Agriculture, Ecosystems and Environment, 34 (1991) 341-362 341 Elsevier Science Publishers B.V., Amsterdam, Invertebrates as bioindicators of soil use Maurizio G. Paoletti', Maria R. Favretto', Benjamin R. Stinner’, FF. Purrington? and J.E. Bater? ‘Department of Biology, Padova University, Via Trieste 75, 35121 Padova (Italy) *Department of Entomology, Ohio State University, Wooster OH 44691 (U.S.A,) (Accepted for publication 5 July 1990) ABSTRACT Paoletti, M.G., Favretto, M.R., Stinner, B.R., Purrington, F.F. and Bater, J.E., 1991. Invertebrates as bioindicators of soil use. Agric. Ecosystems Environ., 34: 341-362. We face an increasing demand from administrative, technical and environmental authorities for bioindicators. Animals, plants and community patterns, which register quantitative and qualitative environmental changes need to be monitored. This can range from simple chemical and physical sam- pling to quantifying the patterns of animal and plant communities. These techniques for analysing soil communities were first developed for aquatic systems, Protozoans, earthworms, woodlice, myria- pods, Acari, springtails and other groups of invertebrates seem to respond to chemical residues and other environmental stresses in many different ways. Although a rich literature on interactions is available, only limited information exists at the community level and little is known of the food chain level in the soil. Research is needed to find appropriate patterns which could model different situations. AN OVERVIEW There is increasing demand for the use of animals, plants and microorga- nisms as bioindicators of environmental impact. Similar requests are being made for evaluating the success of reclamation of damaged areas. Biologists are asked to formulate judgements and evaluation scales regarding the envi- ronmental quality of groundwater and rivers (Woodiwiss, 1978; Ghetti, 1980, 1986; Lebrun, 1981; Blandin and Lamotte, 1985; Blandin, 1986) and other water bodies, and, in recent years, of soils (Sturhan et al., 1986; Curry, 1987; Foissner, 1987; Paoletti et al., 1988). Bioindicators are especially used for evaluating the impact of acid rain and agricultural practices (fertilizers, pesticides residues, tillage, manures, etc.), or the reclamation of contaminated areas, such as city dumps and industrial developments. Power plants and industrial developments are required to evaluate their impact on the surrounding environment. For centuries naturalists were asked to describe and list “‘simplicia” (sim- ple, not human living creatures) around the world. For many decades, natu- 0167-8809/91 /$03.50 © 1991 — Elsevier Science Publishers B.V.342 M.G, PAOLETTIET AL. ralists, and more recently ecologists, have argued about diversity, biological richness, and animal and plant abundance as measures of environmental quality (Odum, 1969; Wilhm, 1975; Golley, 1977; Wilson, 1988). Now bi- ologists are called upon to determine the anthropogenic impacts on terrestrial and aquatic ecosystems. How to define soil invertebrates Some authors indicate soil invertebrates as those living mostly inside the soil which have “‘modified” morphology, behaviour and physiology com- pared with other epigeic invertebrates (Coiffait, 1958). We believe that this approach only deals with a limited portion of soil biota. For us, soil inverte- brates comprise all larval and adult stages living temporarily or permanently in the soil and sometimes on its surface. Most animal groups are involved (Kevan, 1962; Dindal, 1989). It is suggested that soil invertebrates make only a moderate impact on the energy flow in soils dominated by microbes (Crossley et al., 1989), but their importance in decomposition is variable between 1 and 2% up to 30% (Pers- son, 1980). The comminution rate of litter matter by soil invertebrates can attain 68% (Seastedt, 1984; Anderson, 1988). Interaction with other soil biota is far more important (Crossley et al., 1989), such as microbial activity, predation, parasitism, dissemination of mi- crobes, seeds and micorrhyza (Rabatin and Stinner, 1988). HISTORICAL SURVEY OF IDEAS ON SOIL ORGANISMS AS BIOINDICATORS In 1644, many years before the agronomic revolution of the eighteenth cen- tury, Vincenzo Tanara defined agrarian soil fertility as follows: “when birds such as ravens, magpies and others are attracted to a freshly ploughed field and scratch on the soil to eat the small invertebrates released by the plough.” Tanara means that soil animal activity is an indicator of soil fertility. This idea contradicts the mainstream opinion of that period when worms and in- sects were generally accepted as noxious to cultivated plants and sponta- neously regenerated from rotting materials (Gallo, 1584; Tarello, 1567; Redi, 1668; Agostinetti, 1679). Darwin (1837, 1881) suggested that earthworms represent a consistent, underestimated element of activity in the soil, and fo- cused on the role of worms in building soil surface castings and producing humus (vegetable mould). More recently Kubiena (1953) emphasized that soil animals play a decisive role in the formation of soils and humus. In spite of that, Kevan (1962), argued that “soil biology [study] is a long way behind that of freshwater biology and one wonders if this is because biologists, as a whole, would rather get their feet wet than their hands dirty!””. Several inter- national conferences on soil biology, zoology and ecology, since the first oneINVERTEBRATES AS BIOINDICATORS, 343 organized and edited by Kevan (1955), have demonstrated increasing inter- est in soil animals for monitoring biotic and abiotic effects in soils. More re- cent conferences (Brandt and Agger, 1984; Paukert et al., 1986; Arndt et al., 1987; Richardson, 1987; Edwards et al., 1988; Bohal and Ruzicka, 1989; Pa- oletti et al., 1989b) emphasized more information and opportunities for fur- ther research on soil organisms as soil bioindicators. Invertebrates and heavy metals “The distribution of metals on a geographical basis is assessed invariably by measuring concentrations in abiotic components of ecosystems such as air and soil” ...“‘At present we do not have sufficient knowledge of the rates of transfer of metals between species at each trophic level” (Hopkin, 1989). Heavy metals (for definition see Hopkin, 1989), the more common of which are: Fe, Cu, Zn, Se, Cr, Mn, Pb, Sn, Hg, Co, Ni and V, affect soil biota in many different ways, sometimes lethally. However, Fe, Cu, Co, Se, Zn and Mo, are also essential trace elements required for normal growth and repro- duction in higher vertebrates, although in excess they disturb the physiology of the biota, including the invertebrates in soil (Weiser et al., 1977; Jaggy and Streit, 1982; Hopkin, 1989; Piccinni, 1989). Metal uptake through the food is normal, however, absorption through the body surface is also possible, at least for slugs (Cavallero and Ravera, 1966). Soil invertebrates especially earthworms (Ireland, 1979, 1983; Paoletti and Bertoncello, 1985; Paoletti et al., 1988) in orchards and vineyards treated with copper sulphate are highly affected in terms of biomass and species number (Paoletti et al., 1988) (Fig. i) Much work has been done recently owing to the feasibility and moderate cost of heavy metal analysis especially by atomic absorption and plasma mass spectrometry (Eaton and Hutton, 1988). Springtails, oribatid mites and other Acari have recently been examined for their heavy metal content (Bengtsson and Gunnarsson, 1984; Van Straalen et al., 1987; Janssen, 1988). Some social invertebrates, including ants, are promising as environmental indicators (Stary and Kubiznakova, 1987). Isopods, centipedes, millipedes, spiders and carabid beetles have also provided important information for soil-metal pol- lution interactions (Hopkin, 1989; Paoletti et al., 1988). The biomagnifica- tion of heavy metals in animal food chains is not easy to demonstrate in field work; however at least Cu and Zn show a modest accumulation between de- tritivores and their possible predators. Only partial correlation of air pollu- tion and metal content of bees and pollen was shown in Poland (Migula et al., 1989). That is possibly attributable to the rapid movement of predators which can recolonize contaminated areas (such as vineyards) rapidly from surrounding sites.344 M.G. PAOLETTIET AL. SS ae F 4 N MONTHS Fig. 1. Agroecosystems near Padova, Italy. Earthworm biomass, seasonal variation and Cu con- tent of soil in a vineyard. (—)=biomass g m~?; (- - -)=Cu ppm dry weight; F=February; J=June; N=November. Letters within the figures indicate Duncan's test results. Different up- per case letters indicate significant differences between different dates (P<0.05), different lower case letters indicate highly significant differences (P<0.01)) from Paoletti et al. (1988). Pesticide residues in soil Pesticides are extensively used in agricultural activities and affect non-tar- get soil invertebrates. (Thompson and Edwards, 1974; Ridgway et al., 1978; Plapp, 1981; Domsch et al., 1983). Invertebrates and pesticide residues in soil have been studied recently, but the high cost of analysis and the huge number of pesticides on the market pose serious, practical problems (Brown, 1978; Simon-Sylvestre and Fournier, 1979; Edwards, 1989). Earthworms (especially Eisenia foetida and Lumbricus terrestris) have been used in standardized laboratory tests for many different pesticide residues (Haque and Ebing, 1983; Heimbach, 1985). Lee (1985) has reviewed 50 papers (1952-1982) dealing with pesticide toxicity among earthworms. Many soil invertebrates (mesofauna) have been tested in field plots treated with different marketed products (Thompson and Edwards, 1974; Eijsakers and Van der Drift, 1976; Brown, 1978; Eijsakers and Van de Bund, 1980). However, field responses, together with soil resili- ence, are subject to many variables (soil moisture, temperature, composition, structure, microbiology, etc.), which sometimes give uncertain and contra- dictory results. Standards for field work are far from generally accepted and much work is needed (Edwards, 1989; Hassan, 1989). Sometimes products, such as herbicides, applied to the soil have bigger im- pacts on foliage dwelling invertebrates, such as aphids (Rhopalosiphum mai- dis) and common corn smut disease (Ustilago maidis) on corn (Zea mays), which have been reported to increase after 24 D application (Oka and Pimen- tel, 1974). Therefore tests conducted strictly by looking at on-soil effects can be misleading, at least on crop fields.INVERTEBRATES AS BIOINDICATORS, 345 Landscape structure and quality Soil macrofauna such as earthworms, ants, woodlice, millipedes, cen- tipedes, spiders, harvestmen and beetles seem better suited as bioindicators describing landscape mosaic parts since they are more easily collected, sorted and identified compared with micro- and mesofauna. High sample numbers have caused some researchers to use motor netting for flying invertebrates associated with the soil fauna, such as dung beetles, some staphilinid beetles and some ground beetles (Karg, 1980, 1989). Pitfall traps have been used extensively (Brandmayr, 1983; Forman and Godron, 1986; Baudry, 1987; Burel, 1987; Curry, 1987; Paoletti et al., 1985, 1988; Purrington et al. 1989) and handsorting of soil cores less extensively (Paoletti, 1988). Hedgerows have been monitored using pitfall traps (Thile, 1977; Burel, 1987; Nazzi et al., 1989). Using litterbags (Edwards and Heath, 1963; Dodd and Lauenroth, 1980; Seastedt and Crossley, 1980) of different mesh sizes it is possible to select the size of the biota entering the litter bag and affecting the decomposition rates. This system can be used to monitor soil organism activity in soils. Increasing the scale of the study area multiplies the sample number re- quired for quantitative analysis and therefore requires more people and time. In landscape ecology much work is needed to collect more adequate data. Remote sensing could prove promising if the measurement of soil biotic pa- rameters improves (Wessman, 1991). Agricultural operations Agricultural operations, such as tillage, rotation, fertilization and irrigation (Coleman, 1985; Ryszkowski, 1985; Lagerlof, 1987; Brussaard et al., 1988; Kooistra et al., 1989), management of weeds (Altieri and Liebman, 1987) and use of hedges, tree rows or woodland remnants (Paoletti et al., 1989a) have a strong impact on soil biota, both living above the soil and under the soil surface (Paoletti, 1988). Different machinery operations, such as disk- ing, affect soil invertebrates, such as earthworms (Edwards and Lofty, 1977; Lee, 1985) and other soil invertebrate macrofauna (Paoletti, 1988). Inter- actions among soil biota are synergistic and little is known about them (Fig. 2). High vs. low input farming such as mulching, rotation, organic fertiliza- tion, minimum and no-tillage (House and Stinner, 1983; Holland and Coleman, 1987; Paoletti, 1987; Stinner and House, 1989) have been re- searched but more needs to be done. For example, little is known about ridge tillage (Authors, 1989; Pimentel et al., 1989). Living mulch in vineyards with subterranean clover considerably increases invertebrate activity in the Medi- terranean area (Fig. 3).346 M.G. PAOLETTIET AL, AGROECOSYSTEMS Fig. 2. Agroecosystems near Padova, Italy. Mean annual values of earthworm biomass (—) =e 2, (- = -)=number of specimens m 9. a=river bank meadow; b=garden meadow, c=alfalfa; d=vineyard; e=corn. Letters within the figures indicate Duncan's test results. Dif- ferent upper case letters indicate significant differences between different dates (P< 0.05), dif- ferent lower case letters indicate highly significant differences (P-<0.01). Urbanized and polluted areas Mosses (Bryophyta) have been used as bioindicators of heavy metal pol- lution in urbanized areas (Lepneva et al., 1987). The problems involved are similar to those for power plants. Mountain ski slopes effect ecological changes in soils (Cernusca, 1978; Foissner, 1987). Power plant areas Research has documented the sensitivity of soil mesofauna, such as Col- lembola and Acari and scavengers, such as dung beetles (Preston and O’Guinn, 1980; Preston et al., 1981) to power plants. Atomic and other hazardous plant locations, radiation hazards Krivolutsky (1987a,b) has demonstrated the reaction of soil invertebrates to soil radioactive contamination. Industrial settlement areas and contaminating emissions Dioxin contamination (Martinucci et al., 1983) and contamination caused by dry precipitations (Freitag and Hastings, 1973; Freitag, 1979) have been shown to impact on soil invertebrates (Fig. 4). Sour gas plants (Church et al., 1986), coal-fired power plants, and SO, emissions damage some soil in- vertebrates, such as coprophagous and scavenger beetles (Preston and O’Guinn, 1980; Preston et al., 1981.) The smoke-gas emissions from alumin- ium plants also affect soil algae (Melnikova, 1987). Reclamation areas, such as quarries, mines and dumps Soil invertebrates provide important information on reclamation and pol- lution problems (Dindal et al., 1977; Huhta et al., 1979; Koehler and Born,INVERTEBRATES AS BIOINDICATORS 347 SEPT.88-LIVING MULCHING ON VINEYARD SUBTERRANEAM CLOVER 2 / i a 61 7, 2 IV z Joweates a fo) fastiowata = 00 — Cay 7 fprosmamata 3 SJ SSS footer e a — ra ret B50, —— Hh ef 1 psocopteRa = — Jcouroprena 7 7 HIMENOPTERA MULCHED+N MULCHED = =—sBARE+N BARE DEC.88-LIVING MULCHING ON VINEYARD SUBTERRANEAN CLOVER s 2 oer 2 ff jonwaten a J /astigmata = ‘PROSTIGMATA 5 =F [atten g J esostesuara & [orienn /REDAT. URvAE f /srapanumo ne MULCHED+N MULCHED ~=—sBARE*N- BARE. Fig. 3. The case of living mulching in Mediterranean vineyards (with Trifolium subterraneum). Sustainable agriculture forms increase certain amounts of soil invertebrates and more interac- tions are also carried out in the soil surface. Living mulches in vineyards in Mediterranean regions, where the soil under vine on a monthly base is worked, interact with soil invertebrate typology and biomass. Fertilizers (50 kg year~') show little effect when applied to mulched and non-mulched plots, except on Collembola. Collembola, oribatid and astigmatic mites (fungi- vores and detritivores) as well as mesostigmatic mites (generalist predators) are affected by mulching. Some trends found in September 1988 become stronger in December 1988, 8 months after subterranean clover seeding. 1989). In the Netherlands earthworms have been introduced in a new re- claimed polder with amelioration of physical and chemical growing condi- tions for grass (Hoogerkamp, 1987). In New Zealand, the introduction of earthworms, originally from the palearctic region, into the grassland has sometimes been manipulated directly by farmers (Stockdill, 1982; Syers and Spingett, 1983; Lee, 1985).348 MG. PAOLETTIET AL. 40 23 . le a0 8 \ . 8 o ° . 2 3 le 5 20 ° 3 3 .° 5 3 ° E = 10 ° 2 | © Fallout | © Beetles aes i T 500 1000 1500 2000 2500 Distance from mill, y Fig. 4. Composite plot of average annual 1970-1971 SO3~ fallout and size of summer 1971 beetle population samples vs. distance from a kraft mill in Thunder Bay, Ontario (from Freitag and Hastings, 1973). Roadsides, railroad beds, pipelines and electric lines Wade et al. (1980) have demonstrated that soil invertebrates react to heavy metal pollution. Lead may be the dominant cause of toxicity near roadsides (Battaglini and Rosso, 1974; Goldsmith and Scaloni, 1977). Acid rain Environmental problems caused by acid rain have led to a considerable amount of research on soil invertebrates in woodlands (Hagvar, 1984) as well as in agricultural soils (Stinner et al., 1987) and grasslands (Leetham et al., 1984) both on microarthropods (Collembola, Acarina, Enchytraeids) and earthworms (Huhta et al., 1983; Fuehr et al., 1985). Sulphate in soil affects soil invertebrates but interactions in soil are very complex and, as for many pesticide residues, the results seem to be controversial (Hagvar, 1984) more than for SO, emissions from industrial plants (Freitag, 1979) (Fig. 4). Sul- phate emissions seem to affect the parasites of soil invertebrates. In some forests in Germany an increased infection rate of Enchytraeidae, Lumbrici- dae, Acarina, Collembola and Diptera was found at locations with higher SO, emissions (Purrini, 1981). COLLECTING SYSTEMS There are several published manuals that provide information on collecting soil invertebrates (Murphy, 1962; Southwood, 1966; Wallwork, 1976; Phil- lipson, 1971; Edwards and Lofty, 1977; Lee, 1985; as well as many others). In any case, it is useful to point out some of the easy, simple and promising systems.INVERTEBRATES AS BIOINDICATORS. 349 Pitfall traps Traditional systems involve pitfall traps or Barber traps (Barber, 1931). Many different modifications have been applied to this very simple but effec- tive system, such as introduction of bait (piece of meat, bone, cheese, animal faeces, etc.) or introduction of sweet liquid, beer, fruits, etc. The traps can be left empty or filled. Formalin 2-5% solution, potassium bicromate solution, ethylene glycol, water or ethanol solution are recommended. Propylene gly- col, atoxic and odourless, in water or ethanol solution is suggested. Each pre- servative affects a different group of invertebrates. For instance, formalin so- lutions attract more ants than ethanol solution with ethylene glycol (personal unpublished observations, 1989). Barriers can be positioned near pitfall traps in order to detect the directional movements of surface-moving invertebrates. Lids can be used to cover pitfall traps preventing precipitation from filling the traps and microvertebrates from entering (Fig. 5). Pitfall traps give a measure of soil surface activity. Handsorting invertebrates from soil samples Soil cores of 30> 30 cm square, or more, are dug up with a spade to 15-30 cm. The soil is handsorted on a white plastic or cotton sheet in situ or at the laboratory. Animals larger than 3-4 mm can be sorted without any optic de- vice. This simple system is very effective (Bouché, 1975; Ghilarov, 1979) but time consuming. Hand sorting yields an absolute measurement of inverte- brate density. Chemical and physical methods Formalin solution (0.2-2% ), CuSO, (5-10%) and other chemicals (HgCl2 and KMnO,) have been applied by soaking the soil at a rate of 5-101 solution per m’ to collect macrofauna (over 2-4 mm) especially earthworms (Bouché, 1972; Edwards and Lofty, 1977; Lee, 1985). Funnel extractor systems The modified Berlese (1905) systems described by Tullgren (1917) and others, like Macfadyen, (1961), Merchant and Crossley (1970), Edwards and Fletcher (1971), have improved the efficiency of extracting invertebrates from soils (Vannier, 1970; Garay, 1989). Some flotation systems (Murphy, 1962) such as those of Walter et al. (1987), using heptane, are sometimes more efficient, but more time consuming. Flotation of soil in water with some dif- ferent salts (Raw, 1955) has permitted the collection of macrofauna inverte-M.G. PAOLETTIET AL. Fig. 5. Some collection and extraction systems. Pitfall traps (a) with barriers to detect the di- rectional movements of surface-moving invertebrates (OARDC, Wooster, OH). Modified Tull- gren funnel for macrofauna (b) (Padova, Italy) (see text). Figures c, d and ¢ show a simplified gradient temperature Tullgren system (see text) for soil and litter micro- and mesofauna extraction. brates and eggs. Washing the soil in a battery of steering sieves (Bouché, 1972; Lee, 1985) has permitted massive sampling of soil earthworms. This system. is not always practical because of the large volume of water required. Flota- tion in NaCl-saturated water solution of soil samples has offered 30-40% more soil larvae insects than handsorted samples (Nabiatczyk Karg, 1980). A simplified Tullgren funnel adopted for soil and large litter samples toINVERTEBRATES AS BIOINDICATORS 351 extract invertebrate macrofauna is shown in Fig. 5b. The structure is made of galvanized sheet-iron. The litter and soil samples are placed in a mesh basket that rests in the top of the funnel. The lids that cover the funnel are made of plankton nylon mesh and held in place by a heavy iron ring. This system pre-352 M.G. PAOLETTIET AL. vents the escape of active invertebrates (e.g. spiders, centipedes, ground beetles). A simplified system of 84 plastic canisters, useful for the extraction of mi- cro- and mesofauna is shown in Fig. Sc. The steel tank supports a refrigeration system of running water on the bottom; the cover is equipped with electric resistances. The gradient of temperature can be regulated between 30-50°C on the top and 10-28°C on the bottom. The extraction canisters (Figs. 5c-e) are composed of four pieces: a lid covered with plastic mesh; a plastic con- tainer that holds the sample; a second lid; a final plastic container that holds the preservation liquid (Fig. 5d), to form a closed system that prevents the escape of invertebrates. The collection liquid used is propylene glycol and water. Protozoans, nematodes and enchytraeids need particular extraction meth- ods which are developed in the manuals listed or in the textbooks (see Mur- phy, 1962; Wallwork, 1976; Bachelier, 1978). Fixation, preservation and identification It is often relatively easy to collect, preserve (ethanol 80% or formalin 3- 5%) and sort invertebrates by higher taxa such as orders and sometimes by families. However identification at genus and species level usually requires more skill. Macrofauna, such as earthworms, terrestrial isopods and some beetles are relatively easily studied using appropriate manuals, but meso- fauna and microfauna, such as Acari, Protura, Diplura and Collembola need. expert taxonomists, and for many insect larval stages it is difficult to obtain a proper identification (Peterson, 1960, 1962). DISCUSSION Invertebrates as soil bioindicators can respond to many different condi- tions of soil stress in several ways: (1) at a higher taxa level (class, order, family), (Figs. 6-9); (2) at a lower taxonomic level (tribe, genus, species); (3) at the functional level (herbivores, detritivores, scavengers, predators, parasitoids, etc.) (Ghilarov, 1970; Wiegert et al., 1970; Elliott et al., 1988); (4) at the community structure level, ecosystem level, watershed level and landscape level, (Karg, 1980, 1989; Baudry, 1987); (5) at the reproductive, physiological and biochemical level (Purrini, 1981; Hopkin, 1989). Soil invertebrate bioindicators must give sufficiently clear responses to en- vironmental stresses and these changes, both in numbers or of taxonomic di- versity, must be relatively stable in order to be monitored easily. Unimpeded re-immigration in a contaminated or disturbed field affects the levels of toxicants in soil animals and also affects the expected data of con- tamination of the food chains involved (Paoletti, 1988) (Fig. 10). Less mobile soil invertebrates (some earthworms, some coleopteran andINVERTEBRATES AS BIOINDICATORS, 353 ys=10208- avoH10x b4, Feosn0e Oribatid species No. 1 1 1 1 ris sob 20808 tdor—art8 Tototal mean annual macro-plus microfauna per m? Fig. 6. Mean annual soil and litter invertebrate macrofauna plus micro/mesofauna and oribatid mites species number found in four lowland residual deciduous woodlands (b1-b4) and six monocultured corn fields. Northeastern Italy (from Paoletti, 1988). 244 yvg3801+000639% b4o « 3038 " p20 63 E wo é a Zoe E b2 = | ° Zot, ° foiKe a 1 1 1 1 eis t0iaoms estas Microfauna (Tullgren) per m2 Fig. 7. Total soil and litter micro/mesofauna (modified Tullgren extraction ) and mean annual earthworm numbers per m? in four lowland residual woodlands (b1-b4) and six monocultured corn fields. Northeastern Italy (from Paoletti, 1988). dipteran larvae, isopods, millipedes ) are expected to respond to the localized stresses more permanently. In any case, it is difficult to begin a monitoring system without a well-extended preliminary study of the ecosystem involved, the community patterns and the landscape structure and history. It is easier to operate using higher taxa; at the species level the work is much more time consuming, if not impossible, and taxonomic expertise is required. Some- times taxonomies do not improve the results in detail, in spite of the time required for acquiring proper taxonomic knowledge (Figs. 7-8). However, poor taxonomic knowledge (Kevan, 1985) is not recommended! Food chain level knowledge and community level work still need further research, but in our view this knowledge is fundamental in order to construct or reconstruct a model of the food web interaction in soils (Elliott et al., 1988). The number of biota living in the soil or interacting with it are numerous (Dindal, 1989) and only a small number of them are easily identifiable and354 M.G. PAOLETTIET AL, 3004 fee p £0,000 S soo [tanasereens EFFECTS OF LITTER CAPTURE 180 Litter volume jem?) Fig. 8. Relationships between the litter amount (in cm?) and different macroarthropods in de- ciduous woodlands situation in France (from Garay, 1989). Al Fig. 9. Dendrogram of habitat discrimination (clustered species similarity index of Sorensen ) by soil ciliates: (a) 12 sites in the Austrian Alps (Glockner area); (b) 11 sites in the Austrian Alps (Gastei area); (c) two wheat fields (Austria, Tullnerfeld area); (d) two xerothermic un- cultivated grasslands (Austria, Tullnerfeld area); (g) four wheat fields (Austria, Salzburg area); (h) six meadows (Austria, Salzburg area); (i) two spruce forests (Germany, Ulm area) (from Foissner, 1987). hii go easily known by habit, food preference, biology, reproduction, etc. (Kevan, 1985). We have estimated in a range of 800-1500 the species of invertebrates living in the soil and on plants in the corn agroecosystems of northeastern Italy (Paoletti, 1988). Less than 600 invertebrate species have been reported (mostly on plants) in corn fields in Hungary (Meszaros, 1984a), and 1759 species in apple orchards (Meszaros, 1984b). In a corn field in northeastern Italy soil could contain 200-450 invertebrates, and less disturbed lowland deciduous forest could contain 300-500 invertebrate species (Paoletti, 1988). In three national parks in Hungary, 4433, 7384 and 8843 animal species have been listed (Mahunka, 1987). In a north Italian swamp 1178 animal species have been listed (Daccordi and Zanetti, 1989). It is difficult to manage such large numbers of species! We suggest muchINVERTEBRATES AS BIOINDICATORS 355 44 89.8 a t 4 Dipnpots]} | tumbvictne | [epee - 4 844.4 3S ae ogg 1200 9134 30.7 106.6 Talpa LJ 99 161 [| Fig. 10. Pesticide residues in the soil of an agroecosystem with vineyards: copper as a residue of the fungicide Bordeaux mixture in the soil food chain in the Veggiano agroecosystem, near Pa- dova. Copper residues in the vineyard soil are very toxic to earthworms. In this landscape of small-scale farms, invertebrates move rapidly from the nearby fields. The samples collected and analysed in one year (pitfall traps and 30x 30 cm handsorted soil cores) are the result of con- tinuous movement and recolonization. The copper flow chart model shows the low enrichment of copper in the food chain owing to this continuous movement of soil animals. Earthworms and isopods are less active on the soil surface, and accumulate much more copper than carabids and chilopods. Moles (Talpa) concentrate no, or small amounts of, copper. (Shaded arcas: Vineyard samples (Paoletti ct al., 1988). caution and modesty be used when studying the use of soil invertebrates as bioindicators: promises are very interesting but results must be better defined and much basic research is still needed, as suggested by many researchers (Kevan, 1985; Wilson, 1988; Minelli, 1989; Pimentel et al., 1990). ACKNOWLEDGEMENTS Financial assistance from the Ministero Pubblica Istruzione is gratefully acknowledged. Mr. U. Arezzini and U. Friso provided the figures. J. Karg, A. 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