scaber | adult | up to 70 | soil (artificial and natural) | survival, oosorption, gravid females, offspring | control mortality <20% |
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food pellets, leaf litter | survival, oosorption, gravid females, offspring | control mortality <20% | |||||
Porcellio dilatatus | adult | 54 | food (lettuce incorporated in gelatine) | survival, time to pregnancy, pregnancy duration, abortions, juveniles |
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feeding inhibition | Porcellio scaber | adult | 21 | food (pellets) | food consumption rate, chemical assimilation, growth, moulting and survival |
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Porcellionides pruinosus | pre-adult | 14 | soil | consumption rate, assimilation rate, biomass change |
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food (leaf litter) | consumption rate, assimilation rate, excretion rate, biomass change |
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feeding inhibition |
Porcellio
scaber
Oniscus asellus |
adult | 35 | food (leaf litter) | feeding rate, excretion rate, assimilation efficiency, accumulation, chemical ingestion |
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Porcellio scaber | adult | 28 | food (leaf litter or pellets) | body mass gain, food consumption, gravid females, juveniles |
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84 | food (leaf litter or pellets) | survival | |||||
avoidance behaviour | Porcellionides pruinosus | adult | 2 | soil | % avoidance, habitat function | no avoidance in control vs control |
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foraging behaviour | Porcellio scaber | adult | 2 | food | preference (video tracking) |
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bioaccumulation | Porcellionides pruinosus | pre-adult | 40 (21 uptake; 19 elimination) | soil | bioaccumulation, kinetics |
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pre-adult | 41 (21 uptake; 20 elimination) | food (leaf litter) | bioaccumulation, kinetics | ||||
bioaccumulation | Porcellio scaber | adult | 32 (16 uptake; 16 elimination) | Leaf powder | bioaccumulation kinetics |
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Avoidance response behaviour to contaminated food or soil is also the fastest endpoint, with test durations of no more than two days. No standard test guideline for avoidance tests with isopods is available, but such tests have been done by e.g.,
Another interesting endpoint that is directly related to decomposition is the microbiome in the isopod gut (
In addition, mortality, growth, and reproduction are more related to the population level and bridge the gap to higher levels of biological organisation. These studies are more difficult to perform, as mentioned above, due to the life-span of isopods and their moulting behaviour. Reproduction tests with isopod have been performed in a 48-week exposure test via food contaminated with PAHs using Oniscus asellus (
Looking at lower organisational levels, biomarkers are defined as any measurable biochemical, cellular, histological, physiological or behavioural change that can provide evidence of exposure and/or effects from one to more contaminants (
In order to study endocrine disruptor effects,
These biomarkers have been used to detect effects of individual chemicals but also to unravel modes of actions of chemicals and explain their effects when present in the environment as mixtures. In the study of
HSPs, initially discovered in salivary glands of Drosophila exposed to heat (
In addition to HSPs, several other biomarkers were studied in situ in relation to predominantly metal(s) contamination. Metal storage granules and energy reserves were investigated in Oniscus asellus and Porcellio scaber in relation to distance to the smelter at Avonmount, UK (
Considering the extremely high metal concentrations found in animals from contaminated areas (see e.g.,
Isopods have been shown to have a tremendous capacity of storing metals in the hepatopancreas. As mentioned above, the hepatopancreas plays an important role in metal sequestration. Due to the high storage capacity of the hepatopancreas, metal uptake kinetics tends to be fairly slow in isopods. Basically, this means that it takes a long time to reach equilibrium, as was shown for cadmium (
Metal speciation in food may have an effect on metal uptake in isopods, as was for instance shown by
Test methods for determining the uptake and elimination kinetics of organic chemicals in isopods are summarised in Table
Single species toxicity tests have several shortcomings (adapted from
In contrast to single species toxicity tests microcosms, mesocosms or macrocosms are small, medium, or large multispecies systems that simulate natural situations to a certain degree (
The main disadvantage of such multispecies tests is that the more they imitate a natural environment the more difficult they are to replicate and to standardise. Microcosm tests are higher tier tests, usually designed to test a specific hypothesis, and not to be used routinely.
Field studies may take both a predictive and a diagnostic approach. In case of a predictive approach, field studies are just the next step after micro- or mesocosm-based toxicity tests described above. Such tests have rarely been done with isopods. Diagnostic field studies are mainly performed within the framework of monitoring, in order to assess the occurrence of effects at (contaminated) field sites. This section will mainly focus on the latter approaches.
Field (in situ) studies on the effects of pollutants on biota bridge the gap between laboratory-conducted toxicity studies and abiotic measuring of pollution. An increased concentration of a pollutant in the environment does not necessarily mean disruptive effects to biota. To cause toxic effects, a chemical needs to be sensed or taken up by the organism; therefore, bioavailability is crucial for toxicity. Moreover, in the field organisms simultaneously respond to a variety of anthropogenic and also natural stressors with antagonistic and synergistic actions among them. Therefore, biological monitoring is important to measure the disruptive effects of pollutants to biota. There are four main approaches to biological monitoring of pollution (adapted from
In 1975 a marine monitoring scheme ‘The mussel watch’ was proposed to follow the level of marine contamination with metals, artificial radionuclides, petroleum and chlorinated hydrocarbons (
Almost ten years later, results from a large field study were published (
Isopods were also studied in urban areas as bioindicators for Zn (
Field studies where isopods were used in monitoring of contamination with organic chemicals are very rare compared to metal contamination. Some laboratory studies showed that isopods may also accumulate organic chemicals, like veterinary pharmaceuticals (
All these studies showed that isopods, particularly Porcellio scaber, have favourable attributes to become a leading organism in terrestrial biomonitoring (see e.g.,
The previously mentioned studies also demonstrated a strong correlation between body metal concentrations and isopod body mass. It was therefore suggested to compare animals from the same weight class (
In the terrestrial environment metal contamination on one side and isopod distribution on the other are influenced more prominently by local environmental conditions compared to marine ecosystems. Amount and distribution of rainfall during the year, wind directions and relief of the landscape together with soil chemistry and vegetation influence the deposition, retention, and availability of metals to biomonitoring organisms on one side and appropriate conditions for their living on the other. All this makes ‘a global woodlouse watch scheme’ (
Isopods are important organisms in terrestrial ecosystems. For that reason they should be considered as test organisms in soil ecotoxicology. A standardised test with isopods could be a relevant and important addition to the existing battery of toxicity tests with soil invertebrates. The difficulties in culturing and testing could be overcome by selecting species with shorter life cycles, like Porcellionides pruinosus, and by putting more effort in optimising culture conditions for species like Porcellio scaber. This may also help developing standardised toxicity tests that include more relevant endpoints like reproduction, in addition to growth and feeding activity. Little insight exists in the difference in sensitivity of isopod species to different chemicals. The harmonisation between exposure time, the existence of validation criteria based on basal levels for optimum exposure (considering temperature and time) and common endpoints could be a step forward for the accuracy improvement and comparison between studies. Isopods are also relevant and useful organisms for use in field monitoring approaches, for instance to assess the bioavailability of metals, possible (post-registration) effects of pesticide use, exposure to (mixtures of) chemicals and in biological soil quality networks aimed at protecting ecosystem services.
The authors would like to thank Paula Tourinho for the isopod test drawings. Susana Loureiro acknowledges FCT/MEC through national funds, and the co-funding by the FEDER (POCI-01-0145-FEDER-00763), within the PT2020 Partnership Agreement and Compete 2020, to CESAM.
Supporing information