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The impact of grassy field margins on macro-invertebrate abundance in adjacent arable fields
Agriculture, Ecosystems and Environment 139 (2010) 280–283
Contents lists available at ScienceDirect
Agriculture, Ecosystems and Environment journal homepage: www.elsevier.com/locate/agee
The impact of grassy field margins on macro-invertebrate abundance in adjacent arable fields Anouschka R. Hof ∗ , Paul W. Bright School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX, United Kingdom
a r t i c l e
i n f o
Article history: Received 18 January 2010 Received in revised form 21 August 2010 Accepted 24 August 2010 Available online 21 September 2010 Keywords: Arable landscapes Agri-environment scheme Invertebrates Field margin
a b s t r a c t Grassy field margins are thought to be an important feature for a variety of species in arable landscapes. However, not many studies address the impact of such margins in arable landscapes on the abundance of macro-invertebrates in arable fields. We estimated the abundance of earthworms, gastropods and carabids in fields with and without a grassy margin. Additionally, fields were sampled along the edge and further in the field. From our findings we can conclude that the presence of grassy field margins in arable landscapes increases the abundance of carabids and earthworms but decreases the abundance of gastropods. These effects were mainly noticeable on the edge of the field, but appear to be occurring further in the field as well. © 2010 Elsevier B.V. All rights reserved.
1. Introduction About 38% of the total land area of the world was used for agricultural purposes in 2004 (Clay, 2004), an area potentially valuable for an array of species (e.g. Chamberlain et al., 2000; Robinson and Sutherland, 2002). However, especially after the Second World War, farm management rapidly changed and intensified resulting in a reduction in diversity of landscapes (Robinson and Sutherland, 2002; Foley et al., 2005). Consequently, changes in agricultural management have frequently been mentioned as one of the major causes for the loss of species diversity and abundance (e.g. Krebs et al., 1999; Donald et al., 2001; Robinson and Sutherland, 2002; Foley et al., 2005). Agri-environment schemes were introduced into the agricultural policy of the USA, Australia and in the European Union, during the last few decades, partly with the aim of protecting biodiversity and also in an attempt to reverse some of the negative impacts of agricultural intensification on wildlife and the environment (Australian Government, 2009; European Commission, 2009; United States Department of Agriculture, 2009). Many existing agrienvironment schemes have provision for grassy, or uncultivated, field margins (e.g. Benton, 2007; Butler et al., 2007). Many studies focus on the effect of different arable field margin management
∗ Corresponding author at: Department of Ecology and Environmental Science, Umeå University, SE-901 87 Umeå, Sweden. Tel.: +46 090 7866377. E-mail addresses: [email protected], [email protected] (A.R. Hof). 0167-8809/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2010.08.014
strategies on invertebrates (e.g. Morris and Webb, 1987; Kromp and Steinberger, 1992; Baines et al., 1998; Asteraki et al., 2004; Woodcock et al., 2005, 2007). However few studies investigated the impact of the presence of a grassy field margin in itself in comparison with its absence (Yu et al., 2006). More studies investigate whether a possible positive effect of grassy field margins on invertebrate abundance extends to surrounding arable fields (Kromp and Steinberger, 1992; Kádár et al., 2004; Saska et al., 2007; Smith et al., 2008; Werling and Gratton, 2008; Twardowski and Pastuszko, 2008), but many of these studies focus on a specific group of invertebrates. Marshall et al. (2006) investigated the impact of agrienvironment field margins and found positive impacts on diversity or abundance for flora, bees and orthoptera, but not for birds, spiders and carabids. However, it has also been found that undisturbed boundaries such as hedges and beetle banks, may act as winter reservoirs for some species of carabids in arable landscapes (Sotherton, 1984, 1985; Morris and Webb, 1987). Dennis and Fry (1992) found that the predatory arthropod species diversity is higher near grassy field boundaries. Whether the abundance of earthworms and gastropods may be enhanced in arable fields by the presence of an unmanaged boundary is currently not well studied and might be important with respect to the conservation of invertebrates and their predators, and to pest management. Complementary to the available literature, this paper investigates if the presence of grassy field margins affects the abundance of macro-invertebrates (earthworms, gastropods and carabids) in the field margin, and in adjacent arable fields.
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2. Materials and methods A total of 32 arable fields were sampled for invertebrate abundance in May–July 2009. All fields were surrounded by an established hedgerow of at least 2 m wide. Half of these fields were surrounded by a grassy field margin of 4–6 m wide and managed through an agri-environment scheme (Entry Level Stewardship [Natural England, 2008]). The remaining 16 fields did not have a grassy field margin; they were either harvested up to the hedgerow or a fringe (<1 m) of scrub and or nettles was still present. In order to minimize impacts of other environmental variables, such as soil type and soil moisture, on invertebrate abundance, fields with and without a grassy field margin were paired. Paired fields were located on the same farm, were of a similar size, had similar soils, and were under similar management regimes but for the presence of a grassy field margin. Samples on paired fields were taken on the same side (cardinal direction) of the hedgerow when possible. Wheat was grown on all arable fields sampled. Paired fields were sampled on the same day to ensure consistent weather conditions. Fields were located in four study sites in the U.K., i.e. near Brancaster (Norfolk, 52◦ , 96 N, 0◦ , 63 E), Gedney Drove End (Lincolnshire, 52◦ , 85 N, 0◦ , 16 E), Great Easton (Leicestershire, 52◦ , 53 N, −0◦ , 75 E), and Old Windsor (Berkshire, 51◦ , 46 N, −0◦ , 59 E). To study the abundance of earthworms, a soil core with a diameter and depth of 15 cm was taken with the use of a soil auger. The sample was weighed and sieved in the field for worms. The total number of earthworms (both adults and juveniles >5 mm) and their total biomass (weight of all living individuals >5 mm found) were noted. A total of 15 soil samples were taken per field; 5 within 1 m distance of the hedgerow, 5 at 10 m from the hedgerow and 5 at 20 m from the hedgerow. The number and biomass of gastropods (slugs and snails >5 mm) was estimated visually (as recommended by Sutherland, 1996) during the night, when they are most active, by spot sampling, using a 0.5 m2 quadrangle according to the same sampling strategy as used for earthworms. Patches were systematically searched for as long as was necessary for the observer to feel confident that all gastropods larger then 5 mm were collected. A standard observation time was deemed unsuitable due to variability of vegetation cover. Living individuals were counted and weighed before releasing them again. The total number and biomass of gastropods was noted. Pitfall traps were used to study the species richness and abundance of carabids according to the same sampling strategy as mentioned above. Plastic cups (diameter: 8 cm, depth: 14 cm) were placed in the soil 1 cm below the surface so as not to impede access to the cup. Traps were filled half with anti-freeze in order to immobilize invertebrates. The traps were left in the field for 72 h. Carabids in the traps were identified and counted using a standard key (Luff, 2007). As the data was not normally distributed, despite possible data transformation, the non-parametric Wilcoxon signed-rank test and the Kruskal–Wallis test were used to analyse differences in the average invertebrate abundance and biomass (based on five samples per field per edge-distance) between fields with and without a grassy margin and between edge-distances, using PASW Statistics 18 (SPSS Inc., Chicago, USA).
3. Results 3.1. Earthworms The mean number of earthworms in the soil was significantly higher on fields with than on fields without a grassy
Fig. 1. Mean number (N) (±S.E.) of earthworms in the soil in fields with and fields without a grassy margin per edge-distance. *Significant difference (p < 0.05).
margin (Wilcoxon signed-rank test: Z = −5.874, p < 0.001) at 0 and 20 m from the edge (Wilcoxon signed-rank test 0 m: Z = −5.855, p < 0.001, 20 m: F = −2.458, p = 0.014), but not at 10 m from the edge (Wilcoxon signed-rank test: Z = −0.235, p = 0.814). The mean biomass of earthworms was also significantly higher on fields with than on fields without a grassy margin (Wilcoxon signed-rank test: Z = −3.701, p < 0.001) at 0 m (Wilcoxon signed-rank test: Z = −3.859, p < 0.001), but not at 10 and 20 m from the edge (Wilcoxon signed-rank test 10 m: Z = −0.363, p = 0.717, 20 m: Z = −1.820, p = 0.069). We found that on fields with and on fields without a grassy margin both the mean number and the mean biomass of earthworms were significantly higher at 0 m from the edge than at either 10 or 20 m from the edge (Kruskal–Wallis mean number on fields with a grassy margin: 2 = 62.886, df = 2 p < 0.001, mean biomass on fields with a grassy margin: 2 = 46.807, df = 2 p < 0.001, mean number on fields without a grassy margin: 2 = 7.589, df = 2 p = 0.022, mean biomass on fields without a grassy margin: 2 = 6.364, df = 2 p = 0.042). Fig. 1 shows the mean number of earthworms. 3.2. Gastropods The mean number of gastropods was significantly lower on fields with than on fields without a grassy margin (Wilcoxon signed-rank test: Z = −3.208, p = 0.001), at 0 and 10 m from the edge (Wilcoxon signed-rank test 0 m: Z = −2.056, p = 0.040, 10 m: Z = −2.843, p = 0.004), but not at 20 m (Wilcoxon signed-rank test: Z = −2.582, p = 0.010). Their mean biomass was also significantly lower on fields with a grassy margin (Wilcoxon signed-rank test: Z = −2.000, p = 0.045), but only at 0 m from the edge (Wilcoxon signed-rank test: Z = −2.091, p = 0.037). There was no significant difference at 10 and at 20 m from the edge (Wilcoxon signed-rank test 10 m: Z = −0.889, p = 0.374, 20 m: Z = 0.000, p = 1.000). On fields with a grassy margin, the mean number of gastropods did also significantly differ between edge-distances, with the highest number found closest to the edge (Kruskal–Wallis: 2 = 6.318, df = 2 p = 0.042), but not their mean biomass (Kruskal–Wallis: 2 = 5.845, df = 2 p = 0.054). On fields without a grassy margin both the mean number and biomass of gastropods were significantly the highest at 0 m from the edge (Kruskal–Wallis mean number: 2 = 6.078, df = 2 p = 0.048, mean biomass: 2 = 6.522, df = 2
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Fig. 2. Mean number (N) (±S.E.) of gastropods in fields with and fields without a grassy margin per edge-distance. *Significant difference (p < 0.05).
Fig. 3. Mean number (N) (±S.E.) of carabids in the pitfall traps in fields with and fields without a grassy margin per edge-distance. *Significant difference (p < 0.05).
p = 0.038). The result for the mean number of gastropods is shown in Fig. 2.
4. Discussion
3.3. Carabids In total 18 species of carabids were found in the study sites, of which 72% predators, 22% phytophagous species, and 6% detritivores. Pterostichus madidus was by far the most abundant (89%), followed by Dromius quadrimaculatus and Harpalus affinis. More species were found on fields without (n = 18) than on fields with a grassy margin (n = 12). Five of the species not found on fields with a grassy margin were predators (Anchomenus dorsalis, Bembidion tetracolum, Bembidion lampros, Ocypus olens, Ocys harpaloides) whilst one (Bradycellus verbasci) was phytophagous. However, only a few individuals (n < 8) of these species were caught; observations were not significant (Wilcoxon signed-rank test predators: Z = −1.203, p = 0.229, phythophagous species: Z = −1.632, p = 0.103, detrivores: Z = −1.342, p = 0.180). The mean number of predator species found did not significantly differ between edge-distance either (Kruskal–Wallis field margin: 2 = 2.082, df = 2 p = 0.353, no field margin: 2 = 0.638, df = 2 p = 0.727). The mean number of carabids in the pitfall traps was significantly higher on fields with than on fields without a grassy margin (Wilcoxon signed-rank test: Z = −2.956, p = 0.003), but just at 0 m from the edge (Wilcoxon signed-rank test: Z = −2.593, p = 0.010). There were no significant differences at 10 and at 20 m from the edge (Wilcoxon signed-rank test 10 m: Z = −0.931, p = 0.352, 20 m: Z = −1.480, p = 0.139). The mean number of carabids did not significantly differ between edge-distances on fields with and without a grassy margin (Kruskal–Wallis fields with a grassy margin: 2 = 4.556, df = 2 p = 0.102, fields without a grassy margin: 2 = 1.426, df = 2 p = 0.490). The number of species found in the pitfall traps was not significantly different between fields with and fields without a grassy margin, regardless of the edge-distance (Wilcoxon signedrank test all: Z = −0.055, p = 0.956, 0 m: Z = −0.878, p = 0.380, 10 m: Z = −0.465, p = 0.642, 20 m: Z = −0.451, p = 0.652). The number of species was not significantly different between edge-distances either (Kruskal–Wallis fields with a grassy margin: 2 = 5.318, df = 2 p = 0.070, fields without a grassy margin: 2 = 0.815, df = 2 p = 0.665). Fig. 3 shows the mean number of carabids.
In our study carabids were more abundant on arable fields that had grassy margins along the edges. Although this appeared to be especially so away from the edge of the field; we did not find any significant differences at both 10 and 20 m from the edge, likely due to the high standard error of the mean. However, it must be noted that pitfall trap catches not only depend on the density of populations, but on other factors such as activity and body size of the species as well (Lang, 2000). Indeed, it is known that uncultivated borders may act as winter reservoirs in arable landscapes from where carabids disperse to bordering arable fields (Sotherton, 1984, 1985; Morris and Webb, 1987). A hedgerow combined with a grassy field margin seems to be more beneficial than a hedgerow by itself. We found that earthworms, like carabids, were significantly more abundant on fields with a grassy margin than on fields without one. This higher abundance was not limited to the edge of the field. Earthworms were more numerous near the edge of the field, regardless the presence of a grassy margin, than towards the centre of the field. The current available literature is ambiguous with regard to the abundance of earthworms in arable fields. They have been reported to be more abundant in field margins and in hedges than in adjacent arable fields (Curry, 1998; Fournier and Loreau, 2001). This would explain higher earthworm abundance on fields with a grassy margin, and near the edge of the field, as found in our study. However, Lagerlöf et al. (2002) found that earthworms were more abundant in the arable field than on the adjacent margin. Furthermore, under warm and dry conditions, earthworms may burrow deeper into the soil (Curry, 1998), the depth of the soil sample taken might therefore become an important factor in estimating earthworm abundance under such conditions. Our study shows that in contrast to carabids and earthworms, gastropods were less abundant on fields with a grassy margin than on fields without one, which might be related to the presence of predatory carabids. Although slug predation by carabids might diminish in the presence of alternative prey like earthworms (Mair and Port, 2001; Symondson et al., 2006), carabids, such as Pterostichus madidus, are indeed able to control slug pests to a certain extent (Asteraki, 1993; Oberholzer and Frank, 2003; Oberholzer et al., 2003). Furthermore, irrespective of the presence of a grassy margin the mean number of gastropods was higher near the edge of
A.R. Hof, P.W. Bright / Agriculture, Ecosystems and Environment 139 (2010) 280–283
the field. Frank (1998) also found that wild flower strips near arable fields might act as a source for slugs. These results show clear implications for pest management; crops in fields with a grassy field margin are likely to be less affected by the presence of gastropods. We can conclude that grassy field margins in arable landscapes are able to increase the abundance of carabids and earthworms. The addition of such margins in arable landscapes might therefore also benefit predators of macro-invertebrates such as the lapwing (Vanellus vanellus) and the hedgehog (Erinaceus europaeus). Gastropods, pests to a variety of crops, on the other hand, were negatively affected by the presence of a grassy field margin, possibly due to a large amount of carabids in these fields. A variety of existing agri-environment schemes throughout Europe already include grassy field margins (e.g. Benton, 2007; Butler et al., 2007). An increased implementation of such schemes by landowners might therefore be beneficial to a number of macro-invertebrates and their predators (cf. Dennis and Fry, 1992). Acknowledgements We wish to thank the farmers who were so kind in permitting fieldwork on their land. We were also grateful for the help of fieldwork assistants Michael Bennett and Pieter Berends. The entire project was funded jointly by the People’s Trust of Endangered Species, the British Hedgehog Preservation Society and by a legacy of Dilys Breece, to whom we are greatly indebted. We would also like to thank two anonymous referees for their useful comments. References Asteraki, E.J., 1993. The potential of carabid beetles to control slugs in grass/clover swards. Entomophaga 38, 193–198. Asteraki, E.J., Hart, B.J., Ings, T.C., Manley, W.J., 2004. Factors influencing the plant and invertebrate diversity of arable field margins. Agric. Ecosyst. Environ. 102, 219–231. Australian Government, 2009. Caring for our Country—Environmental Stewardship. Available at: http://www.nrm.gov.au/stewardship/index.html (accessed December 2009). Baines, M., Hambler, C., Johnson, P.J., MacDonald, D.W., Smith, H., 1998. The effects of arable field margin management on the abundance and species richness of Araneae (Spiders). Ecography 21, 74–86. Benton, T.G., 2007. Managing farming’s footprint on biodiversity. Science 315, 341–342. Butler, S.J., Vickery, J.A., Norris, K., 2007. Farmland biodiversity and the footprint of agriculture. Science 315, 381–384. Chamberlain, D.E., Fuller, R.J., Bunce, R.G.H., Duckworth, J.C., Shrubb, M., 2000. Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales. J. Appl. Ecol. 37, 771–788. Clay, J., 2004. World Agriculture and The Environment: A Commodity-byCommodity Guide to Impacts and Practices. Island Press, Washington, DC. Curry, J.P., 1998. Factors affecting earthworm abundance in soils. In: Edwards, C.A. (Ed.), Earthworm Ecology. CRC Press LLC, Boca Raton, pp. 37–64. Dennis, P., Fry, G.L.A., 1992. Field margins: can they enhance natural enemy population densities and general arthropod diversity on farmland? Agric. Ecosyst. Environ. 40, 95–115. Donald, P.F., Green, R.E., Heath, M.F., 2001. Agricultural intensification and the collapse of Europe’s farmland bird populations. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 268, 25–29. European Commission, 2009. Agriculture and The Environment. Available at: (accessed http://ec.europa.eu/agriculture/envir/measures/index en.htm September 2009). Foley, J.A., DeFries, R., Asner, G.P., Barford, C., Bonan, G., Carpenter, S.R., Chapin, F.S., Coe, M.T., Daily, G.C., Gibbs, H.K., Helkowski, J.H., Holloway, T., Howard, E.A., Kucharik, C.J., Monfreda, C., Patz, J.A., Prentice, I.C., Navin Ramankutty, N., Snyder, P.K., 2005. Global consequences of land use. Science 309, 570–574.
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Contents lists available at ScienceDirect
Agriculture, Ecosystems and Environment journal homepage: www.elsevier.com/locate/agee
The impact of grassy field margins on macro-invertebrate abundance in adjacent arable fields Anouschka R. Hof ∗ , Paul W. Bright School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX, United Kingdom
a r t i c l e
i n f o
Article history: Received 18 January 2010 Received in revised form 21 August 2010 Accepted 24 August 2010 Available online 21 September 2010 Keywords: Arable landscapes Agri-environment scheme Invertebrates Field margin
a b s t r a c t Grassy field margins are thought to be an important feature for a variety of species in arable landscapes. However, not many studies address the impact of such margins in arable landscapes on the abundance of macro-invertebrates in arable fields. We estimated the abundance of earthworms, gastropods and carabids in fields with and without a grassy margin. Additionally, fields were sampled along the edge and further in the field. From our findings we can conclude that the presence of grassy field margins in arable landscapes increases the abundance of carabids and earthworms but decreases the abundance of gastropods. These effects were mainly noticeable on the edge of the field, but appear to be occurring further in the field as well. © 2010 Elsevier B.V. All rights reserved.
1. Introduction About 38% of the total land area of the world was used for agricultural purposes in 2004 (Clay, 2004), an area potentially valuable for an array of species (e.g. Chamberlain et al., 2000; Robinson and Sutherland, 2002). However, especially after the Second World War, farm management rapidly changed and intensified resulting in a reduction in diversity of landscapes (Robinson and Sutherland, 2002; Foley et al., 2005). Consequently, changes in agricultural management have frequently been mentioned as one of the major causes for the loss of species diversity and abundance (e.g. Krebs et al., 1999; Donald et al., 2001; Robinson and Sutherland, 2002; Foley et al., 2005). Agri-environment schemes were introduced into the agricultural policy of the USA, Australia and in the European Union, during the last few decades, partly with the aim of protecting biodiversity and also in an attempt to reverse some of the negative impacts of agricultural intensification on wildlife and the environment (Australian Government, 2009; European Commission, 2009; United States Department of Agriculture, 2009). Many existing agrienvironment schemes have provision for grassy, or uncultivated, field margins (e.g. Benton, 2007; Butler et al., 2007). Many studies focus on the effect of different arable field margin management
∗ Corresponding author at: Department of Ecology and Environmental Science, Umeå University, SE-901 87 Umeå, Sweden. Tel.: +46 090 7866377. E-mail addresses: [email protected], [email protected] (A.R. Hof). 0167-8809/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2010.08.014
strategies on invertebrates (e.g. Morris and Webb, 1987; Kromp and Steinberger, 1992; Baines et al., 1998; Asteraki et al., 2004; Woodcock et al., 2005, 2007). However few studies investigated the impact of the presence of a grassy field margin in itself in comparison with its absence (Yu et al., 2006). More studies investigate whether a possible positive effect of grassy field margins on invertebrate abundance extends to surrounding arable fields (Kromp and Steinberger, 1992; Kádár et al., 2004; Saska et al., 2007; Smith et al., 2008; Werling and Gratton, 2008; Twardowski and Pastuszko, 2008), but many of these studies focus on a specific group of invertebrates. Marshall et al. (2006) investigated the impact of agrienvironment field margins and found positive impacts on diversity or abundance for flora, bees and orthoptera, but not for birds, spiders and carabids. However, it has also been found that undisturbed boundaries such as hedges and beetle banks, may act as winter reservoirs for some species of carabids in arable landscapes (Sotherton, 1984, 1985; Morris and Webb, 1987). Dennis and Fry (1992) found that the predatory arthropod species diversity is higher near grassy field boundaries. Whether the abundance of earthworms and gastropods may be enhanced in arable fields by the presence of an unmanaged boundary is currently not well studied and might be important with respect to the conservation of invertebrates and their predators, and to pest management. Complementary to the available literature, this paper investigates if the presence of grassy field margins affects the abundance of macro-invertebrates (earthworms, gastropods and carabids) in the field margin, and in adjacent arable fields.
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2. Materials and methods A total of 32 arable fields were sampled for invertebrate abundance in May–July 2009. All fields were surrounded by an established hedgerow of at least 2 m wide. Half of these fields were surrounded by a grassy field margin of 4–6 m wide and managed through an agri-environment scheme (Entry Level Stewardship [Natural England, 2008]). The remaining 16 fields did not have a grassy field margin; they were either harvested up to the hedgerow or a fringe (<1 m) of scrub and or nettles was still present. In order to minimize impacts of other environmental variables, such as soil type and soil moisture, on invertebrate abundance, fields with and without a grassy field margin were paired. Paired fields were located on the same farm, were of a similar size, had similar soils, and were under similar management regimes but for the presence of a grassy field margin. Samples on paired fields were taken on the same side (cardinal direction) of the hedgerow when possible. Wheat was grown on all arable fields sampled. Paired fields were sampled on the same day to ensure consistent weather conditions. Fields were located in four study sites in the U.K., i.e. near Brancaster (Norfolk, 52◦ , 96 N, 0◦ , 63 E), Gedney Drove End (Lincolnshire, 52◦ , 85 N, 0◦ , 16 E), Great Easton (Leicestershire, 52◦ , 53 N, −0◦ , 75 E), and Old Windsor (Berkshire, 51◦ , 46 N, −0◦ , 59 E). To study the abundance of earthworms, a soil core with a diameter and depth of 15 cm was taken with the use of a soil auger. The sample was weighed and sieved in the field for worms. The total number of earthworms (both adults and juveniles >5 mm) and their total biomass (weight of all living individuals >5 mm found) were noted. A total of 15 soil samples were taken per field; 5 within 1 m distance of the hedgerow, 5 at 10 m from the hedgerow and 5 at 20 m from the hedgerow. The number and biomass of gastropods (slugs and snails >5 mm) was estimated visually (as recommended by Sutherland, 1996) during the night, when they are most active, by spot sampling, using a 0.5 m2 quadrangle according to the same sampling strategy as used for earthworms. Patches were systematically searched for as long as was necessary for the observer to feel confident that all gastropods larger then 5 mm were collected. A standard observation time was deemed unsuitable due to variability of vegetation cover. Living individuals were counted and weighed before releasing them again. The total number and biomass of gastropods was noted. Pitfall traps were used to study the species richness and abundance of carabids according to the same sampling strategy as mentioned above. Plastic cups (diameter: 8 cm, depth: 14 cm) were placed in the soil 1 cm below the surface so as not to impede access to the cup. Traps were filled half with anti-freeze in order to immobilize invertebrates. The traps were left in the field for 72 h. Carabids in the traps were identified and counted using a standard key (Luff, 2007). As the data was not normally distributed, despite possible data transformation, the non-parametric Wilcoxon signed-rank test and the Kruskal–Wallis test were used to analyse differences in the average invertebrate abundance and biomass (based on five samples per field per edge-distance) between fields with and without a grassy margin and between edge-distances, using PASW Statistics 18 (SPSS Inc., Chicago, USA).
3. Results 3.1. Earthworms The mean number of earthworms in the soil was significantly higher on fields with than on fields without a grassy
Fig. 1. Mean number (N) (±S.E.) of earthworms in the soil in fields with and fields without a grassy margin per edge-distance. *Significant difference (p < 0.05).
margin (Wilcoxon signed-rank test: Z = −5.874, p < 0.001) at 0 and 20 m from the edge (Wilcoxon signed-rank test 0 m: Z = −5.855, p < 0.001, 20 m: F = −2.458, p = 0.014), but not at 10 m from the edge (Wilcoxon signed-rank test: Z = −0.235, p = 0.814). The mean biomass of earthworms was also significantly higher on fields with than on fields without a grassy margin (Wilcoxon signed-rank test: Z = −3.701, p < 0.001) at 0 m (Wilcoxon signed-rank test: Z = −3.859, p < 0.001), but not at 10 and 20 m from the edge (Wilcoxon signed-rank test 10 m: Z = −0.363, p = 0.717, 20 m: Z = −1.820, p = 0.069). We found that on fields with and on fields without a grassy margin both the mean number and the mean biomass of earthworms were significantly higher at 0 m from the edge than at either 10 or 20 m from the edge (Kruskal–Wallis mean number on fields with a grassy margin: 2 = 62.886, df = 2 p < 0.001, mean biomass on fields with a grassy margin: 2 = 46.807, df = 2 p < 0.001, mean number on fields without a grassy margin: 2 = 7.589, df = 2 p = 0.022, mean biomass on fields without a grassy margin: 2 = 6.364, df = 2 p = 0.042). Fig. 1 shows the mean number of earthworms. 3.2. Gastropods The mean number of gastropods was significantly lower on fields with than on fields without a grassy margin (Wilcoxon signed-rank test: Z = −3.208, p = 0.001), at 0 and 10 m from the edge (Wilcoxon signed-rank test 0 m: Z = −2.056, p = 0.040, 10 m: Z = −2.843, p = 0.004), but not at 20 m (Wilcoxon signed-rank test: Z = −2.582, p = 0.010). Their mean biomass was also significantly lower on fields with a grassy margin (Wilcoxon signed-rank test: Z = −2.000, p = 0.045), but only at 0 m from the edge (Wilcoxon signed-rank test: Z = −2.091, p = 0.037). There was no significant difference at 10 and at 20 m from the edge (Wilcoxon signed-rank test 10 m: Z = −0.889, p = 0.374, 20 m: Z = 0.000, p = 1.000). On fields with a grassy margin, the mean number of gastropods did also significantly differ between edge-distances, with the highest number found closest to the edge (Kruskal–Wallis: 2 = 6.318, df = 2 p = 0.042), but not their mean biomass (Kruskal–Wallis: 2 = 5.845, df = 2 p = 0.054). On fields without a grassy margin both the mean number and biomass of gastropods were significantly the highest at 0 m from the edge (Kruskal–Wallis mean number: 2 = 6.078, df = 2 p = 0.048, mean biomass: 2 = 6.522, df = 2
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Fig. 2. Mean number (N) (±S.E.) of gastropods in fields with and fields without a grassy margin per edge-distance. *Significant difference (p < 0.05).
Fig. 3. Mean number (N) (±S.E.) of carabids in the pitfall traps in fields with and fields without a grassy margin per edge-distance. *Significant difference (p < 0.05).
p = 0.038). The result for the mean number of gastropods is shown in Fig. 2.
4. Discussion
3.3. Carabids In total 18 species of carabids were found in the study sites, of which 72% predators, 22% phytophagous species, and 6% detritivores. Pterostichus madidus was by far the most abundant (89%), followed by Dromius quadrimaculatus and Harpalus affinis. More species were found on fields without (n = 18) than on fields with a grassy margin (n = 12). Five of the species not found on fields with a grassy margin were predators (Anchomenus dorsalis, Bembidion tetracolum, Bembidion lampros, Ocypus olens, Ocys harpaloides) whilst one (Bradycellus verbasci) was phytophagous. However, only a few individuals (n < 8) of these species were caught; observations were not significant (Wilcoxon signed-rank test predators: Z = −1.203, p = 0.229, phythophagous species: Z = −1.632, p = 0.103, detrivores: Z = −1.342, p = 0.180). The mean number of predator species found did not significantly differ between edge-distance either (Kruskal–Wallis field margin: 2 = 2.082, df = 2 p = 0.353, no field margin: 2 = 0.638, df = 2 p = 0.727). The mean number of carabids in the pitfall traps was significantly higher on fields with than on fields without a grassy margin (Wilcoxon signed-rank test: Z = −2.956, p = 0.003), but just at 0 m from the edge (Wilcoxon signed-rank test: Z = −2.593, p = 0.010). There were no significant differences at 10 and at 20 m from the edge (Wilcoxon signed-rank test 10 m: Z = −0.931, p = 0.352, 20 m: Z = −1.480, p = 0.139). The mean number of carabids did not significantly differ between edge-distances on fields with and without a grassy margin (Kruskal–Wallis fields with a grassy margin: 2 = 4.556, df = 2 p = 0.102, fields without a grassy margin: 2 = 1.426, df = 2 p = 0.490). The number of species found in the pitfall traps was not significantly different between fields with and fields without a grassy margin, regardless of the edge-distance (Wilcoxon signedrank test all: Z = −0.055, p = 0.956, 0 m: Z = −0.878, p = 0.380, 10 m: Z = −0.465, p = 0.642, 20 m: Z = −0.451, p = 0.652). The number of species was not significantly different between edge-distances either (Kruskal–Wallis fields with a grassy margin: 2 = 5.318, df = 2 p = 0.070, fields without a grassy margin: 2 = 0.815, df = 2 p = 0.665). Fig. 3 shows the mean number of carabids.
In our study carabids were more abundant on arable fields that had grassy margins along the edges. Although this appeared to be especially so away from the edge of the field; we did not find any significant differences at both 10 and 20 m from the edge, likely due to the high standard error of the mean. However, it must be noted that pitfall trap catches not only depend on the density of populations, but on other factors such as activity and body size of the species as well (Lang, 2000). Indeed, it is known that uncultivated borders may act as winter reservoirs in arable landscapes from where carabids disperse to bordering arable fields (Sotherton, 1984, 1985; Morris and Webb, 1987). A hedgerow combined with a grassy field margin seems to be more beneficial than a hedgerow by itself. We found that earthworms, like carabids, were significantly more abundant on fields with a grassy margin than on fields without one. This higher abundance was not limited to the edge of the field. Earthworms were more numerous near the edge of the field, regardless the presence of a grassy margin, than towards the centre of the field. The current available literature is ambiguous with regard to the abundance of earthworms in arable fields. They have been reported to be more abundant in field margins and in hedges than in adjacent arable fields (Curry, 1998; Fournier and Loreau, 2001). This would explain higher earthworm abundance on fields with a grassy margin, and near the edge of the field, as found in our study. However, Lagerlöf et al. (2002) found that earthworms were more abundant in the arable field than on the adjacent margin. Furthermore, under warm and dry conditions, earthworms may burrow deeper into the soil (Curry, 1998), the depth of the soil sample taken might therefore become an important factor in estimating earthworm abundance under such conditions. Our study shows that in contrast to carabids and earthworms, gastropods were less abundant on fields with a grassy margin than on fields without one, which might be related to the presence of predatory carabids. Although slug predation by carabids might diminish in the presence of alternative prey like earthworms (Mair and Port, 2001; Symondson et al., 2006), carabids, such as Pterostichus madidus, are indeed able to control slug pests to a certain extent (Asteraki, 1993; Oberholzer and Frank, 2003; Oberholzer et al., 2003). Furthermore, irrespective of the presence of a grassy margin the mean number of gastropods was higher near the edge of
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the field. Frank (1998) also found that wild flower strips near arable fields might act as a source for slugs. These results show clear implications for pest management; crops in fields with a grassy field margin are likely to be less affected by the presence of gastropods. We can conclude that grassy field margins in arable landscapes are able to increase the abundance of carabids and earthworms. The addition of such margins in arable landscapes might therefore also benefit predators of macro-invertebrates such as the lapwing (Vanellus vanellus) and the hedgehog (Erinaceus europaeus). Gastropods, pests to a variety of crops, on the other hand, were negatively affected by the presence of a grassy field margin, possibly due to a large amount of carabids in these fields. A variety of existing agri-environment schemes throughout Europe already include grassy field margins (e.g. Benton, 2007; Butler et al., 2007). An increased implementation of such schemes by landowners might therefore be beneficial to a number of macro-invertebrates and their predators (cf. Dennis and Fry, 1992). Acknowledgements We wish to thank the farmers who were so kind in permitting fieldwork on their land. We were also grateful for the help of fieldwork assistants Michael Bennett and Pieter Berends. The entire project was funded jointly by the People’s Trust of Endangered Species, the British Hedgehog Preservation Society and by a legacy of Dilys Breece, to whom we are greatly indebted. We would also like to thank two anonymous referees for their useful comments. References Asteraki, E.J., 1993. The potential of carabid beetles to control slugs in grass/clover swards. Entomophaga 38, 193–198. Asteraki, E.J., Hart, B.J., Ings, T.C., Manley, W.J., 2004. Factors influencing the plant and invertebrate diversity of arable field margins. Agric. Ecosyst. Environ. 102, 219–231. Australian Government, 2009. Caring for our Country—Environmental Stewardship. Available at: http://www.nrm.gov.au/stewardship/index.html (accessed December 2009). Baines, M., Hambler, C., Johnson, P.J., MacDonald, D.W., Smith, H., 1998. The effects of arable field margin management on the abundance and species richness of Araneae (Spiders). Ecography 21, 74–86. Benton, T.G., 2007. Managing farming’s footprint on biodiversity. Science 315, 341–342. Butler, S.J., Vickery, J.A., Norris, K., 2007. Farmland biodiversity and the footprint of agriculture. Science 315, 381–384. Chamberlain, D.E., Fuller, R.J., Bunce, R.G.H., Duckworth, J.C., Shrubb, M., 2000. Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales. J. Appl. Ecol. 37, 771–788. Clay, J., 2004. World Agriculture and The Environment: A Commodity-byCommodity Guide to Impacts and Practices. Island Press, Washington, DC. Curry, J.P., 1998. Factors affecting earthworm abundance in soils. In: Edwards, C.A. (Ed.), Earthworm Ecology. CRC Press LLC, Boca Raton, pp. 37–64. Dennis, P., Fry, G.L.A., 1992. Field margins: can they enhance natural enemy population densities and general arthropod diversity on farmland? Agric. Ecosyst. Environ. 40, 95–115. Donald, P.F., Green, R.E., Heath, M.F., 2001. Agricultural intensification and the collapse of Europe’s farmland bird populations. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 268, 25–29. European Commission, 2009. Agriculture and The Environment. Available at: (accessed http://ec.europa.eu/agriculture/envir/measures/index en.htm September 2009). Foley, J.A., DeFries, R., Asner, G.P., Barford, C., Bonan, G., Carpenter, S.R., Chapin, F.S., Coe, M.T., Daily, G.C., Gibbs, H.K., Helkowski, J.H., Holloway, T., Howard, E.A., Kucharik, C.J., Monfreda, C., Patz, J.A., Prentice, I.C., Navin Ramankutty, N., Snyder, P.K., 2005. Global consequences of land use. Science 309, 570–574.
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