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Effects on earthworm populations of reducing pesticide use in arable crop rotations
PII:
Soil Bid. Biochem. Vol. 29, No. 314, pp. 657-661, 1997 Crown Copyright 0 1997 Published by Elsevier ScienceLtd Printed in Great Britain. All rights reserved 0038-0717/97 $17.00 + 0.00 !Soo38-@717(%)00191-5
EFFECTS ON EARTHWORM POPULATIONS OF REDUCING PESTICIDE USE IN ARABLE CROP ROTATIONS K. A. TARRANT,
S. A. FIELD,
S. D. LANGTON
and A. D. M. HART*
Central Science Laboratory, Sand Hutton, York Y04 ILZ, U.K. (Accepted 24 June 1996)
Summary-The SCARAB project is a field-scale, six-year investigation of the effects of pesticide use on invertebrates and soil microflora in arable crop systems common in the U.K. Two pesticide regimes are being compared: current farm practice (CFP) which represents typical levels of use in the study localities, and reduced input approach (RIA) in which inputs have been reduced by 50% and no insecticides used. The treatments began at three farms in 1990, and effects on earthworm populations have been monitored twice yearly since Spring 1993. Particular attention was paid to age and species composition. Results up to Spring 1994 showed that although some differences existed between earthworm populations in RIA and CFP plots they lacked consistency over time and between the pairs of plots, and were of negligible magnitude compared with overall differences between the farms. It was concluded that the two pesticide regimes caused no ecologically significant differences in earthworm populations at this stage of the project. The substantial differences in earthworm populations between farms were largely consistent with the expected effects of differences in climate, soil types, crop types, cultivations and pesticide use, although the relative importance of these factors can not yet be assessed. Crown Copyright 0 1997 Published by Elsevier Science Ltd
INTRODUCTION
The SCARAB project is a field-scale, long-term investigation of the effects of pesticide use on invertebrates and soil microflora in arable cropping systems (Bowennan, 1993). Two pesticide regimes are being compared on three sites in the U.K. under contrasting crop rotations: current farm practice (CFP), which represents typical levels of use by farmers on similar crops near the study sites, and reduced input approach (RIA), which consists of substantially reduced inputs, especially of insecticides. Earthworms are important because of their role in maintaining soil fertility and structure (Edwards and Lofty, 1977). The intensification of modern agriculture and reliance on the use of pesticides presents potential hazards to earthworm populations. Cultivations can cause substantial mortality of earthworms (Barnes and Ellis, 1979), as may some Bohlen, 1992). and pesticides (Edwards Furthermore, in some cases there may be significant hazards to birds and other vertebrates from ingesting earthworms which contain pesticide residues (Cooke et al., 1992). Both types of pesticide hazard are considered in risk assessment of pesticides for regulatory purposes in the U.K. (Greig-Smith, *Author for correspondence.
1992). Effects on earthworms are therefore being investigated as part of the SCARAB project. The primary objective of the earthworm studies is to monitor effects of the SCARAB treatments on earthworm populations by means of twice-yearly sampling. Monitoring began in Spring 1993, in the third year of the CFP and RIA treatments, and will continue until 1996. Changes will be interpreted in relation to the overall contrast between CFP and RIA levels of pesticide use, and in relation to cropping changes and cultivations during the rotation cycles. Further sampling will be carried out to monitor the immediate effects of particular pesticides thought likely to present a particular hazard to earthworms, in order to assist in understanding longer-term changes. This paper outlines the results obtained so far. Particular attention is given to effects on age and species composition, as these have received less attention in previous studies.
MATERIALS
AND METHODS
Study sites and treatments
The two treatments are being compared at three separate experimental farms in England: High Mowthorpe in North Yorkshire, Drayton in Warwickshire and Gleadthorpe in Nottinghamshire. The three farms include a representative range of 657
K. A. Tarrant et (11.
658
conditions in terms of climate, altitude and soil types. The six-year crop rotations at each site are designed to be typical of the surrounding areas. The experiment is based on a split-field design, including two fields each at High Mowthorpe and Drayton, and three at Gleadthorpe. For the purposes of sampling, the northern and southern parts of one field (Oldtype) at High Mowthorpe are treated as separate fields, in effect giving a total of eight fields. Each field is split into two roughly equal halves, one treated with CFP and one with RIA. CFP is based on general practice on the individual site, to represent pesticide use by a technically competent, financially aware farmer in comparable farming situations. RIA is intended to contrast with CFP in its severity on non-target invertebrates. It includes minimal use of fungicides and herbicides, which are applied at half rate or less. No insecticides, nematicides or molluscicides are used on RIA plots unless a severe threat of crop loss is evident. The treatments began in 1990/91 after a one-year baseline period in which CFP and RIA plots in each field received the same treatment. Overall, less than 50% of the pesticides applied to CFP were used on RIA in 1991, 36% in 1992 and 35% in 1993. No insecticides or nematicides were applied to any RIA plots between Autumn 1990 and Spring 1994, whereas those applied to one or more CFP plots included Aldicarb, Chlorpyrifos, Omethoate, Pirimicarb and Triazophos. Pesticides applied on RIA at half the rate used for CFP included Carbendazim and Flusilazole. The mean number of pesticide applications per crop was 4.9 for CFP, and 2.0 for RIA (half rate applications counted as 0.5). Greater reductions in pesticide use were achieved for the combinable crops. In contrast, the options to reduce pesticide applications to the root crops, sugar beet and potatoes, were limited because of the high risk of yield loss and the lack of thresholds to determine potential losses. Table
1. Total earthworm
densities (CFP,
(numbers
m-l)
Population monitoring
The abundance and diversity of earthworms are monitored biannually, in Spring and Autumn when earthworm activity is expected to be the highest. Three samples are collected in each half-field using a 50 x 50 cm quadrat, dropped at random at lo20 m intervals. Preliminary comparison of the formalin and hand-dug methods indicated that a combination of both was required to obtain fully representative samples of earthworms. This involved hand-digging to the plough layer, followed by extraction of additional worms from below the plough layer using 1.14 1 of a 0.2% formalin solution spread evenly in the base of the hole to bring up any deep-burrowing species that might be below the plough layer (Edwards and Lofty, 1977). Any earthworms emerging in the base of the hole were collected for 20 min after the formalin solution was applied. Sampled earthworms were counted and weighed before being returned to the laboratory in 5% formalin solution. Each sample was subsequently sorted according to species and age classes. The earthworms were identified and classified using the taxonomic details listed by Sims and Gerard (1985). The full names of species mentioned in this paper are as follows: Allolobophora chloroticu Aporrectodea caliginosa (Savigny). (Savigny), Aporrectodea rosea (Savigny), Aporrectodea longa (Ude), Lumbricus terrestris (Linn.) and Octolasium cyaneum (Savigny).
RESULTS
The overall densities of earthworms recorded in the first three sampling periods are shown in Table 1. There were very large differences between farms. By comparison, there were only minor differences between fields within farms, and between CFP and RIA areas in the same field. There was a general tendency for both numbers and biomass to
between Spring 1993 and Spring 1994 in relation to crops and pesticide reduced input approach: see text for details)
Farm
Field
Crop 1992193
Crop 1993194
Treatment
Drayton
One
Grass
Grass
Five
Wheat
Grass
Bugdale
RIA CFP RIA CFP RIA CFP RIA CFP RIA CFP RIA CFP RIA CFP RIA CFP
High Mowthorpe
S. barley
S. beans
North
W. barley
W. oilseed
Oldtype South
W. barley
W. oilseed
South
W. barley
Sugar beet
Balk
W. barley
Potatoes
Near Kingston
S. beans
W. wheat
Oldtype
Gleadthorpe
S, Spring-sown
treatments
current farm practice; RIA,
crops; W, winter-sown
crops
Spring 393 516 493 584 24 23 68 36 19 19 0 0 5 5
1993
Autumn
1993
Spring
I994
756 533 173 616 229 233 144 85 36 28
703 1029 853 981 220 161 Ill 59 43 33
0 0
0
12 17 23 28
2,
n 59 77
Earthworms and pesticides
659
Table 2. Mean numbers of earthworms m- 2 by species, based on data pooled over three sampling periods. Each value is the mean of 36 samples (Drayton and Gleadthorpe) or 54 (High Mowthorpe) Species Lumbricus terrestris
Aporrecrodea longa Allolobophora chlorotica Aporrecrodea caliginosa Octolasium cyaneum Aporrectodea rosea
Unidentified
Drayton
High Mowthorpe
Gleadthorpe
35 26 378
13 20 13
0
233
36
1 21
8 3
4 0.4
0 0
I
I
0
1
increase over time, most of the increase occurring between Spring and Autumn 1993. None of the samples collected from South field at Gleadthorpe contained any earthworms at all. Data for South field were therefore excluded from all statistical analyses. There was a marked difference between the northern and southern parts of the split field at High Mowthorpe (Oldtype). Overall, earthworm biomass was highly correlated with density (r = 0.91). Analysis of variance (ANOVA) was conducted separately for each of the three sampling periods, on the square roots of earthworm numbers and on log(mass + 1). The results confirmed the predominance of differences between farms, which were highly significant (P < 0.05) in every case except for biomass in Spring 1994, when an increase in variability between fields reduced the significance level to P = 0.08. Only for earthworm numbers in Autumn 1993 was there a significant overall difference between the CFP and RIA treatments (F,,,, = 8.81, P < O.OS), reflecting higher numbers for RIA than CFP at Drayton and High Mowthorpe, although the reverse was true at Gleadthorpe. In Spring 1993 there was a significant interaction between farm and treatment (F2.4 = 10.1, P < 0.05), reflecting the fact that while at Drayton higher numbers occurred for CFP than RIA, the reverse was true at the other two farms. It can be concluded that those differences which related to the treatments were relatively small, and were not consistent between farms or over time. Differences between farms were again the main feature when species and age composition were examined. Mean numbers for each farm are shown in Tables 2 and 3. The populations at Drayton were dominated by juveniles, and by the species A. chlorotica and A. caliginosa, whereas there was a much more even distribution of worms amongst age classes and species at High Mowthorpe. A. rosea
was rare at both sites. A. caliginosa was the only numerous species at Gleadthorpe, where age composition resembled High Mowthorpe rather than Drayton. Principal components analysis (Digby and Kempton, 1987) was used to derive new variables that expressed as much as possible of the variation in the age and species composition (in terms of numbers, not biomass). The first three principal components, referred to as PCl, PC2 and PC3, accounted for over 80% of the variability. Examination of the loadings relating them to the raw data (Table 4) indicates that PC1 represents a weighted function of total numbers, PC2 is a contrast between A. chlorotica vs A. caliginosa and A, longa, and PC3 is a contrast between A. caliginosa and juveniles of A. longa and L. terrestris. The relative contributions of time, field and treatment to the total variability in age and species composition (as expressed by PCl, PC2 and PC3) were assessed by estimating the components of variance (Snedecor and Cochran, 1980), using the REML (restricted maximum likelihood) command in the statistical package Genstat (Genstat 5 Committee, 1990). The results are shown in Table 5. The vast majority of the variation is accounted for by differences between the fields (including differences between farms). The strong season x field interactions for PC2 and PC3 show that the differences between fields change over time. The only significant (P < 0.05) contribution of a term involving the RIA and CFP treatments is the field x treatment term interaction for PC2. Inspection of PC2 shows that this mainly attributable to higher scores (i.e. relatively more A. longa and A. caliginosa, less A. chlorotica) for RIA than CFP in Field One and Bugdale, but lower scores (the reverse trends) for RIA in the northern part of Oldtype field. The treatment effect is thus not consistent between fields, even within the same farm.
Table 3. Mean numbers of earthworms rn-’ by age class, based on data pooled over three sampling periods. Totals differ slightly from Table 2 due to rounding
DISCUSSION
Juvenile Sub-adult Adult
Drayton
High Mowthorpe
Gleadthorpe
532 83 70
41 22 18
9 5 8
Dlferences between CFP and RIA treatments
The results showed that although some differences existed between earthworm populations in RIA and CFP plots they lacked consistency over time and between the pairs of plots, and were of negligible magnitude compared with overall differ-
660
K. A. Tarrant ef al.
Table 4. Loadingsrelating the original worm numbers by age and species (after standardization)to the three largest principal components.Age classes are: A, adult; S, sub-adult;J, juvenile Species L. lerresrris
A. longa
A. chlororica
A. caliginosa
0. cyaneum
A. ro.wa
Unidentified
Age class
PC1
PC2
PC3
A S J A s J A S J A S J A S J A S J A S J
-0.037 -0.094 -0.238 -0.007 -0.053 -0.221 -0.327 -0.327 -0.58 I -0.172 -0.226 -0.490 -0.003 -0.025 -0.078 -0.042 -0.015 -0.012 0.000 -0.010 -0.009 69.2
0.056 0.157 0. I37 0.137 0.256 0.308 -0.319 -0.302 -0.423 0.397 0.341 0.354 -0.012 -0.010 -0.017 -0.025 0.009 0.034 -0.009 -0.01 I -0.013 9.2
-0.032 -0. I88 -0.483 -0.120 -0. I94 -0.577 0.076 0.036 -0.056 0.402 0.238 0.312 -0.014 -0.014 -0.118 0.054 0.007 -0.014 -0.025 -0.012 -0.036 4.4
% Variance
ences between the farms. This was true both for the analyses of overall numbers and biomass and for age and species composition. It can therefore be concluded that, at this stage of the project, the two regimes of pesticide use caused no ecologically significant differences in earthworm populations. It is possible that temporary differences may have arisen earlier in the project, particularly after the application of pesticides which are especially toxic to earthworms (e.g. Aldicarb, Carbendazim). Furthermore, the very substantial differences in earthworm populations between the farms may be partly attributable to differences in husbandry, including pesticide use, prior to the start of SCARAB (see below). Differences between sites
Drayton, with the highest earthworm populations, was more representative of pasture rather than the arable crop standing in Field Five at the time of sampling, perhaps because of the predominance of pasture in previous years. Curry (1976) sampled permanent pastures in Ireland and found earthworm numbers of 200-300 m-‘, and higher densities have been reported elsewhere (Edwards and Lofty, 1977). High earthworm densities in pas-
ture are partly attributable to husbandry factors, including reduced frequency of cultivations, manuring by livestock and lower pesticide inputs compared with other crops. However, the predominant species at Drayton were the non-burrowers, A. chlorotica and A. caIiginosa. These are more often dominant in arable fields as they are more tolerant of repeated cultivations than the species which form more permament burrows. Overall densities and biomass at High Mowthorpe were rather low for arable fields (Edwards and Lofty, 1977). The loamy soil over chalk should be favourable for earthworms, but prolonged low temperatures will inhibit reproduction and freezing conditions will kill immature juvenile stages unable to burrow deep enough to escape temperatures below 0°C. This may account for the lower proportion of juveniles at High Mowthorpe in February, compared with Drayton. Other factors which might affect age composition include several types of pesticide effects: differences between juveniles and adults in exposure and toxicity, and the potential for effects on reproduction and growth rate. The very low numbers of earthworms found at Gleadthorpe are probably attributable to the sandy
Table 5. The percentage contribution of each source to the total variability of each of the principal components for age and species composition (PCI-3). See text and Table 4 for explanation of the principal components. An asterisk indicates that the component is too small to estimate (negative estimate produced). Components not significantly different from zero are given in parentheses Source of variation Season
Field Treat Season x field Season x treatment Field x treatment Season x field x treatment Residual variation
PC1
PC2
(2.9%) 89.4%
12.1% 35.1% * 18.8% 1 9.4% (3.3%) 21.4%
(2.i%) (I.;%) (0.1%) 3.9%
PC3 * 37.0% ??
17.8% (0. I %) 1 i 45.1%
661
Earthworms and Pesticides nature of the soil and the growing of root crops in earlier years. Sandy soil is often unfavourable for earthworms due to low moisture content and low pH. Root crops involve more frequent and deeper cultivations than other crops. Gleadthorpe has a previous history of pesticide use including the fungiand the granular nematicide cide Benomyl, Aldicarb, both of which are highly toxic to earthworms (Edwards and Bohlen, 1992). Furthermore, earthworms have previously been shown to be more affected by pesticides in sandy soils than clay soils (Lofs-Holmin, 1982). Differences between fields within the same farm were much smaller than those between farms. However, two differences were particularly notable. At Gleadthorpe, no worms at all were found in South field. It is difficult to assess whether this might be due to pesticide use, since for many pesticides there are no data on toxicity to earthworms. During SCARAB Aldicarb has been used on Near Kingston and Balk fields, in April 1990, but not on South field. South field is the only one so far used for potatoes during SCARAB (in 1990/91), so it will be interesting to discover whether worm numbers fall in Balk field after harvesting of the potato crop in 1994. At High Mowthorpc, the northern part of Oldtype field contained larger earthworm populations than the southern part. This may be due to the presence in the northern part of large shelter belt and apparently better soil, with less chalk content and a greater depth of topsoil. Further analysis of the contributions of field characteristics, cropping and husbandry (including pesticide use) to the differences in earthworm populations between fields and over time is difficult at this stage of the project, because only one or two types of crops have been grown on each field. As the crop rotations continue over the remainder of the project it should become increasingly easy to separate these effects.
Acknowledgements-This work was funded by the Pesticides Safety Directorate of the U.K. Ministry of Agriculture, Fisheries and Food. We are very grateful to ADAS staff at Drayton, Gleadthorpe and High Mowthorpe for their cooperation, and to J. R. Lofty for advice on earthworm identification. REFERENCES
Barnes B. T. and Ellis F. B. (1979) Effects of different methods of cultivation and direct drilling and disposal of straw residues on populations of earthworms. Journal of Soil Science 30, 669-679. Bowerman P. (1993) Sequels to the Boxworth Project -
studies of environmental, agronomic and economic effects of reduced crop inputs. Journal of the Royal Agriculrural Society, England 154,45-60. Cooke A. S., Greig-Smith P. W. and Jones S. A. (1992)
Consequences for vertebrate wildlife of toxic residues in earthworm prey. In Ecotoxicology of Earthworms. (P. W. Greig-Smith, H. Becker, P. J. Edwards and F. Heimbach, Eds), pp. 159-168. Intercept, Andover. Curry J. P. (1976) Some effects of animal manures on earthworms in grassland. Pedobiologia 16, 425438. Digby P. G. N. and Kempton R. A. (1987) Multivuriare Analysis of Ecological Communities. Chapman and Hall, London. Edwards C. A. and Bohlen P. J. (1992) The effects of toxic chemicals on earthworms. Reviews of Environmental Contamination and Toxicology 125, 2399. Edwards C. A. and Lofty J. R. (1977) Biology of Earthworms, 2nd edn. Chapman and Hall, London. Genstat 5 Committee (1990) Gensrat 5, Release 2, Reference Manual Supplement. Numerical Algorithms Group, Oxford. Greig-Smith P. W. (1992) Risk assessment approaches in the U.K. for the side-effects of pesticides on earthworms. In Ecotoxicology of Earthworms (P. W. GreigSmith, H. Becker, P. J. Edwards and F. Heimbach, Eds), pp. 159-168. Intercept, Andover. Lofs-Hohnin A. (1982) Influence of routine pesticide spraying on earthworms in field experiments with winter wheat. Swedish Journal of Agricultural Research 12, 121-123.
B. M. (1985) Earthworms. Synopsis of the British Fauna, Vol. 31. The Linnean
Sims R. W. and Gerard
Society, London. Snedecor G. W. and Cochran W. G. (1980) Statistical Methods, 7th edn. Iowa State University Press.
Soil Bid. Biochem. Vol. 29, No. 314, pp. 657-661, 1997 Crown Copyright 0 1997 Published by Elsevier ScienceLtd Printed in Great Britain. All rights reserved 0038-0717/97 $17.00 + 0.00 !Soo38-@717(%)00191-5
EFFECTS ON EARTHWORM POPULATIONS OF REDUCING PESTICIDE USE IN ARABLE CROP ROTATIONS K. A. TARRANT,
S. A. FIELD,
S. D. LANGTON
and A. D. M. HART*
Central Science Laboratory, Sand Hutton, York Y04 ILZ, U.K. (Accepted 24 June 1996)
Summary-The SCARAB project is a field-scale, six-year investigation of the effects of pesticide use on invertebrates and soil microflora in arable crop systems common in the U.K. Two pesticide regimes are being compared: current farm practice (CFP) which represents typical levels of use in the study localities, and reduced input approach (RIA) in which inputs have been reduced by 50% and no insecticides used. The treatments began at three farms in 1990, and effects on earthworm populations have been monitored twice yearly since Spring 1993. Particular attention was paid to age and species composition. Results up to Spring 1994 showed that although some differences existed between earthworm populations in RIA and CFP plots they lacked consistency over time and between the pairs of plots, and were of negligible magnitude compared with overall differences between the farms. It was concluded that the two pesticide regimes caused no ecologically significant differences in earthworm populations at this stage of the project. The substantial differences in earthworm populations between farms were largely consistent with the expected effects of differences in climate, soil types, crop types, cultivations and pesticide use, although the relative importance of these factors can not yet be assessed. Crown Copyright 0 1997 Published by Elsevier Science Ltd
INTRODUCTION
The SCARAB project is a field-scale, long-term investigation of the effects of pesticide use on invertebrates and soil microflora in arable cropping systems (Bowennan, 1993). Two pesticide regimes are being compared on three sites in the U.K. under contrasting crop rotations: current farm practice (CFP), which represents typical levels of use by farmers on similar crops near the study sites, and reduced input approach (RIA), which consists of substantially reduced inputs, especially of insecticides. Earthworms are important because of their role in maintaining soil fertility and structure (Edwards and Lofty, 1977). The intensification of modern agriculture and reliance on the use of pesticides presents potential hazards to earthworm populations. Cultivations can cause substantial mortality of earthworms (Barnes and Ellis, 1979), as may some Bohlen, 1992). and pesticides (Edwards Furthermore, in some cases there may be significant hazards to birds and other vertebrates from ingesting earthworms which contain pesticide residues (Cooke et al., 1992). Both types of pesticide hazard are considered in risk assessment of pesticides for regulatory purposes in the U.K. (Greig-Smith, *Author for correspondence.
1992). Effects on earthworms are therefore being investigated as part of the SCARAB project. The primary objective of the earthworm studies is to monitor effects of the SCARAB treatments on earthworm populations by means of twice-yearly sampling. Monitoring began in Spring 1993, in the third year of the CFP and RIA treatments, and will continue until 1996. Changes will be interpreted in relation to the overall contrast between CFP and RIA levels of pesticide use, and in relation to cropping changes and cultivations during the rotation cycles. Further sampling will be carried out to monitor the immediate effects of particular pesticides thought likely to present a particular hazard to earthworms, in order to assist in understanding longer-term changes. This paper outlines the results obtained so far. Particular attention is given to effects on age and species composition, as these have received less attention in previous studies.
MATERIALS
AND METHODS
Study sites and treatments
The two treatments are being compared at three separate experimental farms in England: High Mowthorpe in North Yorkshire, Drayton in Warwickshire and Gleadthorpe in Nottinghamshire. The three farms include a representative range of 657
K. A. Tarrant et (11.
658
conditions in terms of climate, altitude and soil types. The six-year crop rotations at each site are designed to be typical of the surrounding areas. The experiment is based on a split-field design, including two fields each at High Mowthorpe and Drayton, and three at Gleadthorpe. For the purposes of sampling, the northern and southern parts of one field (Oldtype) at High Mowthorpe are treated as separate fields, in effect giving a total of eight fields. Each field is split into two roughly equal halves, one treated with CFP and one with RIA. CFP is based on general practice on the individual site, to represent pesticide use by a technically competent, financially aware farmer in comparable farming situations. RIA is intended to contrast with CFP in its severity on non-target invertebrates. It includes minimal use of fungicides and herbicides, which are applied at half rate or less. No insecticides, nematicides or molluscicides are used on RIA plots unless a severe threat of crop loss is evident. The treatments began in 1990/91 after a one-year baseline period in which CFP and RIA plots in each field received the same treatment. Overall, less than 50% of the pesticides applied to CFP were used on RIA in 1991, 36% in 1992 and 35% in 1993. No insecticides or nematicides were applied to any RIA plots between Autumn 1990 and Spring 1994, whereas those applied to one or more CFP plots included Aldicarb, Chlorpyrifos, Omethoate, Pirimicarb and Triazophos. Pesticides applied on RIA at half the rate used for CFP included Carbendazim and Flusilazole. The mean number of pesticide applications per crop was 4.9 for CFP, and 2.0 for RIA (half rate applications counted as 0.5). Greater reductions in pesticide use were achieved for the combinable crops. In contrast, the options to reduce pesticide applications to the root crops, sugar beet and potatoes, were limited because of the high risk of yield loss and the lack of thresholds to determine potential losses. Table
1. Total earthworm
densities (CFP,
(numbers
m-l)
Population monitoring
The abundance and diversity of earthworms are monitored biannually, in Spring and Autumn when earthworm activity is expected to be the highest. Three samples are collected in each half-field using a 50 x 50 cm quadrat, dropped at random at lo20 m intervals. Preliminary comparison of the formalin and hand-dug methods indicated that a combination of both was required to obtain fully representative samples of earthworms. This involved hand-digging to the plough layer, followed by extraction of additional worms from below the plough layer using 1.14 1 of a 0.2% formalin solution spread evenly in the base of the hole to bring up any deep-burrowing species that might be below the plough layer (Edwards and Lofty, 1977). Any earthworms emerging in the base of the hole were collected for 20 min after the formalin solution was applied. Sampled earthworms were counted and weighed before being returned to the laboratory in 5% formalin solution. Each sample was subsequently sorted according to species and age classes. The earthworms were identified and classified using the taxonomic details listed by Sims and Gerard (1985). The full names of species mentioned in this paper are as follows: Allolobophora chloroticu Aporrectodea caliginosa (Savigny). (Savigny), Aporrectodea rosea (Savigny), Aporrectodea longa (Ude), Lumbricus terrestris (Linn.) and Octolasium cyaneum (Savigny).
RESULTS
The overall densities of earthworms recorded in the first three sampling periods are shown in Table 1. There were very large differences between farms. By comparison, there were only minor differences between fields within farms, and between CFP and RIA areas in the same field. There was a general tendency for both numbers and biomass to
between Spring 1993 and Spring 1994 in relation to crops and pesticide reduced input approach: see text for details)
Farm
Field
Crop 1992193
Crop 1993194
Treatment
Drayton
One
Grass
Grass
Five
Wheat
Grass
Bugdale
RIA CFP RIA CFP RIA CFP RIA CFP RIA CFP RIA CFP RIA CFP RIA CFP
High Mowthorpe
S. barley
S. beans
North
W. barley
W. oilseed
Oldtype South
W. barley
W. oilseed
South
W. barley
Sugar beet
Balk
W. barley
Potatoes
Near Kingston
S. beans
W. wheat
Oldtype
Gleadthorpe
S, Spring-sown
treatments
current farm practice; RIA,
crops; W, winter-sown
crops
Spring 393 516 493 584 24 23 68 36 19 19 0 0 5 5
1993
Autumn
1993
Spring
I994
756 533 173 616 229 233 144 85 36 28
703 1029 853 981 220 161 Ill 59 43 33
0 0
0
12 17 23 28
2,
n 59 77
Earthworms and pesticides
659
Table 2. Mean numbers of earthworms m- 2 by species, based on data pooled over three sampling periods. Each value is the mean of 36 samples (Drayton and Gleadthorpe) or 54 (High Mowthorpe) Species Lumbricus terrestris
Aporrecrodea longa Allolobophora chlorotica Aporrecrodea caliginosa Octolasium cyaneum Aporrectodea rosea
Unidentified
Drayton
High Mowthorpe
Gleadthorpe
35 26 378
13 20 13
0
233
36
1 21
8 3
4 0.4
0 0
I
I
0
1
increase over time, most of the increase occurring between Spring and Autumn 1993. None of the samples collected from South field at Gleadthorpe contained any earthworms at all. Data for South field were therefore excluded from all statistical analyses. There was a marked difference between the northern and southern parts of the split field at High Mowthorpe (Oldtype). Overall, earthworm biomass was highly correlated with density (r = 0.91). Analysis of variance (ANOVA) was conducted separately for each of the three sampling periods, on the square roots of earthworm numbers and on log(mass + 1). The results confirmed the predominance of differences between farms, which were highly significant (P < 0.05) in every case except for biomass in Spring 1994, when an increase in variability between fields reduced the significance level to P = 0.08. Only for earthworm numbers in Autumn 1993 was there a significant overall difference between the CFP and RIA treatments (F,,,, = 8.81, P < O.OS), reflecting higher numbers for RIA than CFP at Drayton and High Mowthorpe, although the reverse was true at Gleadthorpe. In Spring 1993 there was a significant interaction between farm and treatment (F2.4 = 10.1, P < 0.05), reflecting the fact that while at Drayton higher numbers occurred for CFP than RIA, the reverse was true at the other two farms. It can be concluded that those differences which related to the treatments were relatively small, and were not consistent between farms or over time. Differences between farms were again the main feature when species and age composition were examined. Mean numbers for each farm are shown in Tables 2 and 3. The populations at Drayton were dominated by juveniles, and by the species A. chlorotica and A. caliginosa, whereas there was a much more even distribution of worms amongst age classes and species at High Mowthorpe. A. rosea
was rare at both sites. A. caliginosa was the only numerous species at Gleadthorpe, where age composition resembled High Mowthorpe rather than Drayton. Principal components analysis (Digby and Kempton, 1987) was used to derive new variables that expressed as much as possible of the variation in the age and species composition (in terms of numbers, not biomass). The first three principal components, referred to as PCl, PC2 and PC3, accounted for over 80% of the variability. Examination of the loadings relating them to the raw data (Table 4) indicates that PC1 represents a weighted function of total numbers, PC2 is a contrast between A. chlorotica vs A. caliginosa and A, longa, and PC3 is a contrast between A. caliginosa and juveniles of A. longa and L. terrestris. The relative contributions of time, field and treatment to the total variability in age and species composition (as expressed by PCl, PC2 and PC3) were assessed by estimating the components of variance (Snedecor and Cochran, 1980), using the REML (restricted maximum likelihood) command in the statistical package Genstat (Genstat 5 Committee, 1990). The results are shown in Table 5. The vast majority of the variation is accounted for by differences between the fields (including differences between farms). The strong season x field interactions for PC2 and PC3 show that the differences between fields change over time. The only significant (P < 0.05) contribution of a term involving the RIA and CFP treatments is the field x treatment term interaction for PC2. Inspection of PC2 shows that this mainly attributable to higher scores (i.e. relatively more A. longa and A. caliginosa, less A. chlorotica) for RIA than CFP in Field One and Bugdale, but lower scores (the reverse trends) for RIA in the northern part of Oldtype field. The treatment effect is thus not consistent between fields, even within the same farm.
Table 3. Mean numbers of earthworms rn-’ by age class, based on data pooled over three sampling periods. Totals differ slightly from Table 2 due to rounding
DISCUSSION
Juvenile Sub-adult Adult
Drayton
High Mowthorpe
Gleadthorpe
532 83 70
41 22 18
9 5 8
Dlferences between CFP and RIA treatments
The results showed that although some differences existed between earthworm populations in RIA and CFP plots they lacked consistency over time and between the pairs of plots, and were of negligible magnitude compared with overall differ-
660
K. A. Tarrant ef al.
Table 4. Loadingsrelating the original worm numbers by age and species (after standardization)to the three largest principal components.Age classes are: A, adult; S, sub-adult;J, juvenile Species L. lerresrris
A. longa
A. chlororica
A. caliginosa
0. cyaneum
A. ro.wa
Unidentified
Age class
PC1
PC2
PC3
A S J A s J A S J A S J A S J A S J A S J
-0.037 -0.094 -0.238 -0.007 -0.053 -0.221 -0.327 -0.327 -0.58 I -0.172 -0.226 -0.490 -0.003 -0.025 -0.078 -0.042 -0.015 -0.012 0.000 -0.010 -0.009 69.2
0.056 0.157 0. I37 0.137 0.256 0.308 -0.319 -0.302 -0.423 0.397 0.341 0.354 -0.012 -0.010 -0.017 -0.025 0.009 0.034 -0.009 -0.01 I -0.013 9.2
-0.032 -0. I88 -0.483 -0.120 -0. I94 -0.577 0.076 0.036 -0.056 0.402 0.238 0.312 -0.014 -0.014 -0.118 0.054 0.007 -0.014 -0.025 -0.012 -0.036 4.4
% Variance
ences between the farms. This was true both for the analyses of overall numbers and biomass and for age and species composition. It can therefore be concluded that, at this stage of the project, the two regimes of pesticide use caused no ecologically significant differences in earthworm populations. It is possible that temporary differences may have arisen earlier in the project, particularly after the application of pesticides which are especially toxic to earthworms (e.g. Aldicarb, Carbendazim). Furthermore, the very substantial differences in earthworm populations between the farms may be partly attributable to differences in husbandry, including pesticide use, prior to the start of SCARAB (see below). Differences between sites
Drayton, with the highest earthworm populations, was more representative of pasture rather than the arable crop standing in Field Five at the time of sampling, perhaps because of the predominance of pasture in previous years. Curry (1976) sampled permanent pastures in Ireland and found earthworm numbers of 200-300 m-‘, and higher densities have been reported elsewhere (Edwards and Lofty, 1977). High earthworm densities in pas-
ture are partly attributable to husbandry factors, including reduced frequency of cultivations, manuring by livestock and lower pesticide inputs compared with other crops. However, the predominant species at Drayton were the non-burrowers, A. chlorotica and A. caIiginosa. These are more often dominant in arable fields as they are more tolerant of repeated cultivations than the species which form more permament burrows. Overall densities and biomass at High Mowthorpe were rather low for arable fields (Edwards and Lofty, 1977). The loamy soil over chalk should be favourable for earthworms, but prolonged low temperatures will inhibit reproduction and freezing conditions will kill immature juvenile stages unable to burrow deep enough to escape temperatures below 0°C. This may account for the lower proportion of juveniles at High Mowthorpe in February, compared with Drayton. Other factors which might affect age composition include several types of pesticide effects: differences between juveniles and adults in exposure and toxicity, and the potential for effects on reproduction and growth rate. The very low numbers of earthworms found at Gleadthorpe are probably attributable to the sandy
Table 5. The percentage contribution of each source to the total variability of each of the principal components for age and species composition (PCI-3). See text and Table 4 for explanation of the principal components. An asterisk indicates that the component is too small to estimate (negative estimate produced). Components not significantly different from zero are given in parentheses Source of variation Season
Field Treat Season x field Season x treatment Field x treatment Season x field x treatment Residual variation
PC1
PC2
(2.9%) 89.4%
12.1% 35.1% * 18.8% 1 9.4% (3.3%) 21.4%
(2.i%) (I.;%) (0.1%) 3.9%
PC3 * 37.0% ??
17.8% (0. I %) 1 i 45.1%
661
Earthworms and Pesticides nature of the soil and the growing of root crops in earlier years. Sandy soil is often unfavourable for earthworms due to low moisture content and low pH. Root crops involve more frequent and deeper cultivations than other crops. Gleadthorpe has a previous history of pesticide use including the fungiand the granular nematicide cide Benomyl, Aldicarb, both of which are highly toxic to earthworms (Edwards and Bohlen, 1992). Furthermore, earthworms have previously been shown to be more affected by pesticides in sandy soils than clay soils (Lofs-Holmin, 1982). Differences between fields within the same farm were much smaller than those between farms. However, two differences were particularly notable. At Gleadthorpe, no worms at all were found in South field. It is difficult to assess whether this might be due to pesticide use, since for many pesticides there are no data on toxicity to earthworms. During SCARAB Aldicarb has been used on Near Kingston and Balk fields, in April 1990, but not on South field. South field is the only one so far used for potatoes during SCARAB (in 1990/91), so it will be interesting to discover whether worm numbers fall in Balk field after harvesting of the potato crop in 1994. At High Mowthorpc, the northern part of Oldtype field contained larger earthworm populations than the southern part. This may be due to the presence in the northern part of large shelter belt and apparently better soil, with less chalk content and a greater depth of topsoil. Further analysis of the contributions of field characteristics, cropping and husbandry (including pesticide use) to the differences in earthworm populations between fields and over time is difficult at this stage of the project, because only one or two types of crops have been grown on each field. As the crop rotations continue over the remainder of the project it should become increasingly easy to separate these effects.
Acknowledgements-This work was funded by the Pesticides Safety Directorate of the U.K. Ministry of Agriculture, Fisheries and Food. We are very grateful to ADAS staff at Drayton, Gleadthorpe and High Mowthorpe for their cooperation, and to J. R. Lofty for advice on earthworm identification. REFERENCES
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Society, London. Snedecor G. W. and Cochran W. G. (1980) Statistical Methods, 7th edn. Iowa State University Press.