doi: 10.1016/j.chemosphere.2005.01.057. - The information available from higher-tier studies does allow to draw important conclusions, for example when addressing the question how much the composition of invertebrate communities determines the level of ecotoxicity (Sechi et al., 2014). Interestingly, the effects in OECD soil in the reproduction tests were almost always lower than in the field soils (EC50Reproduction: 29.2 mg a.i./kg soil DW), while the opposite was determined in the avoidance tests with OECD soil: EC50Avoidance: 14.1 mg a.i./kg soil DW). (2006).
While focusing on the effects of pesticides, attention is also given to their interactions with environmental stressors (e.g., climate change). Pest. Toxicol. B., Sousa, J. P., Nogueira, A. J. Toxicol. The remaining tests were run with pentachlorophenol (PCP) and benomyl (both seven times) and carbendazim (14 times). Handbook of Soil Invertebrate Toxicity Tests. doi: 10.1016/0742-8413(91)90157-o. Dissertation, Universitt Bremen, Bremen. Enchytraeus albidus (Enchytraeidae): a test organism in a standardised avoidance test? B. Pollut. Regarding cellular responses of enchytraeids to pesticides, several of these biomarkers have already been studied. Verhandlungen Gesellschaft kologie 19, 157. Can avoidance in Enchytraeus albidus be used as a screening parameter for pesticides testing? Enchytraeid Reproduction TestPLUS: hatching, growth and full life cycle testAn optional multi-endpoint test with Enchytraeus crypticus. - How can enchytraeids be established in higher-tier tests such as TMEs or field testsand would it be useful to standardize gnotobiotic test systems? 20. (2014) investigated the effects of phenmedipham on E. crypticus, in 12 soils from Spain, Italy and Portugal plus OECD soil. 25, 24802489. They investigated enchytraeid molecular and biochemical mechanisms in response to pesticide exposure using differential gene expression, as well as defense and cell injury biomarker activities (e.g., Howcroft et al., 2011; Novais et al., 2012c, 2014). Ecotoxicology 21, 21632176. Especially in the international ringtest, a huge data set was compiled (92 tests in total), allowing to assess the variability of this test system (Weyers et al., 2002).
In four tests no guideline was used, but they were conducted already in 1988/1989 (Rmbke, 1989). At the end, information from 302 papers was used for this review. Almost the same is true regarding the interaction between pesticides and other agricultural practices (e.g., soil compaction due to the use of heavy machinery; Beylich et al., 2010). UBA-Texte 20/02. Contam. The experiences with enchytraeid higher-tier testing can be summarized as follows: - In these tests total abundance was often the main (or only) endpoint.
J. Agric. However, the total glutathione and TBARSlevels increased, associated with an increase in activities of CAT, GPx, and GR and a decrease in GST activity after 3 weeks of exposure. Schlaghamersk, J. In fact first studies aiming at its standardization have been published (e.g., Sechi et al., 2014). 35, 115134. (2015). Bioaccumulation and elimination of 14C-lindane by Enchytraeus albidus in artificial (OECD) and a natural soil. (2006).
Adaptations of enchytraeids to single and combined effects of physical and chemical stressors. ZooKeys 176, 275296. (2007). Soil Organisms 81, 175196. Benrodis (Suppl.
Enchytraeidae (Oligochaeta, Annelida) are often considered to be typical forestliving organisms, but they are regularly found in agroecosystems of the temperate regions of the world. 100C, 221224. doi: 10.1007/s10646-015-1581-y, Banerjee, B. D., Seth, V., and Ahmed, R. S. (2001). While this is probably no problem for laboratory tests (especially when including recent ideas on life-cycling testing; Bicho et al., 2015), there is surely work to be done on higher-tier testing. 8, 468479. An EC50 value of 0.739 mg a.i./kg soil DW was determined for reproduction, i.e., lower than the predicted environmental concentration (PEC) after the recommended use of this pesticide. Sci. Such an enchytraeid avoidance test was developed by Achazi et al. (2006) for laboratory and field studies, respectively. Avoidance behavior is not more sensitive than reproduction or even mortality (Amorim et al., 2005a). This recommendation has been confirmed several times (Castro-Ferreira et al., 2012; Voua Otomo et al., 2013). Species determination via genetic methods (DNA barcoding and meta-barcoding) is a promising alternative (Orgiazzi et al., 2015) since the establishment of DNA sequencing as a cheap routine laboratory procedure. Afterwards, publication lists regarding Enchytraeidae in general (e.g., Schoch-Bsken and Rmbke, 1993) or their use in ecotoxicology (e.g., Rmbke, 2003) were checked. Figure 3. 42, 6367. (1994) applied an insecticide (parathion) or a herbicide mixture (Amitrole/Diuron) at the highest recommended application rate or a 5-fold higher concentration rate. Int. ASTM Guideline No. Chaetae are straight distally, and body movements are often slower than those of litter dwellers. Rther, U., and Greven, H. (1990). The response of soil organism communities to the application of the insecticide lindane in terrestrial model ecosystems. Schmidt, O., Curry, J. P., Dyckmans, J., Rota, E., and Scrimgeour, C. M. (2004). Die Sukzession der Enchytraeen-Synusie (Annelida, Oligochaeta) eines Ruderalkosystems unter Natrlichen und Anthropogenen Einflssen.
Chemosphere 79, 233237. - The influence of soil properties on the effects of pesticides on enchytraeids is relatively well-studied, at least regarding texture and organic matter. - Even more obvious are advantages in higher-tier tests: in TME tests complex interactions with other soil organisms under a wide range of environmental conditions can be studied with relatively low efforts in comparison to field tests. The most promising method is the SMS (a simplified food-web approach, consisting of springtails, enchytraeids and predatory mites; e.g., Menezes-Oliveira et al., 2014). Since very high concentrations of these pesticides were used, the enchytraeid populations were strongly affected (especially in a year with a long period of drought) during the application period (Rmbke, 1988). (2002). doi: 10.1897/07-385.1. Cortet, J., Gomot-De Vauflery, A., Poinsot-Balaguer, N., Gomot, L., Texier, C., and Cluzeau, D. (1999). J. Appl. ), while Fridericia-species live in slightly acid to basic soils and vary considerably in size (Schmelz, 2003). This work was done by different partners at one arable site (Coimbra, Portugal) and three grassland sites: Amsterdam (The Netherlands), Bangor (Wales, England), and Flrsheim (Germany). Pokarzhevskii, A. D., Filimonova, Z. h. V., and Goryachev, O. Since then, several reproduction tests have been internationally standardized (American Society for Testing and Materials, 2004; International Organization for Standardization, 2004; Organisation for Economic Co-operation and Development, 2004; Associao Brasileira de Normas Tcnicas, 2012). Samples were taken 1 month before application and 1, 2, 3, and 4 months after application. This view is not supported by the many studies where reproduction and (sometimes) avoidance is more sensitive than mortality. New York, NY: Elsevier Applied Science. The effect of heavy metals on enchytraeids. Soil Quality Effects of Pollutants on Earthworms - Part 3: Guidance on the Determination of Effects in Field Situations. doi: 10.1016/j.chemosphere.2012.01.021. (2014). Dzsa-Farkas, K. (1991). doi: 10.1897/IEAM-2009-064.1. (2014). Soil Biol. L/ha mesotrione were studied. The Micro-Distribution of Enchytraeidae. Ecotoxicol. doi: 10.1016/j.chemosphere.2012.03.007, Yang, D., Zhu, J., Shen, G. X., Wang, W. H., Guo, X. P., Wang, Z. Q., et al. Rmbke, J. (2015). Nutr. RIVM-Report 607604009. A., and Soares, A. M. V. M. (1999). Table 2. In addition, a standard semi-field test (Schaeffer et al., 2010) has been proposed, but so far, no field test is available. J. Rev. (2003). Figure 4. (2009) tested the toxicity of lindane on the mortality and avoidance behavior of E. albidus in LUFA 2.2 soil and found that the effects occurred in a similar range. However, enchytraeids did not react more sensitively to the fungicides benomyl and carbendazim in these tests than in chronic tests (Amorim et al., 2005a). Both high numbers and central ecological roles supported the idea to use enchytraeids in standard ecotoxicological tests.
Effects of azoxystrobin, chlorothalonil, and ethoprophos on the reproduction of three terrestrial invertebrates using a natural Mediterranean soil. Reduction in the number of juveniles was best explained by reduced hatching from cocoons, leading to a better understanding of the causes of toxic effects on these worms. Result of a bioaccumulation test of the insecticide lindane in Enchytraeus crypticus in OECD soil, showing both uptake (gray-shaded) and elimination phase (for details see de Amorim et al., 2002). The effect of an insecticide on soil forming fauna (Arthropoda, Oligochaeea).
Geoderma 56, 287299. *Correspondence: Jrg Rmbke, j-roembke@ect.de, Non-Target Effects of Pesticides on Organisms Inhabiting Agroecosystems, View all
Mortality and reproduction do not always show the same tendency: in tests with the field soil Coi3 E. luxuriosus shows almost the same LC50 as in OECD soil, but the EC50Reproduction differs by almost a factor of 30 (E. luxuriosus reacts much stronger than E. albidus). 
Out of these 23 tests, 17 were performed with E. albidus, five with E. luxuriosus and one with Fridericia bulbosa (an invalid name according to Schmelz, 2003). Nielsen, C. O., and Christensen, B. Environ. Rmbke, J. Risk to human health and the environment. J. However, species of the genus Fridericia (i.e., K strategists) are more affected by carbendazim than other enchytraeids, which may be due to different exposure or to physiological differences. Orgiazzi, A., Dunbar, M. B., Panagos, P., de Groot, G. A., and Lemanceau, P. (2015). Biodivers. Both the ERT as well as the enchytraeid avoidance test were used. Another example is the interaction between (changing) climate parameters with chemicals, which in turn can cause unpredictable changes in community structures (Menezes-Oliveira et al., 2014). It seems that there is a potential of using gene expression in risk assessment (Novais et al., 2012b), especially since a database containing genomic information for E. albidus is freely available (Novais et al., 2012a). Oikos 32, 318327. doi: 10.1007/BF00379488, Chelinho, S., Domene, X., Campana, P., Andrs, P., Rmbke, J., Sousa, J., et al. - What about the trait conceptcan we identify morphological/ecological groups which may be more relevant than individual species? Soil Ecol. The toxicity of benomyl decreased with increasing soil moisture content, but the mechanisms behind this behavior were not clearly understood. However, when spiking carbendazim in LUFA 2.2 soil and aging it for one, 14 or 28 days before starting the tests, Kobetiov et al. - An Enchytraeid Bioaccumulation Test has been standardized by the OECD some years ago, but despite its advantages in comparison to earthworms (shorter duration, smaller size and thus need of less space) it has rarely been used. B., Novais, S., Rmbke, J., and Soares, A. M. V. M. (2008b). Environ. Another example is the effect of lambda-cyhalothrin on the reproduction of the fragmenting species E. bigeminus which was examined under three different soil moisture levels (30, 50, and 70% of the soil WHC) (Bandow et al., 2013). 157, 625636. 83, 512. doi: 10.1016/S0045-6535(02)00322-3, Didden, W. A. M. (1990). Considering that the molecular and biochemical responses of E. albidus to pesticides appeared to be dose-related and time-dependent, it is recommended to test different concentrations of pesticides and different times of exposure. About 5% of this list were not found via literature search but due to personal contacts (mainly older work or diploma reports). Effects of natural and chemical stressors on Enchytraeus albidus: can oxidative stress parameters be used as fast screening tools for the assessment of different stress impacts in soils? (2012c). Similarly, gamma-aminobutyric acid (GABA) is the major inhibitory transmitter at neuromuscular synapses and synapses in the central nervous system, being also a biomarker of neurotoxic effects (Bicho et al., 2015). 26, 183199. Environ. For convenience, these preferences can be combined into three groups as follows: LD: litter dwellers (e.g., Buchholzia appendiculata, Cognettia sphagnetorum); SD: soil dwellers (e.g., Marionina clavata, Fridericia bulboides, Fridericia galba); IS: intermediate species (e.g., Henlea perpusilla, Enchytraeus christenseni). doi: 10.1002/etc.2368, Novais, S. C., and Amorim, M. J. Environ. Experiment durations should be chosen to assess short, medium, and long-term responses, thus allowing to characterize gene expression and biomarker changes in a situation where reproduction occurred. Negative reactions on the enchytraeid community were found at concentrations lower than those identified in the laboratory. Part 2: Determination of Effects on Reproduction. Toxicity of dimethoate to some soil animal species in different soil types. Effects of two concentrations of the fungicide PCP (light gray dotted line: 0.5 kg/m2; dark gray dotted line: 5 kg/m2) on the enchytraeids of a beech wood forest (bimonthly application: 19821983; recovery time: 19841985) in percent of the control (solid darkline) (for details see Rmbke, 2001). Schrffenberg, B. Biochem. This difference in the bioaccumulation factors (BAF) of lindane in the two species is probably due to size-related differences and the respective volume: surface ratio (E. albidus is larger than E. luxuriosus; Amorim et al., 2002). Soil Quality Avoidance Test for Evaluating the Quality of Soils and the Toxicity of Chemicals. in uncontaminated field soil at three different moisture levels (40, 55 and 70% of the soil WHC). doi: 10.2307/3544689. (2015). Laboratory single-species tests do not allow to address properly these complex effects of chemical exposure at the community level or higher, since they focus on single species under highly standardized conditions. Environ. doi: 10.1007/BF02987596, Way, M. Y., and Scopes, N. E. A. An updated checklist of currently accepted species of Enchytraeidae (Oligochaeta).
Currently the Enchytraeid Reproduction Test (ERT) is listed as an alternative or addition to earthworm tests in several regulations (e.g., European Plant Protection Organisation, 2003; VICH, 2005; European Chemicals Agency, 2014; EFSA Panel on Plant Protection Products and their Residues (PPR) et al., 2017). (2012). 6, 117126. Soil Ecosystem Profiling in the Netherlands with Ten References for Biological Soil Quality. The ERT allows some flexibility, i.e., various species of the genus Enchytraeus as well as different soils and endpoints can be used. Scholz-Starke, B., Beylich, A., Moser, T., Nikolakis, A., Rumpler, N., Schffer, A., et al. These are small vessels filled with field soil (rarely including plants), kept in the laboratory under controlled conditions. Test with Earthworms (Eisenia fetida/andrei). Indicator values, strategy types and life forms of terrestrial Enchytraeidae and other microannelids, in Newsletter on Enchytraeidae, Vol. According to Schrffenberg (1950) and Friberg et al. doi: 10.1139/er-2015-0013. Interestingly, avoidance behavior (EC50: 38 mg a.i./kg soil DW) was found to be an even less sensitive endpoint than mortality (LC50: 12 mg a.i./kg soil DW) (Novais et al., 2010). (2001). All available information is from forest sites. Amorim, M. J., Sousa, J. P., Nogueira, A. J. - By definition, higher-tier studies do include site-specific properties (which means mainly soil properties but also climatic factors) and this inclusion of realism has to be addressed in current risk assessment procedures. The one exception is carbendazim, which has already been used in a European ring test, both in TMEs and the field. (1999) firstly summarized the experiences with PPP effects on enchytraeids, listing five papers. Despite the scarce literature, some advice can be given to assess the effects of pesticides on enchytraeids at sub-individual levels. Regarding land-use types, our review focuses on agro-ecosystems, i.e., crop sites, mainly on cereal crops, but also grasslands. Presented is the canonical coefficient (Cdt) of the different application rates at the sampling points w+1, w+4, w+8, und w+16 (weeks after application) and the taxon weight (bk) for all taxa. B. (2008). Bioaccumulation of lindane and hexachlorobenzene by the oligochaetes Enchytraeus luxuriosus and Enchytraeus albidus (Enchytraeidae, Oligochaeta, Annelida). Testing the effects of ethoprophos on E. crypticus in a Mediterranean soil resulted in an EC50 value of 68.5 mg a.i./kg soil DW (Leito et al., 2014). B., Novais, S. C., van der Ven, K., Vandenbrouck, T., Soares, A. M. V. M., and de Coen, W. (2011). Effects of pesticides on soil invertebrates in laboratory studies: a review and analysis using species sensitivity distributions. Thus, enchytraeids can be classified as biological regulators, i.e., they regulate in particular the abundance and activity of microbes through their feeding (Turb et al., 2010). doi: 10.1016/j.chemosphere.2005.03.048, Amorim, M. J. Figure 2. With the exception of the avoidance tests, the performance of all tests did not differ much. In any case, a central part of practical work (extraction of enchytraeids from soil samples) is already covered in an ISO guideline (International Organization for Standardization, 2007), focusing on monitoring enchytraeids. 117, 8992. Enchytraeids are one out of seven soil organism groups for which specific protection goals have been definedand they are quite detailed regarding the magnitude and duration of effects. Environ. Nat. doi: 10.1007/s10646-014-1265-z, Novais, S. C., Howcroft, C. F., Carreto, L., Pereira, P. M., Santos, M. A. S., de Coen, W., et al. (2011). Cholinesterases (ChE) are a family of enzymes that catalyze the breakdown of some choline esters that act as neurotransmitters. Carbendazim was sprayed on small plots at two concentrations and the abundance, biomass and diversity of the enchytraeid community was studied for two years, divided into an application phase and a recovery phase. Bioaccumulation in Terrestrial Oligochaetes. In a beech forest in Southern Germany, two model pesticides, the fungicide PCP and the herbicide 2,4,5-T were applied bimonthly on small field plots (25 m2) for about 2 years (Rmbke, 2001). Environ. Bandow, C., Coors, A., and Rmbke, J. EFSA J.
Chem. International Cooperation on Harmonisation of Technical Requirements for Registration of Veterinary Medicinal Products, London. Soils 9, 152158. (2015). Influence of application of a fungicide, an insecticide, and compost upon soil biotic community, in Soil Biology as Related to Land Use Practices, ed D. L. Dindal (Washington, DC: Office of Pesticide and Toxic Substances, Environmental Protection Agency), 9499. Soil Tillage Res. After stopping the applications of PCP, enchytraeid abundance started to recover less than half a year later in plots with the lower application rate, while abundance remained significantly lower at the higher application rate for about at least one more year. Life-cycle length determines the differences in sensitivity to toxicants between Enchytraeid species. Ecotoxicogenomic approaches can be used to analyze initial molecular and cellular effects, and the necessary sequence information is now available for enchytraeids, especially E. albidus. Burkhardt, U., Russell, D. J., Buryn, R., Decker, P., Dhler, M., Hfer, H., et al. Ferreira, M. P. C., Roelofs, D., van Gestel, C. A. M., Amorim, M. J. Physiol.
(2000). We do not include copper, which is used as a fungicide, especially in vineyards. 
1. Enchytraeids can be very important for soil functions such as maintaining soil structure and porosity, especially when earthworms are not abundant. Moreover, although the reported references allow to infer the cascade of reactions that occurs when potworms are exposed to pesticides, few authors studied the link between different levels of biological organization (Novais et al., 2012b; Bicho et al., 2015) Finally, it is worth noting that to be able to discriminate between stress responses and natural ecological variations of biomarker expression, it is necessary to know the normal operating range (NOR) of a species. Toxicol. For lambda-cyhalothrin, the 21-day EC50Reproduction values at the three levels of soil moisture were calculated to be 1.33, 3.79, and 4.75 mg as/kg soil DW, respectively. Ultra-high Throughput TRANScryptOME Sequencing of Enchytraeus crypticus- Innovative Tool for Stress Response Assessment. Graefe, U., and Beylich, A. Forest. Their diversity is rarely studied or often underestimated due to difficulties in distinguishing the species. VICH Guideline 38 (Ecotoxicity Phase II). Results from other field soils are somewhere in between, i.e., there is no clear difference to tests in OECD soil. Environ. Pedobiologia 43, 635640. (2016). Depending on the soil properties, especially the pH value, these numbers can be 24 times higher in grasslands. State of knowledge of enchytraeid communities in German soils as a basis for biological soil quality assessment. 13, 257277. The best example for the use of enchytraeids (E. albidus, E. luxuriosus) in the standard OECD bioaccumulation test (Organisation for Economic Co-operation and Development, 2010) is a study performed with the insecticide lindane, which is, at least in Europe, no longer registered (Bruns et al., 2001; de Amorim et al., 2002). (2012) studied the effects of the insecticide/nematicide carbofuran on E. crypticus under tropical conditions in the laboratory, following basically the ISO standard (International Organization for Standardization, 2004). 91, 545548. Ambio 27, 6269. Kuperman, R. G., Simini, M., Phillips, C. T., and Checkai, R. T. (1999). Bengtsson, G., and Rundgren, S. (1982). Enchytraeids may also avoid chemicals by vertical migration, which has been observed in a field study in a German grassland (Rmbke and Federschmidt, 1995). The low number of herbicides tests is probably caused by the fact that, due to their MoA, low effects on enchytraeids are expected. It has been shown that dimethoate caused ChE inhibition in E. albidus, indicating an impairment of the neuronal function, but further work is surely needed before such endpoints can be used in regulatory testing (Novais et al., 2014). - Only few pesticides have been studied intensively, mainly the fungicide carbendazim, the insecticide dimethoate and the herbicide phenmedipharm. Four field soils with varying properties and two forest soils (without and with pH modification (pH = 4.5 and 6.0, respectively) were used in order to evaluate the influence of soil acidity. In addition, no clear relationship between avoidance behavior and ecologically more relevant endpoints such as reproduction could be established (Novais et al., 2010). doi: 10.3897/zookeys.176.2275, Van Vliet, P. C. J., West, L. T., Hendrix, P. F., and Coleman, D. C. (1993). Chem. According to Graefe and Schmelz (1999), enchytraeid species differ with respect to their preferred occurrence in the soil profile. Normal operating range (NOR) in Enchytraeus albidus Transcriptional responses to control conditions. Evaluation of exposure metrics for effect assessment of soil invertebrates. From the beginning, almost exclusively species of the genus Enchytraeus were tested, using both acute and chronic endpoints (Purschke et al., 1991) as well as bioaccumulation (Rther and Greven, 1990). Geneve: ISO 175121. Geneva: ISO 16387. International Organization for Standardization (2007). (1977). Achazi, R. K., Frhlich, E., Henneken, M., and Pilz, C. (1999). (2004). Weuffen, W. (1968). However, the outcome is hardly useful since samples were not replicated.
Note that results were obtained in tests following either a NOEC design or ECx design (for details see Rmbke and Moser, 2002). Other endpoints scannot be judged due to low level of experience. (2010). Rmbke et al. A draft standard method exists for a semi-field method, i.e., TMEs (Schaeffer et al., 2010), but nothing like that is available for field tests. The influence of Zeazin 50 on Enchytraeidae (Oligochaeta) in an apple orchard soil. The value of 10 mg a.i./kg soil DW was chosen since even in worst case conditions, the exposure in the field will not exceed this concentration. 184, 586596. Beyond this threshold, cellular homeostasis is no longer ensured, and short and long-term, and often irreversible, negative consequences may occur (Mercurio, 2017). In parallel it has been checked whether changes in cellular energy allocation (CEA) could be used for the evaluation of the energetic status of an organism, but again not much experience is available so far (Gomes et al., 2015). Hung. Loureiro et al. Fridericia peregrinabunda (Enchytraeidae) as a new test species for soil toxicity assessment. Such microcosms are suitable for specific questions, e.g., the influence of pesticides on combinations of standard test soil invertebrates (E. crypticus, together with some springtail species and a predatory mite), but so far no standard guideline is available (Jensen and Scott-Fordsmand, 2012). Both NOEC and EC50Reproduction are below 5 mg a.i./kg dry soil (Hartnik et al., 2008). Ring-testing and field-validation of a Terrestrial Model Ecosystem (TME) An instrument for testing potentially harmful substances: effects of carbendazim on enchytraeids. all above-mentioned functions have to be protected.
- Which endpoints are the most sensitive, relevant, robust and practical ones? 68, 326334. 1 (Brighton). doi: 10.1078/0031-4056-00120. Soil Biol. The EC50Reproduction in the field soils differed between 3.8 and 32.8 mg a.i./kg soil DW. We decided to exclude copper despite the fact that for more than 100 years it has been the active ingredient in a fungicide product, originally known as Bordeaux Mixture. There is a huge amount of information available regarding the effects of copper on soil organisms in general (especially earthworms), but its effects on enchytraeids when sprayed as a pesticide are not yet covered. Dormidontova, G. N. (1973). The experiences with enchytraeid laboratory tests can be summarized as follows: - Testing started with the large species E. albidus, but today it is used mainly when addressing other endpoints than those required in the standard tests. 22, 1424114247. More contrasting results were found when looking at the effects of insecticides on enchytraeids in detail. Appl. - BioIntelligence Service. Fridericia is by far the richest terrestrial genus of the family; up to now only few differences in habitat preferences have been found among the individual species. Environ. Sci. Integr. Kitazawa, Y., and Kitazawa, T. (1980). This picture is mainly caused by r-strategists (i.e., those adapting quickly to changing environments) such as Cognettia sphagnetoruma potworm which can reproduce by fragmentation (Nielsen and Christensen, 1959).
42, 219245. The effect of soil from former irrigation fields and of sewage sludge on dispersal activity and colonizing success of the annelid Enchytraeus crypticus (Enchytraeidae, Oligochaeta). Aquatic toxicity test for enchytraeids. Edwards, C. A., Thompson, A. R., and Beynon, K. I. Technol. Assess. However, they have the disadavantage of targeting only certain genes present on the microarray, i.e., they do not allow to screen the genome without an a priori selection of the genes that are expressed. (2004). doi: 10.1080/002229399300461.
Supplement 2, Vol. (2014). Comparison of the influence of an artificial and a natural soil on the behaviour of Enchytraeus albidus laboratory tests. 42, 18621893. With the improvement of extraction methods and a better availability of taxonomic keys in the past 10 years (Schmelz and Collado, 2010), our knowledge on enchytraeid taxonomy and ecology as well as their reaction to pesticides have certainly increased considerably, not only in Europe but also for example in Brazil (Chelinho et al., 2012; Assis, 2015). Res. The antioxidant nutrients and disease prevention - what do we know and what do we need to find out? Alpha-cypermethrin belongs to the second group (i.e., effect values <10 mg a.i./kg soil DW). Knacker, T., Van Gestel, C. A. M., Jones, S. E., Soares, A. M. V. M., Schallna, H.-J., Frster, B., et al. It is less toxic in dry soil than in moist soil. Regulation (EC) 1107/2009 of the European Parliament and of the Council of 21 October 2009 Concerning the Placing of Plant Protection Products on the Market and repealing Council Directives 79/117/EEC and 91/414/EEC, Vol. doi: 10.1016/S0269-7491(01)00156-7, Lock, K., Schamphelaere, K. A. C., and de Janssen, C. R. (2002). doi: 10.2307/3546996, Lagerlf, J., Andren, O., and Paustian, K. (1989). 
