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Earthworm populations in two low-input cereal farming systems
applied soil ecology 37 (2007) 184–191
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Earthworm populations in two low-input cereal farming systems Lukas Pfiffner *, Henryk Luka Research Institute of Organic Agriculture (FiBL), Ackerstrasse, CH-5070 Frick, Switzerland
article info
abstract
Article history:
Earthworm populations in low-input integrated crop management (ICM: no application of
Received 24 May 2006
insecticides, fungicides and growth regulators) and organic farming systems were com-
Received in revised form
pared. The study was performed as a 3-year field survey using a paired-farm approach in six
15 June 2007
different locations in northwestern Switzerland. Earthworms were extracted from soils
Accepted 18 June 2007
sampled from 24 winter cereal fields using a combined method of extraction by mustard flour solution and handsorting. Earthworm communities differed between these farming systems. Over all sites, the
Keywords:
mean biomass, abundance and species richness of earthworms found in the low-input ICM
Integrated crop management
fields were significantly lower than in the organic fields. Adult earthworms in organic fields
Organic agriculture
were 114% more abundant than in ICM fields, but the frequencies of most species within the
Sustainable agriculture
respective systems were similar in both farming systems. The numbers of earthworm
Earthworms
species and juveniles were higher in organic fields. Five species – Lumbricus terrestris (L.),
Agri-environmental programme
Nicodrilus longus (Ude), Nicodrilus nocturnus (Evans), Nicodrilus caliginosus (Sav.) and Allolobo-
Soil management
phora rosea (Sav.) – were significantly more numerous in the organic fields than in the ICM fields. Multivariate analysis showed that the farming system explained most of the variance and was found to be the key factor in altering the earthworm fauna. Late ploughing in autumn was found to have a major negative effect on earthworm abundance, irrespective of the farming system. Farming practices that differ between these farming systems and may considerably influence earthworm populations and diversity are discussed. # 2007 Elsevier B.V. All rights reserved.
1.
Introduction
With the intensification of arable land use over the last four decades, deterioration of soil fertility and increases in soil pollution have emerged as major issues. Maintenance of soil and water quality is fundamental for future agricultural production (Scialabba and Hattam, 2002). Therefore, there is a requirement for sustainable farming systems which exploit the natural biotic mechanisms that maintain soil structure, fertility and drainage, and help to regulate and control pests, diseases and weeds.
Nowadays, sustainable and low-input farming systems are of increasing public interest. Agri-environmental schemes in Europe aim to support ecological functions and biodiversity in agroecosystems. This is related to both farming practices and site conditions. Organic farming is a system in which many ecological requirements have been fulfilled (EU regulations 2092/91/EEC), which has been assessed to be environmentally benign, and in which various abiotic as well as biotic benefits have been found (Stolze et al., 2000; Maeder et al., 2002; Hole et al., 2005). As a consequence, all EU-countries promote organic farming through agri-political measures (Lampkin et al., 1999).
* Corresponding author. Tel.: +41 62 865 72 72; fax: +41 62 865 72 73. E-mail address: [email protected] (L. Pfiffner). 0929-1393/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.apsoil.2007.06.005
applied soil ecology 37 (2007) 184–191
The role of earthworms in enhancing soil fertility is well known, and different farming practices have considerable effects on both earthworm abundance and species composition (e.g., Lee, 1985; Edwards and Bohlen, 1996). Earthworms contribute to physical, chemical and biological soil processes such as soil structure formation, e.g., formation of stable aggregates (Schrader and Zhang, 1997), and organic matter dynamics through nutrient cycling, decomposition of residues (Wolters and Ekschmitt, 1995), and soil pore water dynamics through their burrowing activities, which provide soil pores for aeration and water infiltration (Edwards et al., 1990; Pitka¨nen and Nuutinen, 1997). Consequently, the productivity of arable farming systems can be improved by the presence of abundant earthworm populations. Positive effects of specific farm practices on earthworms such as direct drilled and minimal cultivation of cereals have been found (Edwards and Lofty, 1982a; Maillard and Cuendet, 1997). These are practices which are not always compatible with organic production due to the ban on herbicides. The analysis of whole farm systems in numerous comparative investigations has shown that under organic farming regimes, with lower inputs of off-farm materials, higher abundance and biomass of earthworms are found in most cases compared with high-input conventional arable crops (e.g., Bauchhenss, 1991; Pfiffner, 1993; Pfiffner and Maeder, 1997; Scullion et al., 2002). A few studies performed on perennial crops such as orchards revealed similar results (Paoletti et al., 1995). Moreover, in a 10-year study by Hutcheon et al. (2001), earthworm species were found to differ in their response to conventional and integrated farming systems. Only few on-farm studies include specific information on the influence of agricultural practices on species diversity and earthworm community structure. Most investigations addressed high-input conventional and organic farming systems (for review, see Hole et al., 2005). Furthermore, there is a lack of data from on-farm studies comparing low-input integrated and organic arable farming systems, which are currently promoted by agri-environmental programmes. In the present study, we focus on the effects of these two lowinput farming systems on the earthworm fauna using a paired-farm approach at six different locations in northwestern Switzerland. Corresponding results for carabid and spider fauna using this trial design and comparing the same fields have already been published (Pfiffner and Luka, 2003). The key questions of this on-farm survey were, (1) are there any differences between the earthworm fauna of integrated and organically managed arable fields, and (2) what are the driving forces altering the earthworm populations in these two low-input farming systems?
2.
Materials and methods
2.1.
Study area
A 3-year field study using a paired-farm approach at six different locations in northwestern Switzerland was conducted (Table 1). Low-input ICM farming (ICM: Integrated Cropping Management) within the Swiss ‘extensive cereal production’ agri-environmental programme (Bundesrat, 1998)
185
and organic or bio-dynamic farming were taken to be lowinput farming systems. The present analysis will focus on the data collected from 24 differently managed cereal fields. During the investigation period of 1996–1998, two locations were studied per year. All farms were controlled and certified as ICM or organic farms and worked according to their official standards within the label programme of IP Suisse or Bio Suisse. This means that the whole farm was managed according to these standards. Only farms with a sufficiently long transition period and very similar soil conditions were selected for comparison. It was considered that the transition period should be at least 5 years depending on regime history and farming intensity. Moreover, the selection of typical farms within a given region was made in consultation with the official advisory services, providing a set of representative farms using common fertilizer and soil tillage management. The low-input ICM farming system at the study sites applies no insecticides, fungicides or growth regulators to the cereal crops, although herbicides are permitted and were used. No pesticides and only organic fertilizers were applied to the organic and bio-dynamic fields. Crop rotations were similar in both systems. Sampling was carried out in winter cereal fields (mostly winter wheat), cultivated in a 7–9 year crop rotation, including at least one grass-clover crop. Field size ranged from 0.8 to 1.5 ha. Soil, relief conditions and exposition were similar in each location. Details on site characteristics and agricultural practices are shown in Table 1. Hereafter, the term ‘organic’ field includes bio-dynamic farming. Twenty-four winter cereal fields on 12 farms were investigated. The paired fields were adjacent or at least neighbouring plots. Two fields per farm were sampled in order to obtain more information and statistical power on the general situation within each farm. Soils were analysed for the following parameters: organic carbon, pH, calcium, phosphate, potassium, magnesium and iron. Biotic parameters such as crop density were recorded at growth stage Z 30/31 (Zadoks et al., 1974) once during the growing season, using 10 samples of 0.5 m 0.5 m. Total weed cover was assessed in five quadrants (2 m 2 m) about 7 weeks before harvest.
2.2.
Sampling methods
Earthworm populations were investigated using a two-step method from 1996 to 1998 after the winter cereal crop harvest. Six samples were taken once per field in the autumn after the cereal harvest (1 and 3 October 1996 at locations 1 and 2; 21 and 22 October 1997 at locations 3 and 4; and 21 and 22 October 1998 at locations 5 and 6), extracted with a 0.33% mustard flour solution and then sorted by hand (Ho¨gger, 1993; Emmerling, 1995). For the extraction, 15 l of mustard solution was used over a sampling time of 40 min. The sampling unit that was hand-sorted was 50 cm 50 cm wide and 15 cm deep, and samples were separated by a distance of at least 15 m. With this well-established sampling method, anecic species (mustard extraction) as well as early diapausing and endogeic earthworms (handsorting) were efficiently recorded. The specimens collected were preserved in 4% formalin solution. Biomass loss during preservation was adjusted according to Cuendet (1995). Individual earthworms were identified as
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Table 1 – Site characteristics of low-input integrated (ICM) and organic arable fields and agricultural practices in winter cereal fields within each farm Site characteristics Region Location/paired farms m a.s.l. Soil type
Soil analysisa Organic C (%) pH (0.1 KCl) Calcium (HCl/H2SO4)b P (sodium acetate)b Potassium (sodium acetate)b Cereal standsa (plants per m2) Weed cover (%)a Weed speciesa
351 330 Luvisol from Loess, medium silty-loam
b c d e
Tabular jura (Meso-European Foreland) 3 4
Pleistocene terraces 5
6
520 Calcic Cambisol, medium clay-loam ICM Bio-dyn. 2 2 >5 13
331 Cambisol from Loess, medium clay-loam ICM Organic 2 2 >5 17
356 Luvisol, medium clay-loam (6.1) and sandy-loam (6.2) ICM Organic 2 2 >10 5
ICM 2 >10
Organic 2 51
ICM 2 >10
Organic 2 17
499 Eutric Cambisol, medium clay-loam ICM Bio-dyn. 2 2 >10 19
3.2 6.5 6535
2.7 5.5 1855
2.5 6.0 2760
2.8 6.5 4615
4.6 6.3 3485
3.7 6.0 2515
4.7 7.2 6680
5.6 6.9 5595
3.1 6.0 2730
2.7 6.1 5420
3.0 5.1 830
3.7 6.1 1245
24
19
68
43
35
6
48
29
34
11
44
77
135
155
245
170
145
100
165
95
115
75
155
205
925
706
877
626
1003
809
964
756
942
508
880
699
6 5
21.5 14
0 0
14 8
6 5.5
11.5 13
5 8.5
12.5 18
0 0
10.5 13
4 2.5
15.5 10.5
OF 0.25 t, 0.3 t PS
FYM 20 m3, 0.27 t AN
FYM 33 m 3
65 m3 slurry, 0.1 t AN
30 m3 slurry
0.35 t AN
30 m3 slurry, 8 m3 compost
0.17 t AN
Compost 10 m 3
0.29 t AN
Compost 15 m3, 30 m3 slurry
Agricultural practices and yields Fertilizer to cereal cropc 90 m3 slurry, 0.07 t AN
a
2
Weed control Mechanical Chemicald
Yes 1
Yes –
No 2
Yes –
Yes 1
Yes –
No 2
No –
No 2
Yes –
No 2
Yes –
Cereal yielde
Medium
Medium
Medium
Low
Medium
Low
Medium
Medium
High
Medium
High
Low
Mean value for two fields per farm. mg/kg. Amount per ha. AN: ammonium nitrate, FYM: farmyard manure; PS: potassium sulphate, OF: organic poly-nutrient fertilizer. Number of applications. Yields: high 7–9 t/ha; medium 5–7 t/ha; low <5 t/ha.
applied soil ecology 37 (2007) 184–191
Farming method Number of fields Conversion time (years)
Loess covered hilly region 1
applied soil ecology 37 (2007) 184–191
187
adult (clitellate), sub-adult (large, but non-clitellate) or juvenile (non-clitellate). Species identification was performed according to the classification of Bouche´ (1972) and Cuendet (1990). For the purposes of presenting population data, earthworm species found on individual farms were grouped into the three ecological categories defined by Bouche´ (1977). The main principle in the ecological classification of earthworms is based on their behaviour, morpho-physiological features and key habitat.
2.3.
Statistical analysis
A two-way ANOVA was performed on the field level to test the effects of location and farming system on abundance, biomass and number of species (SPSS 10). Before analysis, each data set was tested for departure from normality using the Shapiro Wilk test. All analyses of data on abundances and biomass were performed on cube root transformed data (Boag et al., 1994). The mean values of number of juveniles and abundance of most abundant species were examined over all fields using the non-parametric Wilcoxon/Kruskal–Wallis test (Chi square approximation). To assess the potential impact of different soil tillage regimes on earthworms, differences in earthworm densities between fields at each location were analysed using the Multiple Tukey–Kramer HSD test ( p < 0.05). The influence of various environmental and management variables on the earthworm communities was studied using an ordination method, redundancy analysis (RDA), performed with the CANOCO program, version 4.5 (Ter Braak and Smilauer, 2002). This linear method performs a direct gradient analysis and is useful if gradients are short, as was the case in this investigation (Palmer, 2003). For this purpose, the data were pooled and rare species (frequency < 0.25) were omitted to minimize random effects and sampling errors. The farming systems were applied as two dummy-variables. All RDAs were run using untransformed data. Soil properties such as organic carbon, pH, calcium, phosphate, potassium, magnesium, iron, weed cover and cereal stand density were selected as quantitative environmental variables. Applying RDA in combination with forward selection, the significance of the single main variable was analysed by Monte Carlo with 499 permutations through testing of the axis associated with this variable, using the axis eigenvalue as the test statistic (Ter Braak, 1996).
3.
Results
Over all sites, the farming system significantly affected altered biomass (F-value = 23.83), abundance (F-value = 32.8) and species richness (F-value = 21.73), and no effect of location was found (two-way ANOVA with p < 0.001). The mean biomass and abundance of earthworms found in ICM fields were significantly lower than in the organic fields (Fig. 1a and b). During the 3-year investigation period, 12 earthworm species were found in the arable winter cereal fields, comprising 7 endogeic, 3 anecic and 2 epigeic species (Table 2). Seven endogeic, three anecic and two epigeic species occurred in the winter cereal plots. Over all sites, adult
Fig. 1 – Overall mean biomass W S.E.M. (a) and number of earthworms W S.E.M. (b) in low-input ICM cereal fields (white bars) and organic cereal fields (black bars). Twoway ANOVA: ***p < 0.001.
earthworms in organic fields were 114% more abundant than in ICM fields, but the frequencies for most species within the specific system were similar in both farming systems (Table 2). There were some exceptions with differences of more than 10% in frequency: Nicodrilus longus (Ude) and Nicodrilus nocturnus (Evans) occurred more frequently in the organic and Lumbricus rubellus (Sav.) more often in the ICM system (Table 2). The total number of species found per field was higher in the organic fields in 9 out of 12 cases and ranged from 4 to 8 species in the ICM and 5–9 species in the organic fields. The mean number of earthworm species and the number of juveniles found in all fields was significantly lower in ICM fields than in the organic fields (Table 3). Among the abundant species, numbers of anecic, vertically burrowing species such as Lumbricus terrestris (L.), N. longus and N. nocturnus as well as endogeic species such as Nicodrilus caliginosus (Sav.), Allolobophora rosea (Sav.) were significantly higher in the organic fields than in the low-input ICM fields. Allolobophora chlorotica (Sav.) was only found in four locations (1, 2, 3 and 4), and its numbers did not differ in ICM fields and organic fields. Redundancy analysis of earthworm communities as related to the analysed environmental factors revealed only farming system, density of cereal stands and potassium as significant factors. Farming system explained most of the variance at 40%, wheat density explained 15% and soil potassium 4%. Wheat density is a factor that is directly dependent on farming intensity, particularly on fertilizer input. Differences of earthworms within the same farm were also found on the level of location, which may be a consequence of
188
applied soil ecology 37 (2007) 184–191
Table 2 – Occurrence of adult earthworms in low-input ICM and organic cereal fields and their frequency per farming system, sorted according to ecological categories Typea
Species
Low-input farming system ICM
Lumbricus terrestris (Linnaeus, 1758) Nicodrilus longus (Ude, 1885) Nicodrilus nocturnus (Evans, 1946) Allolobophora chlorotica (Savigny, 1826) Allolobophora handlirschi (Rosa, 1897) Allolobophora icterica (Savigny, 1826) Allolobophora rosea (Savigny, 1826) Nicodrilus caliginosus (Savigny, 1826) Octolasion cyaneum (Savigny, 1826) Octolasion tyrtaeum lacteum (Oerley, 1885) Lumbricus castaneus (Savigny, 1826) Lumbricus rubellus (Hoffmeister, 1843)
Anecic Anecic Anecic Endogeic Endogeic Endogeic Endogeic Endogeic Endogeic Endogeic Epigeic Epigeic
Total adult individuals
Organic
Ab
F
Ab
F
43 103 45 72 7 72 122 88 8 11 6 24
0.92 0.83 0.75 0.58 0.42 0.33 0.92 0.83 0.42 0.17 0.25 0.42
192 240 108 86 17 118 207 273 16 17 7 4
0.92 1.00 0.92 0.67 0.33 0.33 1.00 0.92 0.42 0.17 0.25 0.25
601
1285
Ab: abundance (total number of earthworms in all samples); F: frequency per farming system. Ecological category.
a
different soil tillage regimes. Variation in earthworm densities between two fields at the same location and subject to the same farming system (Fig. 2) can partly be attributed to the use of the plough. When compared with reduced tillage using a grubber or harrow, ploughing consistently decreased earthworm densities. After late ploughing in autumn, earthworm densities were always significantly lower than with no ploughing or early ploughing in July or August. This can be
Table 3 – Analysis of number of earthworm species, juveniles and density of the most abundant species in low-input integrated (ICM) and organic (Org) farming system (Wilcoxon/Kruskal–Wallis test) System
SM
ChiSq
p
Number of species
ICM Org
58.32 86.68
17.24
***
Juveniles
ICM Org
61.47 83.53
10.10
**
ICM Org
60.56 84.44
14.06
***
Nicodrilus longus
ICM Org
56.12 88.88
23.28
***
Nicodrilus nocturnus
ICM Org
62.17 82.83
10.93
**
ICM Org
59.11 85.89
16.33
***
ICM Org
63.01 81.99
7.76
ICM Org
75.54 69.46
1.01
Anecic species Lumbricus terrestris
Endogeic species Nicodrilus caliginosus
Allolobophora rosea
Allolobophora chlorotica
SM: score mean; ChiSq: Chi square; n.s.: not significant. p < 0.01. *** p < 0.001. **
explained by earthworm biology: in the dry season, they prefer deeper soil layers with higher humidity, and are thus less severely affected by the plough and the accompanied tillage treatments.
4.
Discussion
4.1.
Earthworm biomass and abundance
The abundance, biomass and diversity of earthworm populations in agricultural soils is related to abiotic factors such as soil condition (e.g., soil structure, soil texture, temperature and humidity) and altitude, as well as agricultural practices
**
n.s.
Fig. 2 – Mean number of earthworms W S.E.M. in low-input integrated (ICM) and organic cereal field (org) in respect of soil tillage, indicated as follows: no plough use (white bar), early plough use (grey bar) and late plough use in autumn (black bar). Tukey HSD test performed separately for each location. Means with different letters are significantly different at p < 0.05.
applied soil ecology 37 (2007) 184–191
such as soil tillage, cropping systems and the use of fertilizers and pesticides (Lee, 1985; Edwards and Bohlen, 1996). In this study, the biomass and abundance of earthworms differed significantly between the two low-input farming systems but also in some cases within the farm. This indicates that the whole farming system, as well as specific practices differing at the farm level, may influence earthworms in a significant way. In many cases, earthworm communities in organic fields were significantly larger in abundance and biomass, and richer in number of species than in the low-input integrated farmed fields. These results are similar to those from comparative studies of conventional and organic farming systems (Bauchhenss, 1991; Scullion et al., 2002). However, in many cases earthworm biomass and abundance in both farming systems were relatively high for arable soils—Swiss arable soils cultivated using traditional, so-called ‘good agricultural practice’ (GAP), generally exhibit ranges of 60– 100 g/m2 and 80–120 specimens/m2. On a few sites, biomass and abundance were even higher than in nearby perennial, non-tilled grassland strips, mostly in organic fields. This indicates careful soil management at these sites that may increase numbers of earthworms through specific practices. Earthworm populations are usually significantly depressed in arable fields relative to grassland or undisturbed land (Didden, 2001). Multivariate analysis showed that the farming system, winter cereal density and one soil parameter (potassium) were significant factors influencing the earthworm populations. Winter cereal density correlated negatively and potassium soil content positively with earthworms. The farming system, explained 40% of the variance, and was thus shown to be a strong driving factor. The poor correlations of earthworm fauna with most chemical soil parameters indicate that the different agricultural practices may have much greater impacts on earthworms than the soil properties that varied within a small range between the different sites at each location. Therefore, agricultural practices which differed between the farming systems such as soil tillage, fertilizer management and plant protection management (history) were assumed to have altered the earthworm fauna in a significant way. Intensive soil tillage on arable land can eliminate earthworm populations within a single season (Curry et al., 2002). The extent of population reduction depends on the nature and frequency of cultivation and initial population levels, which in turn depend on the management history (Chan, 2001). The use of the plough in the fields investigated, particularly late ploughing in autumn when earthworm activity is high, clearly had a major negative impact on earthworm abundance, irrespective of farming system, and may therefore explain differences found within the farming system. Significant differences within the same farming system at one location can be attributed mainly to this key factor (locations 1, 2, 4 and 6). Ploughing has adverse effects on population density and diversity due to the mechanical disturbance that can lead to unstable microclimatic conditions and abrasive effects in the soil profile, as well as the removal of protective surface residues. The direct mortality arising from injury caused by ploughing was estimated at about 25% in a range of soils in Switzerland (Cuendet, 1983) or up to 60–70% using rotary cultivation, as reported from
189
Sweden (Bostro¨m, 1988). In this investigation, which considers the same farming system using different methods of soil tillage, the reduction rate in numbers of earthworms by ploughing seems to be rather higher than 50% in some cases. In general, the fertilizer management of the organic fields may be more favourable due to a regular input of different organic materials (farmyard manure, slurry or compost) than the ICM that is mainly based on mineral fertilizers. As decomposers, earthworms need a constant supply of organic materials of various types, depending on the species (Piearce, 1978). The negative effect of mineral fertilizers may depend on the nature the fertilizer (Edwards and Lofty, 1982b). In the long-term trial conducted at Rothamsted, it was observed that the amount of N applied per hectare of organic matter N was more effective in raising earthworm populations than inorganic N; inorganic fertilizers led to significant lower abundance of L. terrestris and N. caliginosus. Similarly, in the present study, these two species were significantly more abundant in the organically fertilized than in the mineral or mixed fertilized ICM fields. This may be partly attributed to the specific fertilizer management. Pfiffner (1993) found negative effects of long-term pure mineral fertilization on earthworms (abundance, biomass and juvenile earthworms) compared with mixed mineral–organic nutrient management of conventionally managed arable fields. A 14-year study by Estevez et al. (1996) has shown that solid cattle manure improved earthworm populations and diversity compared to mineral fertilizer treatment and the control without fertilizer. However, depending on the type and the amount of fertilizer used, fertilizer management alters earthworm populations in a significant way. The fertilizer management on these organic farms was assumed to be more favourable for earthworms in terms of quantity, quality and continuity of food supply. A further aspect concerns plant protection measures differing between these two farming systems. It is well known that pesticides, particularly insecticides, nematicides, certain fungicides (e.g., benomyl), and herbicides (e.g., dinoseb), reduce earthworm populations. There is a considerable body of literature documenting the sublethal and lethal effects of pesticides and other chemicals on earthworms (e.g., Edwards and Bohlen, 1992, 1996; Greigh-Smith et al., 1992). In the present trial, no harmful pesticides were applied to the winter cereal crops in either farming system during the investigation period—only herbicides were used in the ICM fields. Herbicides tend to have low toxicity for earthworms, but can cause population reduction by decreasing sources of organic matter on which earthworms feed. However, non-target effects of insecticides or fungicides applied to the pre-crops of ICM farms are unclear, but not unlikely.
4.2.
Effects on earthworm species
In general, 12 common arable earthworm species were found in the 24 arable fields, which shows a relatively high species diversity, with 6 species occurred consistently or fairly frequently. In their investigation of 19 sites in Bavaria, Germany, Bauchhenss and Herr (1986) found much lower values, with 1–6 species in conventional arable fields.
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applied soil ecology 37 (2007) 184–191
There was evidence that individual earthworm species differed in their response to the different farming systems. The numbers of earthworm species and juveniles were mostly significantly lower in ICM fields. Deep burrowing, anecic species such as L. terrestris, N. longus and N. nocturnus, as well as endogeic species such as N. caliginosus, A. rosea and A. icterica were generally more prevalent in the organic fields than in the low-input ICM fields. This confirms findings in a long-term field trial comparing conventional and organic arable fields, where higher biomass and abundance of anecic earthworms was found in the organic plots (Pfiffner, 1993). High densities of anecic species can alter soil properties. They are particularly effective in the creation of stable, vertical, macroporous channels which can modify aeration and patterns of water infiltration (Joschko et al., 1989; Edwards et al., 1990). Lower number of species, less juvenile earthworms and lower abundance of certain species found in the ICM fields reveal different communities of earthworms in these two farming systems. However, the relative frequencies of most species within the respective systems were similar in both farming systems, which indicate that a species potential still exists in these ICM-fields.
5.
Conclusions
A comparison of two low-input farming systems revealed higher biomass, density, number of juveniles and adults and differences in species occurrence of earthworms in organic cereal fields. This demonstrates differences in community structure between the two farming systems and indicates that organic farming can benefit earthworm populations on a broader range than ICM low-input farming. Agricultural practices such as soil tillage, fertilizer management and plant protection are assumed to be the factors that exert the greatest influence on earthworm populations. A careful choice of earthworm-enhancing or harmless farming practices across the whole crop rotation is necessary to conserve earthworms in a sustainable way. For example, we observed that a single factor, e.g., ploughing in late autumn, can drastically reduce the earthworm fauna, irrespective of the farming system. Differences such as higher abundance of deep burrowing species and species diversity in organic fields found in populations may have implications for soil fertility and wider ecosystem functions—this warrants further investigation.
Acknowledgements We would like to thank D. Zwygart, R. Mu¨hlethaler for field assistance and the farmers for their cooperation on their land, and also P. Maeder, A. Lang and G. Cuendet (taxonomic support), and the two anonymous referees for useful comments and suggestions on an earlier draft of the manuscript. We thank the canton Baselland, Ministry for Environment, Pro Natura Switzerland, Foundation E. Guggenheim-Schnurr and Arbeitsgemeinschaft fu¨r Natur- and Heimatschutz for their financial support.
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available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/apsoil
Earthworm populations in two low-input cereal farming systems Lukas Pfiffner *, Henryk Luka Research Institute of Organic Agriculture (FiBL), Ackerstrasse, CH-5070 Frick, Switzerland
article info
abstract
Article history:
Earthworm populations in low-input integrated crop management (ICM: no application of
Received 24 May 2006
insecticides, fungicides and growth regulators) and organic farming systems were com-
Received in revised form
pared. The study was performed as a 3-year field survey using a paired-farm approach in six
15 June 2007
different locations in northwestern Switzerland. Earthworms were extracted from soils
Accepted 18 June 2007
sampled from 24 winter cereal fields using a combined method of extraction by mustard flour solution and handsorting. Earthworm communities differed between these farming systems. Over all sites, the
Keywords:
mean biomass, abundance and species richness of earthworms found in the low-input ICM
Integrated crop management
fields were significantly lower than in the organic fields. Adult earthworms in organic fields
Organic agriculture
were 114% more abundant than in ICM fields, but the frequencies of most species within the
Sustainable agriculture
respective systems were similar in both farming systems. The numbers of earthworm
Earthworms
species and juveniles were higher in organic fields. Five species – Lumbricus terrestris (L.),
Agri-environmental programme
Nicodrilus longus (Ude), Nicodrilus nocturnus (Evans), Nicodrilus caliginosus (Sav.) and Allolobo-
Soil management
phora rosea (Sav.) – were significantly more numerous in the organic fields than in the ICM fields. Multivariate analysis showed that the farming system explained most of the variance and was found to be the key factor in altering the earthworm fauna. Late ploughing in autumn was found to have a major negative effect on earthworm abundance, irrespective of the farming system. Farming practices that differ between these farming systems and may considerably influence earthworm populations and diversity are discussed. # 2007 Elsevier B.V. All rights reserved.
1.
Introduction
With the intensification of arable land use over the last four decades, deterioration of soil fertility and increases in soil pollution have emerged as major issues. Maintenance of soil and water quality is fundamental for future agricultural production (Scialabba and Hattam, 2002). Therefore, there is a requirement for sustainable farming systems which exploit the natural biotic mechanisms that maintain soil structure, fertility and drainage, and help to regulate and control pests, diseases and weeds.
Nowadays, sustainable and low-input farming systems are of increasing public interest. Agri-environmental schemes in Europe aim to support ecological functions and biodiversity in agroecosystems. This is related to both farming practices and site conditions. Organic farming is a system in which many ecological requirements have been fulfilled (EU regulations 2092/91/EEC), which has been assessed to be environmentally benign, and in which various abiotic as well as biotic benefits have been found (Stolze et al., 2000; Maeder et al., 2002; Hole et al., 2005). As a consequence, all EU-countries promote organic farming through agri-political measures (Lampkin et al., 1999).
* Corresponding author. Tel.: +41 62 865 72 72; fax: +41 62 865 72 73. E-mail address: [email protected] (L. Pfiffner). 0929-1393/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.apsoil.2007.06.005
applied soil ecology 37 (2007) 184–191
The role of earthworms in enhancing soil fertility is well known, and different farming practices have considerable effects on both earthworm abundance and species composition (e.g., Lee, 1985; Edwards and Bohlen, 1996). Earthworms contribute to physical, chemical and biological soil processes such as soil structure formation, e.g., formation of stable aggregates (Schrader and Zhang, 1997), and organic matter dynamics through nutrient cycling, decomposition of residues (Wolters and Ekschmitt, 1995), and soil pore water dynamics through their burrowing activities, which provide soil pores for aeration and water infiltration (Edwards et al., 1990; Pitka¨nen and Nuutinen, 1997). Consequently, the productivity of arable farming systems can be improved by the presence of abundant earthworm populations. Positive effects of specific farm practices on earthworms such as direct drilled and minimal cultivation of cereals have been found (Edwards and Lofty, 1982a; Maillard and Cuendet, 1997). These are practices which are not always compatible with organic production due to the ban on herbicides. The analysis of whole farm systems in numerous comparative investigations has shown that under organic farming regimes, with lower inputs of off-farm materials, higher abundance and biomass of earthworms are found in most cases compared with high-input conventional arable crops (e.g., Bauchhenss, 1991; Pfiffner, 1993; Pfiffner and Maeder, 1997; Scullion et al., 2002). A few studies performed on perennial crops such as orchards revealed similar results (Paoletti et al., 1995). Moreover, in a 10-year study by Hutcheon et al. (2001), earthworm species were found to differ in their response to conventional and integrated farming systems. Only few on-farm studies include specific information on the influence of agricultural practices on species diversity and earthworm community structure. Most investigations addressed high-input conventional and organic farming systems (for review, see Hole et al., 2005). Furthermore, there is a lack of data from on-farm studies comparing low-input integrated and organic arable farming systems, which are currently promoted by agri-environmental programmes. In the present study, we focus on the effects of these two lowinput farming systems on the earthworm fauna using a paired-farm approach at six different locations in northwestern Switzerland. Corresponding results for carabid and spider fauna using this trial design and comparing the same fields have already been published (Pfiffner and Luka, 2003). The key questions of this on-farm survey were, (1) are there any differences between the earthworm fauna of integrated and organically managed arable fields, and (2) what are the driving forces altering the earthworm populations in these two low-input farming systems?
2.
Materials and methods
2.1.
Study area
A 3-year field study using a paired-farm approach at six different locations in northwestern Switzerland was conducted (Table 1). Low-input ICM farming (ICM: Integrated Cropping Management) within the Swiss ‘extensive cereal production’ agri-environmental programme (Bundesrat, 1998)
185
and organic or bio-dynamic farming were taken to be lowinput farming systems. The present analysis will focus on the data collected from 24 differently managed cereal fields. During the investigation period of 1996–1998, two locations were studied per year. All farms were controlled and certified as ICM or organic farms and worked according to their official standards within the label programme of IP Suisse or Bio Suisse. This means that the whole farm was managed according to these standards. Only farms with a sufficiently long transition period and very similar soil conditions were selected for comparison. It was considered that the transition period should be at least 5 years depending on regime history and farming intensity. Moreover, the selection of typical farms within a given region was made in consultation with the official advisory services, providing a set of representative farms using common fertilizer and soil tillage management. The low-input ICM farming system at the study sites applies no insecticides, fungicides or growth regulators to the cereal crops, although herbicides are permitted and were used. No pesticides and only organic fertilizers were applied to the organic and bio-dynamic fields. Crop rotations were similar in both systems. Sampling was carried out in winter cereal fields (mostly winter wheat), cultivated in a 7–9 year crop rotation, including at least one grass-clover crop. Field size ranged from 0.8 to 1.5 ha. Soil, relief conditions and exposition were similar in each location. Details on site characteristics and agricultural practices are shown in Table 1. Hereafter, the term ‘organic’ field includes bio-dynamic farming. Twenty-four winter cereal fields on 12 farms were investigated. The paired fields were adjacent or at least neighbouring plots. Two fields per farm were sampled in order to obtain more information and statistical power on the general situation within each farm. Soils were analysed for the following parameters: organic carbon, pH, calcium, phosphate, potassium, magnesium and iron. Biotic parameters such as crop density were recorded at growth stage Z 30/31 (Zadoks et al., 1974) once during the growing season, using 10 samples of 0.5 m 0.5 m. Total weed cover was assessed in five quadrants (2 m 2 m) about 7 weeks before harvest.
2.2.
Sampling methods
Earthworm populations were investigated using a two-step method from 1996 to 1998 after the winter cereal crop harvest. Six samples were taken once per field in the autumn after the cereal harvest (1 and 3 October 1996 at locations 1 and 2; 21 and 22 October 1997 at locations 3 and 4; and 21 and 22 October 1998 at locations 5 and 6), extracted with a 0.33% mustard flour solution and then sorted by hand (Ho¨gger, 1993; Emmerling, 1995). For the extraction, 15 l of mustard solution was used over a sampling time of 40 min. The sampling unit that was hand-sorted was 50 cm 50 cm wide and 15 cm deep, and samples were separated by a distance of at least 15 m. With this well-established sampling method, anecic species (mustard extraction) as well as early diapausing and endogeic earthworms (handsorting) were efficiently recorded. The specimens collected were preserved in 4% formalin solution. Biomass loss during preservation was adjusted according to Cuendet (1995). Individual earthworms were identified as
186
Table 1 – Site characteristics of low-input integrated (ICM) and organic arable fields and agricultural practices in winter cereal fields within each farm Site characteristics Region Location/paired farms m a.s.l. Soil type
Soil analysisa Organic C (%) pH (0.1 KCl) Calcium (HCl/H2SO4)b P (sodium acetate)b Potassium (sodium acetate)b Cereal standsa (plants per m2) Weed cover (%)a Weed speciesa
351 330 Luvisol from Loess, medium silty-loam
b c d e
Tabular jura (Meso-European Foreland) 3 4
Pleistocene terraces 5
6
520 Calcic Cambisol, medium clay-loam ICM Bio-dyn. 2 2 >5 13
331 Cambisol from Loess, medium clay-loam ICM Organic 2 2 >5 17
356 Luvisol, medium clay-loam (6.1) and sandy-loam (6.2) ICM Organic 2 2 >10 5
ICM 2 >10
Organic 2 51
ICM 2 >10
Organic 2 17
499 Eutric Cambisol, medium clay-loam ICM Bio-dyn. 2 2 >10 19
3.2 6.5 6535
2.7 5.5 1855
2.5 6.0 2760
2.8 6.5 4615
4.6 6.3 3485
3.7 6.0 2515
4.7 7.2 6680
5.6 6.9 5595
3.1 6.0 2730
2.7 6.1 5420
3.0 5.1 830
3.7 6.1 1245
24
19
68
43
35
6
48
29
34
11
44
77
135
155
245
170
145
100
165
95
115
75
155
205
925
706
877
626
1003
809
964
756
942
508
880
699
6 5
21.5 14
0 0
14 8
6 5.5
11.5 13
5 8.5
12.5 18
0 0
10.5 13
4 2.5
15.5 10.5
OF 0.25 t, 0.3 t PS
FYM 20 m3, 0.27 t AN
FYM 33 m 3
65 m3 slurry, 0.1 t AN
30 m3 slurry
0.35 t AN
30 m3 slurry, 8 m3 compost
0.17 t AN
Compost 10 m 3
0.29 t AN
Compost 15 m3, 30 m3 slurry
Agricultural practices and yields Fertilizer to cereal cropc 90 m3 slurry, 0.07 t AN
a
2
Weed control Mechanical Chemicald
Yes 1
Yes –
No 2
Yes –
Yes 1
Yes –
No 2
No –
No 2
Yes –
No 2
Yes –
Cereal yielde
Medium
Medium
Medium
Low
Medium
Low
Medium
Medium
High
Medium
High
Low
Mean value for two fields per farm. mg/kg. Amount per ha. AN: ammonium nitrate, FYM: farmyard manure; PS: potassium sulphate, OF: organic poly-nutrient fertilizer. Number of applications. Yields: high 7–9 t/ha; medium 5–7 t/ha; low <5 t/ha.
applied soil ecology 37 (2007) 184–191
Farming method Number of fields Conversion time (years)
Loess covered hilly region 1
applied soil ecology 37 (2007) 184–191
187
adult (clitellate), sub-adult (large, but non-clitellate) or juvenile (non-clitellate). Species identification was performed according to the classification of Bouche´ (1972) and Cuendet (1990). For the purposes of presenting population data, earthworm species found on individual farms were grouped into the three ecological categories defined by Bouche´ (1977). The main principle in the ecological classification of earthworms is based on their behaviour, morpho-physiological features and key habitat.
2.3.
Statistical analysis
A two-way ANOVA was performed on the field level to test the effects of location and farming system on abundance, biomass and number of species (SPSS 10). Before analysis, each data set was tested for departure from normality using the Shapiro Wilk test. All analyses of data on abundances and biomass were performed on cube root transformed data (Boag et al., 1994). The mean values of number of juveniles and abundance of most abundant species were examined over all fields using the non-parametric Wilcoxon/Kruskal–Wallis test (Chi square approximation). To assess the potential impact of different soil tillage regimes on earthworms, differences in earthworm densities between fields at each location were analysed using the Multiple Tukey–Kramer HSD test ( p < 0.05). The influence of various environmental and management variables on the earthworm communities was studied using an ordination method, redundancy analysis (RDA), performed with the CANOCO program, version 4.5 (Ter Braak and Smilauer, 2002). This linear method performs a direct gradient analysis and is useful if gradients are short, as was the case in this investigation (Palmer, 2003). For this purpose, the data were pooled and rare species (frequency < 0.25) were omitted to minimize random effects and sampling errors. The farming systems were applied as two dummy-variables. All RDAs were run using untransformed data. Soil properties such as organic carbon, pH, calcium, phosphate, potassium, magnesium, iron, weed cover and cereal stand density were selected as quantitative environmental variables. Applying RDA in combination with forward selection, the significance of the single main variable was analysed by Monte Carlo with 499 permutations through testing of the axis associated with this variable, using the axis eigenvalue as the test statistic (Ter Braak, 1996).
3.
Results
Over all sites, the farming system significantly affected altered biomass (F-value = 23.83), abundance (F-value = 32.8) and species richness (F-value = 21.73), and no effect of location was found (two-way ANOVA with p < 0.001). The mean biomass and abundance of earthworms found in ICM fields were significantly lower than in the organic fields (Fig. 1a and b). During the 3-year investigation period, 12 earthworm species were found in the arable winter cereal fields, comprising 7 endogeic, 3 anecic and 2 epigeic species (Table 2). Seven endogeic, three anecic and two epigeic species occurred in the winter cereal plots. Over all sites, adult
Fig. 1 – Overall mean biomass W S.E.M. (a) and number of earthworms W S.E.M. (b) in low-input ICM cereal fields (white bars) and organic cereal fields (black bars). Twoway ANOVA: ***p < 0.001.
earthworms in organic fields were 114% more abundant than in ICM fields, but the frequencies for most species within the specific system were similar in both farming systems (Table 2). There were some exceptions with differences of more than 10% in frequency: Nicodrilus longus (Ude) and Nicodrilus nocturnus (Evans) occurred more frequently in the organic and Lumbricus rubellus (Sav.) more often in the ICM system (Table 2). The total number of species found per field was higher in the organic fields in 9 out of 12 cases and ranged from 4 to 8 species in the ICM and 5–9 species in the organic fields. The mean number of earthworm species and the number of juveniles found in all fields was significantly lower in ICM fields than in the organic fields (Table 3). Among the abundant species, numbers of anecic, vertically burrowing species such as Lumbricus terrestris (L.), N. longus and N. nocturnus as well as endogeic species such as Nicodrilus caliginosus (Sav.), Allolobophora rosea (Sav.) were significantly higher in the organic fields than in the low-input ICM fields. Allolobophora chlorotica (Sav.) was only found in four locations (1, 2, 3 and 4), and its numbers did not differ in ICM fields and organic fields. Redundancy analysis of earthworm communities as related to the analysed environmental factors revealed only farming system, density of cereal stands and potassium as significant factors. Farming system explained most of the variance at 40%, wheat density explained 15% and soil potassium 4%. Wheat density is a factor that is directly dependent on farming intensity, particularly on fertilizer input. Differences of earthworms within the same farm were also found on the level of location, which may be a consequence of
188
applied soil ecology 37 (2007) 184–191
Table 2 – Occurrence of adult earthworms in low-input ICM and organic cereal fields and their frequency per farming system, sorted according to ecological categories Typea
Species
Low-input farming system ICM
Lumbricus terrestris (Linnaeus, 1758) Nicodrilus longus (Ude, 1885) Nicodrilus nocturnus (Evans, 1946) Allolobophora chlorotica (Savigny, 1826) Allolobophora handlirschi (Rosa, 1897) Allolobophora icterica (Savigny, 1826) Allolobophora rosea (Savigny, 1826) Nicodrilus caliginosus (Savigny, 1826) Octolasion cyaneum (Savigny, 1826) Octolasion tyrtaeum lacteum (Oerley, 1885) Lumbricus castaneus (Savigny, 1826) Lumbricus rubellus (Hoffmeister, 1843)
Anecic Anecic Anecic Endogeic Endogeic Endogeic Endogeic Endogeic Endogeic Endogeic Epigeic Epigeic
Total adult individuals
Organic
Ab
F
Ab
F
43 103 45 72 7 72 122 88 8 11 6 24
0.92 0.83 0.75 0.58 0.42 0.33 0.92 0.83 0.42 0.17 0.25 0.42
192 240 108 86 17 118 207 273 16 17 7 4
0.92 1.00 0.92 0.67 0.33 0.33 1.00 0.92 0.42 0.17 0.25 0.25
601
1285
Ab: abundance (total number of earthworms in all samples); F: frequency per farming system. Ecological category.
a
different soil tillage regimes. Variation in earthworm densities between two fields at the same location and subject to the same farming system (Fig. 2) can partly be attributed to the use of the plough. When compared with reduced tillage using a grubber or harrow, ploughing consistently decreased earthworm densities. After late ploughing in autumn, earthworm densities were always significantly lower than with no ploughing or early ploughing in July or August. This can be
Table 3 – Analysis of number of earthworm species, juveniles and density of the most abundant species in low-input integrated (ICM) and organic (Org) farming system (Wilcoxon/Kruskal–Wallis test) System
SM
ChiSq
p
Number of species
ICM Org
58.32 86.68
17.24
***
Juveniles
ICM Org
61.47 83.53
10.10
**
ICM Org
60.56 84.44
14.06
***
Nicodrilus longus
ICM Org
56.12 88.88
23.28
***
Nicodrilus nocturnus
ICM Org
62.17 82.83
10.93
**
ICM Org
59.11 85.89
16.33
***
ICM Org
63.01 81.99
7.76
ICM Org
75.54 69.46
1.01
Anecic species Lumbricus terrestris
Endogeic species Nicodrilus caliginosus
Allolobophora rosea
Allolobophora chlorotica
SM: score mean; ChiSq: Chi square; n.s.: not significant. p < 0.01. *** p < 0.001. **
explained by earthworm biology: in the dry season, they prefer deeper soil layers with higher humidity, and are thus less severely affected by the plough and the accompanied tillage treatments.
4.
Discussion
4.1.
Earthworm biomass and abundance
The abundance, biomass and diversity of earthworm populations in agricultural soils is related to abiotic factors such as soil condition (e.g., soil structure, soil texture, temperature and humidity) and altitude, as well as agricultural practices
**
n.s.
Fig. 2 – Mean number of earthworms W S.E.M. in low-input integrated (ICM) and organic cereal field (org) in respect of soil tillage, indicated as follows: no plough use (white bar), early plough use (grey bar) and late plough use in autumn (black bar). Tukey HSD test performed separately for each location. Means with different letters are significantly different at p < 0.05.
applied soil ecology 37 (2007) 184–191
such as soil tillage, cropping systems and the use of fertilizers and pesticides (Lee, 1985; Edwards and Bohlen, 1996). In this study, the biomass and abundance of earthworms differed significantly between the two low-input farming systems but also in some cases within the farm. This indicates that the whole farming system, as well as specific practices differing at the farm level, may influence earthworms in a significant way. In many cases, earthworm communities in organic fields were significantly larger in abundance and biomass, and richer in number of species than in the low-input integrated farmed fields. These results are similar to those from comparative studies of conventional and organic farming systems (Bauchhenss, 1991; Scullion et al., 2002). However, in many cases earthworm biomass and abundance in both farming systems were relatively high for arable soils—Swiss arable soils cultivated using traditional, so-called ‘good agricultural practice’ (GAP), generally exhibit ranges of 60– 100 g/m2 and 80–120 specimens/m2. On a few sites, biomass and abundance were even higher than in nearby perennial, non-tilled grassland strips, mostly in organic fields. This indicates careful soil management at these sites that may increase numbers of earthworms through specific practices. Earthworm populations are usually significantly depressed in arable fields relative to grassland or undisturbed land (Didden, 2001). Multivariate analysis showed that the farming system, winter cereal density and one soil parameter (potassium) were significant factors influencing the earthworm populations. Winter cereal density correlated negatively and potassium soil content positively with earthworms. The farming system, explained 40% of the variance, and was thus shown to be a strong driving factor. The poor correlations of earthworm fauna with most chemical soil parameters indicate that the different agricultural practices may have much greater impacts on earthworms than the soil properties that varied within a small range between the different sites at each location. Therefore, agricultural practices which differed between the farming systems such as soil tillage, fertilizer management and plant protection management (history) were assumed to have altered the earthworm fauna in a significant way. Intensive soil tillage on arable land can eliminate earthworm populations within a single season (Curry et al., 2002). The extent of population reduction depends on the nature and frequency of cultivation and initial population levels, which in turn depend on the management history (Chan, 2001). The use of the plough in the fields investigated, particularly late ploughing in autumn when earthworm activity is high, clearly had a major negative impact on earthworm abundance, irrespective of farming system, and may therefore explain differences found within the farming system. Significant differences within the same farming system at one location can be attributed mainly to this key factor (locations 1, 2, 4 and 6). Ploughing has adverse effects on population density and diversity due to the mechanical disturbance that can lead to unstable microclimatic conditions and abrasive effects in the soil profile, as well as the removal of protective surface residues. The direct mortality arising from injury caused by ploughing was estimated at about 25% in a range of soils in Switzerland (Cuendet, 1983) or up to 60–70% using rotary cultivation, as reported from
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Sweden (Bostro¨m, 1988). In this investigation, which considers the same farming system using different methods of soil tillage, the reduction rate in numbers of earthworms by ploughing seems to be rather higher than 50% in some cases. In general, the fertilizer management of the organic fields may be more favourable due to a regular input of different organic materials (farmyard manure, slurry or compost) than the ICM that is mainly based on mineral fertilizers. As decomposers, earthworms need a constant supply of organic materials of various types, depending on the species (Piearce, 1978). The negative effect of mineral fertilizers may depend on the nature the fertilizer (Edwards and Lofty, 1982b). In the long-term trial conducted at Rothamsted, it was observed that the amount of N applied per hectare of organic matter N was more effective in raising earthworm populations than inorganic N; inorganic fertilizers led to significant lower abundance of L. terrestris and N. caliginosus. Similarly, in the present study, these two species were significantly more abundant in the organically fertilized than in the mineral or mixed fertilized ICM fields. This may be partly attributed to the specific fertilizer management. Pfiffner (1993) found negative effects of long-term pure mineral fertilization on earthworms (abundance, biomass and juvenile earthworms) compared with mixed mineral–organic nutrient management of conventionally managed arable fields. A 14-year study by Estevez et al. (1996) has shown that solid cattle manure improved earthworm populations and diversity compared to mineral fertilizer treatment and the control without fertilizer. However, depending on the type and the amount of fertilizer used, fertilizer management alters earthworm populations in a significant way. The fertilizer management on these organic farms was assumed to be more favourable for earthworms in terms of quantity, quality and continuity of food supply. A further aspect concerns plant protection measures differing between these two farming systems. It is well known that pesticides, particularly insecticides, nematicides, certain fungicides (e.g., benomyl), and herbicides (e.g., dinoseb), reduce earthworm populations. There is a considerable body of literature documenting the sublethal and lethal effects of pesticides and other chemicals on earthworms (e.g., Edwards and Bohlen, 1992, 1996; Greigh-Smith et al., 1992). In the present trial, no harmful pesticides were applied to the winter cereal crops in either farming system during the investigation period—only herbicides were used in the ICM fields. Herbicides tend to have low toxicity for earthworms, but can cause population reduction by decreasing sources of organic matter on which earthworms feed. However, non-target effects of insecticides or fungicides applied to the pre-crops of ICM farms are unclear, but not unlikely.
4.2.
Effects on earthworm species
In general, 12 common arable earthworm species were found in the 24 arable fields, which shows a relatively high species diversity, with 6 species occurred consistently or fairly frequently. In their investigation of 19 sites in Bavaria, Germany, Bauchhenss and Herr (1986) found much lower values, with 1–6 species in conventional arable fields.
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There was evidence that individual earthworm species differed in their response to the different farming systems. The numbers of earthworm species and juveniles were mostly significantly lower in ICM fields. Deep burrowing, anecic species such as L. terrestris, N. longus and N. nocturnus, as well as endogeic species such as N. caliginosus, A. rosea and A. icterica were generally more prevalent in the organic fields than in the low-input ICM fields. This confirms findings in a long-term field trial comparing conventional and organic arable fields, where higher biomass and abundance of anecic earthworms was found in the organic plots (Pfiffner, 1993). High densities of anecic species can alter soil properties. They are particularly effective in the creation of stable, vertical, macroporous channels which can modify aeration and patterns of water infiltration (Joschko et al., 1989; Edwards et al., 1990). Lower number of species, less juvenile earthworms and lower abundance of certain species found in the ICM fields reveal different communities of earthworms in these two farming systems. However, the relative frequencies of most species within the respective systems were similar in both farming systems, which indicate that a species potential still exists in these ICM-fields.
5.
Conclusions
A comparison of two low-input farming systems revealed higher biomass, density, number of juveniles and adults and differences in species occurrence of earthworms in organic cereal fields. This demonstrates differences in community structure between the two farming systems and indicates that organic farming can benefit earthworm populations on a broader range than ICM low-input farming. Agricultural practices such as soil tillage, fertilizer management and plant protection are assumed to be the factors that exert the greatest influence on earthworm populations. A careful choice of earthworm-enhancing or harmless farming practices across the whole crop rotation is necessary to conserve earthworms in a sustainable way. For example, we observed that a single factor, e.g., ploughing in late autumn, can drastically reduce the earthworm fauna, irrespective of the farming system. Differences such as higher abundance of deep burrowing species and species diversity in organic fields found in populations may have implications for soil fertility and wider ecosystem functions—this warrants further investigation.
Acknowledgements We would like to thank D. Zwygart, R. Mu¨hlethaler for field assistance and the farmers for their cooperation on their land, and also P. Maeder, A. Lang and G. Cuendet (taxonomic support), and the two anonymous referees for useful comments and suggestions on an earlier draft of the manuscript. We thank the canton Baselland, Ministry for Environment, Pro Natura Switzerland, Foundation E. Guggenheim-Schnurr and Arbeitsgemeinschaft fu¨r Natur- and Heimatschutz for their financial support.
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