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Environmental Pollution 107 (2000) 233±238 www.elsevier.com/locate/envpol Decomposer animals and bioremediation of soils J. Haimi* Department of Biological and Environmental Science, University of JyvaÈskylaÈ, PO Box 35, FIN-40351 JyvaÈskylaÈ, Finland Received 29 August 1998; accepted 22 May 1999 ``Capsule'': Soil animals do not themselves degrade soil contaminants, but they do have an important indirect role in these processes performed by microbes. Abstract Although microorganisms are degrading the contaminants in bioremediation processes, soil animals can also have important Ð while usually an indirect Ð role in these processes. Soil animals are useful indicators of soil contamination, both before and after the bioremediation. Many toxicity and bioavailability assessment methods utilizing soil animals have been developed for hazard and risk-assessment procedures. Not only the survival of the animals, but also more sensitive parameters like growth, reproduction and community structure have often been taken into account in the assessment. The use of bioassays together with chemical analyses gives the most reliable results for risk analyses. This is because physical, chemical and biological properties of the remediated soil may be changed during the process, and it is possible that transformation rather than mineralization of the contaminants has taken place. In addition, the soil may contain other harmful substances than those searched in chemical analyses. Finally, because the ultimate goal of the bioremediation should be Ð together with mineralization of the harmful substances Ð the ecological recovery of the soil, development of diverse decomposer community as a basis of the functioning ecosystem should be ensured. Soil animals, especially the large ones, can also actively take part in the ecological recovery processes through their own activity. The potential risk of transfer of contaminants accumulated in soil animals to the above-ground food webs should be borne in mind. # 2000 Published by Elsevier Science Ltd. All rights reserved. Keywords: Soil contamination; Harmful chemicals; Bioremediation; Decomposer animals; Decomposition processes 1. Introduction There are to two general approaches in remediating or reclaiming severely degraded soils: (1) an engineering approach; and (2) an ecological approach (Logan, 1992). The engineering approach relies exclusively on external methods for soil restoration, while ecological remediation involves the manipulation of inherent soil processes to mobilize, immobilize, transform or degrade contaminants. This manipulation may include, e.g. fertilization or liming of the soil, revegetation of the site and the use of organic amendments to stimulate soil biological activity. Bioremediation of contaminated material is based on the ecological approach, microbes being responsible for the degradation processes. Bioremediation is usually recognized as an inexpensive, eective, and environmentally safe technology to * Tel.: +358-14-2602303; fax: +358-14-2602321. E-mail address: [email protected].® (J. Haimi). clean up hazardous wastes or chemicals. The soil is considered remediated when concentrations of the contaminants have diminished to the recommended, directed or appropriate levels. The ultimate goal of the process is Ð or at least should be Ð full mineralization of the harmful substances by their conversion into microbial biomass and harmless products of metabolism, such as water, carbon dioxide and inorganic salts. Once bioremediation treatment has been completed, the soil can be utilized, e.g. as land®ll cover material. Bioremediation techniques use biostimulation and/or bioaugmentation in the degradation of various harmful contaminants. Bioaugmentation involves the addition of a microbial inoculum to a contaminated soil, whereas biostimulation involves amendment, addition and/or mechanical manipulation to stimulate indigenous bacterial populations. Abiotic conditions are optimized for biodegradation, that is, the functioning of desired microbes. At the moment, the incomplete understanding of biodegradation processes and the absence of diverse engineering techniques required for applications are 0269-7491/00/$ - see front matter # 2000 Published by Elsevier Science Ltd. All rights reserved. PII: S0269-7491(99)00142-6 234 J. Haimi / Environmental Pollution 107 (2000) 233±238 regarded as major problems in the development of bioremediation (Pritchard et al., 1996). There are both biological and environmental reasons to extend the concept of bioremediation to ecological remediation. This approach requires Ð in addition to the degradation of hazardous wastes Ð the establishment or recovery of approriate microbial, plant and animal communities to create a functioning ecosystem (Majer, 1989). The same ultimate goal is included in reclamation processes of disturbed sites (Recher, 1989). Recreating the original diverse and complex biota of the site is probably not possible or feasible in most cases, but a reasonable approximation can generally be achieved. At the moment, many other objectives, such as legislation, public opinion and ®nancial considerations, are pursued when bioremediation processes and technology are designed. 2. Potential utilization of soil animals in bioremediation Usually, abiotic conditions in the soil under bioremediation process are hostile for soil decomposer animals. The physical and chemical soil conditions may be outside the tolerance limits of most species, or animals may have been unable to colonize the soil due to limited dispersal. In addition, because animals do not harbour signi®cant metabolic ability to degrade the chemicals to be treated, one may argue that decomposer animals are not important in remediation processes. It should be noticed, however, that when dierent kinds of organic wastes are composted, many soil animals, like earthworms, enchytraeids and mites, do have positive eects on the process by utilizing organic compounds in their own metabolism, and more importantly, by increasing metabolic activity of soil microbes (Haimi and Huhta, 1987; Edwards, 1998). Stabilization of household wastes may even be faster in vermicomposting (utilizing eec- tively the earthworms) than in conventional composting process (Haimi and Huhta, 1986). Soil animals can also be exploited in remediation and reclamation processes, principally in two ways. First, they can take part in the process, increasing overall, and especially microbial, metabolic activity of the soil. Second, soil animals can be used as indicators of soil contamination, either to assess the toxicity and risk of the contaminated soil or to evaluate the ecacy of the remediation process, that is, to evaluate the toxicity and risk of the end product. Indeed, a number of methodologies with respect to pre-application testing, postapplication bioassays, monitoring, waste management and risk assessment have been proposed and also already utilized in environmental management (Table 1). 3. Soil animals as indicators of environmental contamination Contaminated soils are usually characterized by complex chemical mixtures rather than single chemicals. Moreover, soils may contain compounds that have not been expected and not looked for in chemical analyses. Transformation of the original harmful substances may further complicate the situation. To determine the environmental impact associated with complex contaminations, a toxicity-based approach rather than a chemically-based approach should be adopted in risk assessment (Callahan and Linder, 1992). It has been emphasized that direct measurements of, e.g. heavy metal concentrations in soils, has relatively little value, whereas uptake into e.g. earthworms is a much more sensitive and meaningful criterion (Morgan, 1986). Thus, relevant biological information needs to be incorporated into the toxicity and risk-assessment procedures. Soil animals can for good reasons be used as indicators of soil contamination both before and after a Table 1 A scheme for the use of soil decomposer animals in bioremediation processes Phase of the process Role/function of soil animals Study of potentially contaminated soil Preliminary toxicity testing Monitoring the concentrations of contaminants in the tissues of animals Contaminated soil Testing of bioavailability and toxicity to organisms Bioremediation processes in situ on site ex situ Increasing microbial activity Monitoring the ecacy of the process Soil after application placing/use of the remediated soil Post-application toxicity testing Ecological reclamation with animals organic amendments liming, etc. inoculation of animals J. Haimi / Environmental Pollution 107 (2000) 233±238 bioremediation process. Dierent kinds of bioassays have been developed to determine bio-availability and biological eects of harmful chemicals and contaminated soils. Together with chemical analyses, soil animal studies will help in ®nding out the linkage between actual contamination levels and adverse eects on biota. Being important and large soil decomposer animals, earthworms have gained acceptance for use in tests to assess the eects of chemicals on soil organisms. The survival test has been standardized (ISO, 1993), and it is widely used to analyze toxicity of pure chemicals in standardized soil. The survival test has further been developed to a reproduction test (ISO, 1998), and to a ®eld test (ISO, 1999). In addition to earthworms, a collembolan reproduction test is in its ®nal stage of standardization (ISO, 1997), and a proposal for an enchytraeid worm reproduction test is under international evaluation at the moment (Table 2). While these toxicity tests are very simple and done in quite arti®cial conditions, their use in combination with more complex bioassays is important to ®nd out causal explanations for changes observed in animal densities and community structures in the ®eld. Relevant information about the ecological consequences of chemicals in the soil is urgently needed. It has been suggested that certain earthworm species could be used in testing the toxicity of contaminated soils. The test procedure has already been modi®ed from the standardized arti®cial soil earthworm bioassay (Callahan and Linder, 1992). Gibbs et al. (1996) developed a procedure that allows quanti®cation of the eects of soil contaminants on earthworm (Eisenia fetida) growth and reproduction. They applied the method both in evaluating the toxicity of compost-remediated soils and as a fast-screening analysis for ®eld soils in a large-scale ecological risk assessment. In the procedure, pairs of earthworms are incubated in the studied soil, and total biomass production (growth of the adults plus reproductive output) and several reproduction end points are 235 measured. The results showed that sublethal end points are more sensitive and relevant than pure mortality when evaluating ecological risk of potentially contaminated soils (Gibbs et al., 1996). Salanitro et al. (1997) applied the traditional earthworm toxicity test in evaluating the toxicity of crude oil-contaminated soils after bioremediation. Chang et al. (1997) used the earthworm bioassay (test soils supplemented in arti®cial soil in dierent ratios) together with plant bioassays to evaluate the remediation of a lead-contaminated soil. Tests revealed that the remediated soil was clearly more toxic to earthworms than the original soil. High salt levels generated during the remediation process were concluded to be responsible for the increased soil toxicity (Chang et al., 1997). Laine et al. (1995) studied the bioavailability of organic halogen compounds in contaminated sawmill soils using the standard test species, Eisenia andrei, as a test species. They found that higher soil organic matter diminished the bioaccumulation potential of these chemicals in the earthworms. Some biomarkers measured in earthworms (like enzyme and immune functions, hemoglobin content, sperm production and fertility) have been developed and proposed for the use in reliable toxicity testing (see Reinecke and Reinecke, 1998). These parameters are very sensitive and useful, but their use needs more facilities and expertise than measurements of the more simple individual-level parameters. In addition, community and system-level ecotoxicological studies have proved to be valuable methods to support ecological risk assessment procedures (Table 3). However, the use of parameters of higher levels of biological organization as simple routine end points is unrealistic because of large variation in community structure in space and time, and large amount of labour needed for reliable analyses (Salminen and Sulkava, 1997). However, Heimbach (1997) emphasized that indirect eects of chemicals, like changes in food Table 2 Decomposer animals frequently used (the procedure has been established or is under development) in the evaluation of toxicity of chemicals and contaminated soils Animal group Species Comments Earthworms Eisenia fetida/andrei Standardized survival (ISO, 1993) and reproduction (ISO, 1998) tests in arti®cial soil, tests also with contaminated soils Common species in ®eld soils, used in several ecotoxicological studies as above Proposed standardized toxicity test in arti®cial soil, reproduction and survival Standardized toxicity test (ISO, 1997) in arti®cial soil, reproduction and survival Numerous studies in laboratories and in the ®eld Enchytraeids Collembola Mites Isopods Nematodes Protozoans Aporrectodea caliginosa Lumbricus terrestris Enchytraeus albidus, also other species Folsomia candida several species, e.g. Folsomia ®metaria and Orchesella cincta Platynothrus peltifer Porcellio scaber Trichoniscus pusillus e.g. Plectus parietinus e.g. Colpoda cucullus Long life cycle, used in many studies Used in many studies, no standardization, nutrient mineralization also measured In soil pore water, dicult to extrapolate to the ®eld, some studies As above 236 J. Haimi / Environmental Pollution 107 (2000) 233±238 Table 3 Organism groups and soil processes that should be considered in hazard and risk assessment of soil contamination (according to Eijsackers and Lokke, 1992) 1. Taxonomic groups: Microorganisms: Invertebrates: Higher plants 2. Functional groups: Primary producers Decomposers Herbivores Predators and parasites 3. Soil processes: Decomposition, soil respiration Nutrient mineralization, nitri®cation Other enzyme activities Saprotro®c fungi, mycorrhizal fungi, bacteria Protozoa, Nematoda, Oligochaeta (earthworms, enchytraeids), microarthropods (Collembola, Acarina etc.), macroinvertebrates (Isopoda, Diplopoda etc.), insects and their larvae in soils availability and soil structure, may be more important in risk assessment than direct toxic eects of chemicals on earthworms. There are some complicating factors that make interpretation of the results from studies with soil animals dicult. Resistance against the contaminant may increase, at least in long lasting exposure. Resistance may be physiologically and energetically expensive, leading to a trade-o situation in animals. Posthuma et al. (1992) and Donker et al. (1993) found changes in life history characteristics of soil animals living at contaminated sites. These changes without doubt also have eects at community and ecosystem levels. Another factor hampering evaluation of the results is avoidance behavior of soil animals. It has been observed that soil animals are able to minimize their exposure by distinguishing contaminated substrate or food and actively avoiding it (Haimi and Paavola, 1998). Thus, density of individuals or concentrations in animal tissues may necessarily not re¯ect the actual concentration in the soil. 4. Promoting land reclamation and amelioration with soil animals When ecological rehabilitation of the soil is the reasonable ®nal goal, soil fauna can be very important for biological activity of the soil after the more or less technically driven bioremediation processes. Activity of decomposer animals in the soil can result in faster recovery of the site and ®nally in properly functioning ecosystem. Especially larger soil animals, such as earthworms, are able to enhance soil physical properties through their comminution and burrowing activity (review by Edwards and Bohlen, 1996). In addition, nutrient cycling at the site can be enhanced through the soil animals' own metabolism and especially, through the increased metabolic activity of soil microbes caused by animal grazing. As most of the biologically cleaned soils are used as a covering layer, e.g. on waste dumps, ecological properties of these soils are considered to be the most important part of the soil quality (Tamis and Udo de Haes, 1995). The success of reclamation of poor mineral soils, polder soils, open-cast mining sites and areas of cutover peats are often limited by poor soil structure, low inherent soil fertility or high soil metal content. Also here, large decomposer animals, especially earthworms, have successfully been used in improving soils (Dunger, 1969; van Rhee, 1969; Curry and Cotton, 1983). Organic matter incorporation has greatly been accelerated and soil structure improved which has resulted in increased soil fertility. In many cases the faunal restoration processes should have been supported by deliberate introductions of earthworms (Dunger, 1969; van Rhee, 1969; Curry and Cotton, 1983) and/or addition of organic amendments onto the soils (Dunger, 1969). Usually, the sites with remediated soils are small and have long edges in relation to their area, and therefore natural immigration may play an important role in colonization by soil animals (Tamis and Udo de Haes, 1995). On the other hand, Rundgren (1994) found out, when studying the remediation of acidi®ed coniferous forest soils through liming that remediation programme should include earthworm inoculations, because the dispersal and colonization abilities of these animals are low. The site can be ameliorated in several ways to provide more suitable habitat conditions for soil decomposer animals. As mentioned earlier, these measures include liming to counteract soil acidity and metal toxicity, addition of organic amendments, and establishment of plant cover. Spreading of clean soil can also provide as an inoculum of diverse soil fauna. More important than certain faunal structure with particular species of the decomposers is the proper functioning of the community and decomposition J. Haimi / Environmental Pollution 107 (2000) 233±238 processes. However, all species do not have an equal impact on ecosystem processes. Opportunistic colonizers and keystone species may be a prerequisite for the successful development of the remediated soil (Lawton, 1994). These species are not necessarily among the best species to recover after hostile conditions (Pimm, 1991). While activity of earthworms has lead to enhanced productivity at many reclaimed sites, amounts of metals or other harmful substances have not been aected by the animals. Martinucci et al. (1983) even observed that burrowing and casting activity of earthworms brought the highly hazardous substance TCDD, back to the soil surface from the deeper soil layers. In laboratory experiments, Haimi et al. (1992) showed that while increasing overall soil microbial activity, earthworms did not aect the amount of polychlorinated phenols in the soil. 5. Soil animals as a risk Ð food web transfer of the contaminants In some cases soil animals may transfer contaminants accumulated in them to the above-ground food webs. Especially the earthworms, having considerable ability to accumulate contaminants from soil into their bodies, and having relatively low sensitivity to many of these compounds, can be an important transfer route from soil to the above ground ecosystems (Eijsackers, 1998). Many vertebrate animals, like badgers, foxes and several bird species, are frequently feeding on earthworms. Because bioconcentration factors (concentration in earthworms vs. that in soil) have been observed to be quite high, it has been calculated that maximum permissible soil concentrations for e.g. heavy metals are often exceeded, even in normal agricultural soils (Spurgeon and Hopkin, 1996). In central Finland, earthworms have been found in high numbers in several compost piles built for degradation of PCPs. Surprisingly, even the compost-living species Eisenia andrei was very abundant in these piles (consisting of sawdust and contaminated soil) which indicate high microbial activity in the material (J. Haimi and J. Salminen, unpublished information). These specimens contained high amounts of several polychlorinated compounds in their bodies, and also compounds which were not found in measurable amounts in the soil (Knuutinen et al., 1990). However, because the total biomass of these earthworms was quite small, and their distribution was very local, the real threat to predators of the earthworms was limited. Dense populations of several species of earthworms were also found in highly PCP-contaminated soils at an old saw-mill site in central Finland (Knuutinen et al., 1990). Here, the earthworms had obviously avoided high accumulation of PCP through their behavior, 237 because concentrations were signi®cantly lower than could have been predicted from the soil concentrations (Knuutinen et al., 1990). As already pointed out earlier, the burrowing and casting activity of earthworms can bring hazardous chemicals from deeper soil layers back to the surface. This has been observed in Seveso, Italy, in the case of TCDD (Martinucci et al., 1983). Continuous mixing of soil layers may easily lead to continuous exposure of above-ground biota to the contaminants in the soil. In addition, it should be noted that there is a potential risk of contaminant transport down into deeper soil layers or even to ground water by preferential ¯ow of rain water along earthworm burrows. References Callahan, C., Linder, G., 1992. Assessment of contaminated soils using earthworm test procedures. In: Greig-Smith, P., Becker, H., Edwards, P., Heimbach, F. 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