ECOTOXICOLOGY

AND

ENVIRONMENTAL

SAFETY

23,22 l-236 ( t 992)

Validation of Earthworm Toxicity Tests by Comparison with Field Studies: A Review of Benomyl, Carbendazim, Carbofuran, and Carbaryl C. A. M. VAN GESTEL’ National Institute of Public Health and Environmental Protection, P.O. Box 1. 3720 BA Bilthoven. The Netherlands Received June 17, 1991 To investigate whether results of laboratory toxicity tests with earthworms are capable of being used to predict effects in the field, a literature study was carried out. Benomyl, its metabolite carbendazim, carbofuran, and carbaryl were chosen as model substances.From data on the behavior of these pesticides in soil, it can be concluded that shortly after application most of the dosage will be in the top 2.5-cm soil layer. Soil concentrations can be estimated from field dosages used. Estimated field soil concentrations that affected earthworm populations were in agreement with effect levels determined in laboratory studies. In the field, species living in the surface layers (e.g., juveniles of many species) or coming to the soil surface to feed (e.g., Lumbricus terrestris) are most affected, since they experience a high degree of exposure. Evidently, species having long generation times need a relatively long time to recover. Both the distribution of the pesticide and the behavior of earthworms in soil affect earthworm exposure. Insight into these aspects may provide tools to predict both short- and long-term effectsof pesticides on earthworm populations in field soils. 0 1992 Academic press, Inc.

1. INTRODUCTION In recent years, guidelines to determine the acute toxicity of chemical substances for earthworms have been established (OECD, 1984; EEC, 1985). Recently a method for assessing the effect of chemicals on the reproduction of earthworms was published (Van Gestel et al., 1989). In ecotoxicology, laboratory toxicity data are used to: (a) predict the potential impact of pesticides on earthworm populations in agricultural land; (b) assess the potential hazard of industrial chemicals for terrestrial ecosystems: and (c) establish “safe” values for industrial chemicals and pesticides in terrestrial ecosystems. The first item concerns the protection of earthworms as important contributors to soil fertility. The second item implies the use of laboratory toxicity data in the registration of new chemicals. The last two items also involve the prediction of levels of no concern for whole ecosystems. Such an extrapolation from laboratory to field, like that proposed by Van Straalen and Denneman (1989), requires data on a number of organisms representative of the ecosystem to be protected. ’ Present address: Department of Ecology and Ecotoxicology, Free University, De Boelelaan 1087, 108 I HV Amsterdam, The Netherlands. 221

0147-6513192 $3.00 Copyright 0 1992 by Academic Press. Inc. All rights of reprG&ction in any form resewed.

222

C. A. M.

VAN

GESTEL

Since there are many differences between laboratory studies and field situations, the question arises whether results of such laboratory tests are capable of predicting effects in the field. Some differences between laboratory and field studies can be mentioned. -In the laboratory, only one or a few species are tested, mostly cultured and selected on the basis of the ease of culturing and handling; in the held many different species are present. -In laboratory studies, all test organisms are of the same age and health, whereas in the field organisms representing different age classes and exhibiting great variations in physical condition are present. -Laboratory tests are carried out under optimal conditions (temperature, pH, soil moisture content, etc.); in the field environmental conditions are highly fluctuating. -In laboratory studies, test chemicals are mixed homogenously through the soil, and only one chemical is tested at a time; in the field, distribution of chemicals is always inhomogeneous, and organisms may be exposed to mixtures of chemicals. -In the field organisms may suffer from other stress factors, like predation and competition. -When long-term or repeated exposure takes place, adaptation and selection of less sensitive species may occur in the field; on the other hand, adaptation may increase sensitivity of organisms. -In the field, biological availability of chemicals may be lower than in laboratory tests. Field studies are quite expensive, and results are often overshadowed by natural variations and the influence of fluctuating environmental conditions. From a practical point of view, it is impossible to test all chemicals in the field. Laboratory tests are, therefore, required to gain insight into the potential risk of chemicals for ecosystems. The use of laboratory data requires that test systems resemble natural situations as much as possible (Committee to Review Methods for Ecotoxicology, 1981). Only careful design of laboratory tests can guarantee that test organisms react the same way as in the field. Therefore, it was recommended (Committee to Review Methods for Ecotoxicology, 198 1) that test procedures should be verified as resembling the natural system, either by using data in mathematical models to predict effects or by validating with field studies. To follow this recommendation, a literature study on the earthworm toxicity of four pesticides in laboratory and field studies was carried out. The choice was made to use pesticides as model substances, since for these chemicals time and rate of application are well known, and sufficient literature information is available on their behavior in soil. This enables the estimation of exposure levels of earthworms in the field. Benomyl, its metabolite carbendazim, carbofuran, and carbaryl were chosen for this study since considerable information on their toxicity to earthworms in both laboratory and field studies is available. 2. EARTHWORM

TOXICITY

IN LABORATORY

STUDIES

Tables 1 through 4 summarize the literature on the acute and chronic toxicity of the four pesticides under study for earthworms. In these tables, results are expressed as LC50 (concentration giving 50% mortality) and NOEC (no-observed-effect concen-

VALIDATION

OF EARTHWORM TABLE

223

TOXICITY TESTS

1

SUMMARYOFLITERATURE DATA ONTHEACUTETOXICITYOFBENOMYLFOREARTHWORMS Duration Temperature Species Soiltype/substrate (days) (“C) E. andrei

Artificialsoil Artificialsoil Artificialsoil

E. fetida L. terrestris

28 14 21 42 Artificialsoil 14 Sand/soil (4:1) lo-29 Sandyloam/peat 14 Sandyloam/rabbit 7 feces(855) 14

22 22 20 22 24 10-15 13

Reference 22 19 6.0 5.1 27 11” 3.5 1.7 0.4

Heimbach,1984 Heimbach,I985 VanGestelet al., 1992 HaqueandEbing,1983 RoarkandDale,1979 HaqueandEbing,1983 RamakandHamelink.1982

aCalculated fromdatagivenby the authors,considering a soilbulkdensityof I400kg. mm3.

tration) values. Because soil characteristics may have great influence on the bioavailability and on the toxicity of chemicals, only studies carried out in soil are evaluated. Studies carried out in artificial substrates, like filter paper or silicagel, and in 100% dung are not taken into consideration as results of such studies cannot be related to effects in real soil. The artificial soil mentioned in Tables l-4 is the substrate prescribed by OECD (1984) and EEC (1985) or a similar substrate containing 10% peat as organic matter. The high sensitivity of Lumbricus terrestris for benomyl in the study of Kamak and Hamelink (1982) (Table 1) may be caused by the use of a mixture of soil and rabbit feces. Lofs-Holmin (1980), using mixtures of soil with cattle dung, observed high mortality and poor reproduction of the earthworms in sandy soil (Table 2). Results obtained in the latter substrate therefore have to be considered less reliable. Only two studies on the toxicity of carbendazim for earthworms were found, both carried out in OECD artificial soil. Van Gestel et al. (1992) determined the effect of TABLE

2

SUMMARYOFLITERATUREDATA ONTHECHRONICTOXICITYOFBENOMYL FOREARTHWORMS Species

Soiltype/ substrate

Duration (days)

Parameter

E. andrei

Artificialsoil

42

Reproduction

A. caliginosa

Clay + dung1:1 (10%OM)

26 90

Cocoonproduction Growth

Sand+ dung1:l (10%OM)

90

Growth

A. A. L. A.

chlorotica rosea terrestris caliginosa

A. rosea A. chlorotica L. terrestris

NOEC (mgakg-‘) 1.0 0.25 >0.5 >0.5 >0.5 0.25

Validation of earthworm toxicity tests by comparison with field studies: a review of benomyl, carbendazim, carbofuran, and carbaryl.

To investigate whether results of laboratory toxicity tests with earthworms are capable of being used to predict effects in the field, a literature st...
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