- Email: [email protected]
Does hedgerow management on organic farms benefit small mammal populations?
Agriculture, Ecosystems and Environment 129 (2009) 124–130
Contents lists available at ScienceDirect
Agriculture, Ecosystems and Environment journal homepage: www.elsevier.com/locate/agee
Does hedgerow management on organic farms benefit small mammal populations? Felicity Siaˆn Bates *, Stephen Harris School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
A R T I C L E I N F O
A B S T R A C T
Article history: Received 24 November 2007 Received in revised form 31 July 2008 Accepted 5 August 2008 Available online 11 September 2008
Organic farming is a whole-farm management approach believed to encourage biodiversity by excluding the input of agrochemicals and introducing specific management regimes for non-crop habitats. We examined the impact of the hedgerow management regime encouraged for organic farms on small mammal populations, since small mammal numbers influence a range of species at higher trophic levels and, in particular, are key to the conservation of a range of mammalian and avian predators. We compared differences in management and structure of non-crop habitats at the farm-scale between organic and conventional farms, and used within-farm variations in hedgerow size to predict the effect of hedgerow size on small mammals on both farm types. There were no significant differences in the proportion of non-crop habitats between organic and conventional farms, although management differences produced larger hedgerows on organic farms and greater diversity of hedgerow growth stages. However, a difference in hedgerow size between the farm types did not have a significant effect on small mammal abundance or diversity. We conclude that increased hedgerow size is not benefiting small mammal populations on organic farms: significant gains in small mammal numbers may be more effectively achieved by increasing the area of non-crop habitats rather than by improving management regimes. ß 2008 Elsevier B.V. All rights reserved.
Keywords: Agricultural intensification Hedgerow management Agri-environment schemes Environmental Stewardship Apodemus sylvaticus Clethrionomys glareolus
1. Introduction Agricultural intensification in Britain since the 1940s has resulted in large increases in yields, although this process has led to an overall reduction in biodiversity in agricultural areas (Robinson and Sutherland, 2002), and the loss of key landscape features such as hedgerows (Barr and Gillespie, 2000). Whilst hedgerows play a critical role in maintaining agricultural biodiversity by providing habitats, refuges and corridors for large numbers of species (Burel, 1996), widespread hedgerow removal occurred between the 1960s and early 1990s, and there was an increasing trend to cut hedgerows much shorter and narrower (Newton, 2004). In the UK, financial support has been available for organic farming since 1994, most recently through a scheme run by the Department for Environment, Food and Rural Affairs (DEFRA), the Organic Entry Level of the Environmental Stewardship (ES) (DEFRA, 2002). The general consensus is that organic farming has, on average, a beneficial effect on biodiversity (Hole et al.,
* Corresponding author. Tel.: +44 1179 287593; fax: +44 1173 317985. E-mail address: [email protected] (F.S. Bates). 0167-8809/$ – see front matter ß 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2008.08.002
2005). Wickramasinghe et al. (2003) and Fuller et al. (2005) found increased bat activity on organic farms, but there have only been a few small-scale studies examining the benefits of organic agriculture for other mammals (Brown, 1999; Macdonald et al., 2007). Organic farming is a whole-system approach which aims to maintain a sustainable ecosystem, largely through replacing the use of agrochemicals by growing legumes and using crop rotations, animal manures and biological pest control (Lampkin, 1998). Whilst the exclusion of synthetic chemical inputs may contribute to increased biodiversity on organic farms, specific guidelines on the management of non-crop habitats (Soil Association, 2002) may also have significant benefits. For instance, the Soil Association prohibit the annual trimming of hedges, and encourages farmers to trim hedges in January and February, with each hedge cut every 2 or 3 years as part of a staggered cutting cycle, thereby increasing farm-scale diversity of hedgerow size and structure. Croxton and Sparks (2002) recommend a 3 year cutting cycle to benefit biodiversity by increasing the yield of hedgerow berries and more opportunities for shelter and nest sites for a range of species. Although several studies have shown that hedges are larger on organic than conventional farms (e.g. Fuller et al., 2005), and
F.S. Bates, S. Harris / Agriculture, Ecosystems and Environment 129 (2009) 124–130
hedgerow size may contribute to the increases in biodiversity on organic farms (Wickramasinghe et al., 2003), there has not been an intensive study of farm-scale differences in hedgerow size taking into account diversity of cutting stages and management practices. Small mammals on farmland are largely confined to areas of non-crop habitat and, therefore, are particularly vulnerable to agricultural intensification. In Britain, they represent an important prey source for around 20 species of mammals and birds (Harris et al., 2000), as well as influencing a range of biotic and abiotic environmental factors (e.g. Hayward and Phillipson, 1979). Many species of raptor have been negatively affected by prey declines associated with agricultural intensification (Tucker and Heath, 1994). Small mammal numbers have a significant impact on the breeding success of many avian and mammalian predators (e.g. Tapper, 1979; Percival, 1991), and so healthy small mammal populations are key to the conservation of many predators. The influence of hedgerow structure on numbers of farmland birds is well studied (Walker et al., 2005), yet there has been less research on the relationship between small mammals and field boundary characteristics. The bank vole Clethrionomys glareolus is largely restricted to non-crop habitats such as hedgerows, and may be negatively affected by characteristics such as the number of hedgerow gaps (Gelling et al., 2007). The wood mouse Apodemus sylvaticus utilises crop areas throughout the year, although hedgerows are the predominant over-wintering habitat (Todd et al., 2000), and Gelling et al. (2007) found hedgerow connectivity to be a positive predictive variable for this species. Hedgerow gaps also have a negative effect on the yellow-necked mouse Apodemus flavicollis, which prefers well-established hedges (Kotzageorgis and Mason, 1997). An increase in hedgerow size has the potential to benefit small mammals; wider hedges have a larger area of sheltered habitat at ground level, increasing the area for foraging, cover and shelter from predation and weather. A greater hedge surface area is likely to increase yields of the seeds or fruits which provide a food source for granivorous small mammals, particularly where increased hedgerow size is due to less frequent hedge trimming (Croxton and Sparks, 2002). Hedgerows on existing organic farms provide a good model for the management regimes to be introduced on both organic and conventional farms under the ES. This scheme aims to increase
125
biodiversity, including birds, mammals, butterflies and bees, by improving the management of field margins, set-aside and hedgerows, with an increase in hedge size and decrease in cutting frequency (DEFRA, 2005). We used a matched-pairs design to compare non-crop habitats on organic and conventional farms at the farm-scale and to link these habitat differences with small mammal abundance at the hedgerow-scale. To determine whether the larger hedges found on organic farms benefit small mammal populations, we compared small mammal numbers in hedgerows of different size on both farm types. The aims of the study were (i) to compare the structure and management of the non-crop habitats on organic and conventional farms; (ii) to compare the abundance and diversity of small mammals along hedgerows of different size on both farm types; and (iii) to determine whether a difference in hedgerow size of the magnitude found between farm types has an effect on small mammal numbers and diversity. 2. Methods 2.1. Study region The study was carried out in southwest England and southeast Wales, a ‘complex agricultural landscape’ with a mild climate dominated by grassland (Gibson et al., 2007). Over the last 20 years there has been a decline in the area of cereal crops and an increase in oilseed rape, linseed and maize. Soils in the study area are predominantly lime-rich or loamy and clayey. Average annual rainfall is 719.0 mm, with average rainfall in June and December of 58.5 and 77.4 mm, respectively. The average annual maximum temperature is 13.3 8C and the maximum temperatures in June and December are 18.5 and 7.4 8C, respectively (Met Office, 2007). 2.2. Farm-scale habitat surveys Habitat surveys were undertaken in 2005 on 15 pairs of farms (Fig. 1). Fifteen organic farms which had completed a ‘conversion’ period of 2 years organic management and a minimum of one additional year post-conversion were selected at random from a list of certified organic producers provided by the Soil Association and paired with conventional farms of the same land use type
Fig. 1. Map of paired farm sites used in farm-scale habitat surveys. The circles around farm pairs are 5 km in diameter. Open symbols represent farms where small mammal surveys were also carried out.
126
F.S. Bates, S. Harris / Agriculture, Ecosystems and Environment 129 (2009) 124–130
(arable only, pastoral only or mixed) within 5 km to standardize for geographical variation; farms were also matched for topography and elevation. Thirteen farm pairs were mixed, with beef, dairy and/or sheep herds, and one or more arable crops. One pair was arable only, one pair livestock only. Data were collected on management of non-crop habitats. Phase 1 habitat surveys (Nature Conservancy Council, 1990) were undertaken by one surveyor between January and June 2005 on whole farms up to 200 ha; farm buildings, yards and gardens were not included in area calculations. On larger farms, 200 ha was randomly selected from grid squares covering the main farm block. For farms with more than one farm block, where the main block was <200 ha, proportions of two blocks were randomly selected. Farm pairs were surveyed on consecutive days to avoid the effect of season. During the Phase 1 surveys all fields and field boundaries were mapped. Fields were either a crop or non-crop habitat. Set-aside, i.e. arable land removed from production for one cropping season or longer, was classified as non-crop, whereas crop habitats were either grassland (improved or unimproved pasture, grass leys) or land in arable rotation (cropped, harvested, ploughed). Other noncrop habitats were hedgerow, woodland and non-cropped arable margins. A hedgerow was defined as a more or less continuous line of woody vegetation <4.5 m high managed to maintain a linear shape (Barr and Gillespie, 2000). A continuous line of woody vegetation with an average height >4.5 m and dominated by woody stems at the base was classed as a treeline. A hedgerow was classified as ‘cut’ if there was evidence of a horizontal and/or vertical cut carried out within the current cutting season, or ‘uncut’. Hedge height and width were measured, at 50 m intervals, to the nearest 0.25 m, including both the basic woody framework of the hedge, and any substantial recent growth (very sparse new growth of a small number of shoots was excluded). All shrub species within 2 m either side of the data collection point recorded. The ‘quality’ of each hedgerow was assessed as the percentage of gaps along the total length (0, 5, 10, 20, 40 and >40%), because the frequency of hedgerow gaps has been shown to affect A. flavicollis and C. glareolus (Kotzageorgis and Mason, 1997). The number and size of hedgerow trees were recorded (10–40 cm diameter breast height (dbh) or >40 cm dbh), as standard trees within hedgerows can benefit granivorous species, including A. sylvaticus (Montgomery and Dowie, 1993). Areas of woodland, including established areas of trees and new plantations >0.005 ha, were mapped. Arable field margins were defined as an uncultivated area >0.5 m between the field boundary and the cultivated area. The width of uncropped arable field margins was measured to the nearest 0.25 m every 50 m along the field boundary. Georeferenced tiles of the study sites derived from digitized Ordnance Survey maps (http://digimap.edina.ac.uk) were put into Arcview version 3.2 and Arcview Spatial Analyst, Environmental Systems Research Institute, California, USA and used to calculate farm and field areas and the length of hedgerows.
hedgerows were matched per farm, one small and one large hedge, thus controlling for farm type and other between-farm management differences, such as time since conversion of organic farms. Large hedgerows selected were a minimum of 35% taller and/or 35% wider, with a cross-sectional area 35% greater than the paired small hedges, based on the average size difference we found between organic and conventional farms. Members of the pair were matched for other variables which may affect small mammal populations, for both sides of the hedge and the adjacent land. Hedgerows were matched for equal shrub species composition. Since species such as hawthorn Crataegus monogyna and hazel Corylus avellana may directly influence granivorous species, it was important to isolate the effect of increases in the volume of particular shrubs as hedge cross-sectional area increases from the effect of composition of shrub species along the hedge. Land use and crop type were matched since neighbouring land use (pasture or arable) can affect species such as A. sylvaticus (Montgomery and Dowie, 1993). The percentage live ground vegetation cover was measured because hedge-base ground cover is important, especially for C. glareolus. Where adjacent land was arable, margin width was matched; increased margin width has been shown to benefit C. glareolus and Sorex araneus (Shore et al., 2005). Flailing has been shown to have a negative effect on bank vole density and a positive effect on the density of field voles Microtus agrestis (Gelling et al., 2007), and so both members of a pair were cut or uncut. There was a size difference in the basic woody framework of two members of a pair, as well as total size including any recent growth. A maximum difference of 908 orientation was accepted within hedgerow pairs. A 100 m transect with <5% gaps was selected on each hedgerow with no hedgerow trees. Eight hedgerow pairs were adjacent to pastoral land only; two pairs adjacent to arable land. Hedge height and width were measured to the nearest 0.25 m at three points along the transect. To confirm that pairs were matched rigorously, ground vegetation cover (live ground flora and shrubs) at the hedge-base was estimated qualitatively to the nearest 10% within three 0.5 m 0.5 m squares along the hedgerow; shrub density 1 m from ground level was measured as a qualitative assessment of visibility through the hedge to the nearest 10% (whereby 100% represented zero visibility through the hedge, i.e. high density vegetation). Longworth trapping (Gurnell and Flowerdew, 1994) was carried out between August and December 2005, with two traps every 5 m along the transect on one side of the hedge, i.e. 42 traps per hedge, 84 traps per hedgerow pair per night; each pair of hedgerows was trapped simultaneously. Traps were baited with blow-fly pupae, crushed oats and carrot, with hay for bedding, and treadle weights set for 2 g to facilitate capture of juvenile rodents and shrews. Traps were left in place for three nights, set at dusk and checked at dawn; they were closed during the day. All captures were identified to species, weighed, sexed, aged (juvenile, adult) and fur-clipped on the left or right to identify recaptures from days 1 and/or 2, respectively.
2.3. Small mammal surveys
2.4. Data analysis
Small mammal surveys were conducted on a subset of five organic and five conventional farms which were not treated as farm pairs. A paired design was used at the scale of matched hedgerows to examine the effect of a difference in hedgerow size. To maintain a high standard of pairing, only farms where it was possible to match a pair of hedgerows closely were included. The matched-pairs design aims to exclude the effect of confounding variables including landscape variables, aspects of farming system, e.g. agrochemical inputs, as well as the time of season. Two
Hedge cross-sectional area was calculated as average height by average width, hedgerow area as average width by total length. For the analysis of the farm-scale habitat data, each farm was treated as the sample unit; farm averages were calculated for variables measured multiple times, e.g. hedgerow height, number of hedgerow trees per hedge. The area and structure of non-crop habitats were analyzed using a multivariate repeated measures general linear model (MANOVA) in SPSS 12.0, SPSS Inc., with farm type (organic or conventional) as treatment factors (see Gibson
F.S. Bates, S. Harris / Agriculture, Ecosystems and Environment 129 (2009) 124–130
et al., 2007). Where appropriate, related variables, e.g. hedge width, height and cross-sectional area, were analyzed together in a single test to reduce the risk of Type 1 errors. Variables considered unrelated to other dependent variables, e.g. number of hedgerow shrub species, were analyzed in a univariate repeated measure general linear model. Data were transformed where necessary to achieve normality of the residuals. Diversity indices were arc sine square root transformed prior to analysis. All figures quoted are untransformed means S.E. Small mammal abundance was the total number of individuals captured, excluding recaptures, and species richness the number of species captured. We calculated small mammal species diversity using the Shannon index (H0 ), the Shannon evenness measure (J) (Michel et al., 2006), Simpson’s index (D) and Simpson’s measure of evenness (1/D); the latter two measures take into account species dominance (Magurran, 2004). The effect of hedgerow size on small mammal numbers was analyzed using a repeated measures MANOVA. Related dependent variables, such as total small mammal abundance and the abundance of the three most common species, were analyzed in the same test. 3. Results 3.1. Farm-scale differences in the structure and management of noncrop habitats
127
their hedgerows on a yearly cycle. A higher proportion of organic than conventional farmers staggered the cutting over 2 or more years. Consequently, a significantly greater area of hedgerow was uncut on organic than conventional farms (F1,14 = 18.448, P = 0.001), leading to a significant difference in hedgerow size between farm types (Table 2); hedgerows on organic farms were significantly taller and had a greater cross-sectional area than those on conventional farms but were not significantly wider on organic than conventional farms. There was no difference in shrub species richness or in the number of trees in organic and conventional hedgerows. A higher proportion of organic than conventional farmers had carried out hedgerow planting, either to establish new hedgerows or to fill in gaps within existing low quality hedgerows (8 and 2 of 15 farmers, respectively). However, there was no significant difference in the proportion of farm area occupied by hedgerows of different quality (Table 2). Non-cropped arable margins tended to be wider on organic (3.0 0.61 m) than conventional farms (2.2 0.64 m) but this difference was not significant (F1,12 = 3.093, P = 0.104). When pairs including one or more farms involved in another Agri-Environment Scheme (AES) were excluded, no significant difference was found between margin width on organic (3.4 0.45 m) and conventional (1.4 0.03 m) farms (F1,5 = 0.592, P = 0.476). 3.2. Effect of hedgerow size on small mammal abundance
Organic farms had completed conversion 4.3 0.5 years prior to the study. Organic hedgerow management regimes were also implemented during the 2 year conversion period prior to certification. There was no significant difference in either the total size of organic (145 27.5 ha) and conventional farms (155.5 25.4 ha) selected (F1,14 = 0.321, P = 0.580) or the area included in the farmscale surveys: 124.8 14.4 and 130.4 15.6 ha, respectively (F1,14 = 0.342, P = 0.568). There was a significant difference in the area occupied by different landscape elements between farm types (Table 1 and Fig. 2). The percentage area of arable land was higher on conventional than organic farms, whereas the area of grass was significantly greater on organic farms. Uncut hedgerows formed a larger area of organic than conventional farms. Although conventional farms had a larger area of cut hedgerows, there was no difference in percentage area occupied by all hedgerows (cut and uncut) between farm types. Nor was there any difference between farm types in the percentage area of woodland or total area of noncrop elements (hedgerow, woodland and set-aside). Fourteen out of 15 organic farmers cut their hedges at intervals of 2 or more years, whereas 11 of 15 conventional farmers cut all Table 1 Proportion of crop and non-crop habitats on 15 pairs of organic and conventional farms Habitat
Grass fields Arable fields Set-aside All hedgerow Uncut hedgerow Cut hedgerow Woodland Total non-crop habitat
Mean percentage area (S.E.) Organic farms
Conventional farms
64.4 27.2 2.4 1.1 0.7 0.4 4.8 8.4
50.0 40.9 2.2 1.1 0.2 0.9 3.8 9.1
(6.6) (5.2) (2.3) (0.2) (0.1) (0.1) (1.2) (2.4)
(7.4) (6.8) (3.4) (0.2) (0.1) (0.2) (1.5) (2.4)
F1,14
8.652 8.731 N/A 0.351 16.254 8.799 1.346 0.063
P
0.011* 0.010* 0.563 0.001* 0.010* 0.265 0.806
Percentages represent proportion of total farm area. Prior to analysis, the percentage of woodland and total non-crop habitat were log10 transformed; the percentage of uncut and cut hedgerow were x3 transformed. Total non-crop habitat includes set-aside, hedgerow and woodland. N/A: data were not included in statistical analysis due to zeros in the data set. * P < 0.05.
Hedgerows were paired for a difference in size; a repeated measures MANOVA confirmed a significant difference in hedgerow size within the pairs. ‘Large’ hedgerows were significantly greater in height (2.7 0.31 m), width (2.5 0.22 m) and cross-sectional area (7.11 1.42 m2) than ‘small’ hedgerows (height, 1.8 0.71 m, width 1.76 0.15 m, cross-sectional area 3.34 0.54 m2) (height, F1,9 = 23.840, P = 0.001; width, F1,9 = 13.658, P = 0.005; cross-sectional area, F1,9 = 66.869, P < 0.001). Hedge-base ground cover and hedgerow shrub density were matched when selecting sites, and there was no significant difference in ground cover between large (64.0 5.06%) and small hedgerows (57.7 3.0%) or in the mean shrub density of large (83.3 4.01%) and small (81.3 3.38%)
Table 2 Differences in hedgerow characteristics on 15 pairs of organic and conventional farms Hedge variable
Mean (S.E.)
F1,14
P
Organic farms
Conventional farms
2.00 (0.02) 1.80 (0.01) 3.70 (0.05)
1.63 (0.01) 1.60 (0.01) 2.70 (0.03)
13.047 2.916 8.781
0.030* 0.110 0.010*
Shrub species per 100 m Trees per 100 m (10–40 cm dbh) Trees per 100 m (>40 cm dbh)
7.70 (0.03) 0.14 (0.001)
7.50 (0.03) 0.11 (0.001)
0.094 0.018
0.764 0.210
0.13 (0.001)
0.10 (0.001)
0.894
0.654
Area hedge (0–5% gaps) (m2) Area hedge (10–20% gaps) (m2) Area hedge (>40% gaps) (m2)
0.76 (0.11)
0.78 (0.16)
0.047
0.831
0.31 (0.16)
0.24 (0.03)
0.452
0.512
0.07 (0.01)
0.05 (0.01)
2.332
0.149
Hedge Hedge Hedge area
height (m) width (m) cross-sectional (m2)
Data for hedgerow size, hedgerow quality, and hedgerow shrubs and trees were analyzed in three separate repeated measures MANOVAs. Prior to analysis, hedge height, cross-sectional area and trees per 100 m were log10 transformed. All hedge area variables were square root transformed. * P < 0.05.
F.S. Bates, S. Harris / Agriculture, Ecosystems and Environment 129 (2009) 124–130
128
Fig. 2. Proportion of area occupied by different landscape elements on (a) organic and (b) conventional farms.
hedgerows (cover, F1,9 = 2.212, P = 0.171; density, F1,9 = 0.288, P = 0.604). We had 584 captures of 359 different small mammals (four rodents—A. flavicollis, A. sylvaticus, C. glareolus and M. agrestris, and three shrews—water shrew Neomys fodiens, common shrew S. Table 3 Small mammals trapped in small and large hedges Species
Number of individuals (%) Small hedges
Yellow-necked mouse Apodemus flavicollis Wood mouse Apodemus sylvaticus Bank vole Clethrionomys glareolus Field vole Microtus agrestris Water shrew Neomys fodiens Common shrew Sorex araneus Pygmy shrew Sorex minutus Total number
9 (5.2)
Large hedges 13 (7.0)
All hedges
62 (33.5)
115 (32.0)
47 (27.0)
45 (24.3)
92 (25.6)
8 (4.6)
3 (1.6)
2 (1.1)
0 (0)
11 (3.1) 2 (0.6)
47 (27.0)
55 (29.7)
102 (28.4)
8 (4.6)
7 (3.8)
15 (4.2)
185
Table 4 Abundance of small mammals along small and large hedges Species
22 (6.1)
53 (30.5)
174
araneus and pygmy shrew Sorex minutus) in 2520 trap nights (Table 3). There was no significant difference in the abundance of small mammals along large and small hedgerows (Table 4). Hedgerow size had no effect on species richness or species diversity (Table 5). Nor was there a significant interaction between hedgerow size and farm type on either abundance or diversity of small mammals (Tables 4 and 5).
359
Number of individuals excludes recaptures; figures in parentheses are percentages.
Hedge size All species Apodemus sylvaticus Clethrionomys glareolus Sorex araneus Hedge size farm type All species Apodemus sylvaticus Clethrionomys glareolus Sorex araneus
Mean (S.E.) Small hedges
Large hedges
17.4 5.3 4.7 4.7
18.5 6.2 4.5 5.5
(2.19) (1.05) (1.19) (1.44)
(2.28) (0.95) (1.27) (1.06)
F1,8
P
0.129 0.326 0.064 0.561
0.728 0.584 0.807 0.748
0.001 1.775 0.420 0.035
0.975 0.220 0.535 0.856
Data for abundance of C. glareolus were log10 transformed prior to analysis. Total abundance and the abundance of the three most common species were analyzed using a repeated measures MANOVA, with farm type included as a between subjects factor.
F.S. Bates, S. Harris / Agriculture, Ecosystems and Environment 129 (2009) 124–130 Table 5 Small mammal species richness and diversity in small and large hedges Diversity measure
Hedge size Number of species Shannon H0 Shannon J Simpson D Simpson 1/D
Mean (S.E.) Small hedges
Large hedges
3.80 0.45 0.76 0.39 2.95
3.90 0.50 0.86 0.33 3.25
(0.25) (0.05) (0.09) (0.07) (0.28)
(0.43) (0.03) (0.04) (0.03) (0.25)
Hedge size farm type Number of species Shannon H0 Shannon J Simpson D Simpson 1/D
F1,8
P
0.030 0.227 1.845 0.401 0.379
0.866 0.646 0.211 0.544 0.555
0.758 0.215 0.383 0.027 0.046
0.409 0.656 0.553 0.875 0.836
Before analysis, Shannon H0 and Shannon J were x2 transformed, Simpson D was x2 transformed. Data were analyzed using a repeated measures MANOVA, with farm type included as a between subjects factor.
4. Discussion A large number of studies have shown higher abundance and diversity of a range of species on organic farms (Hole et al., 2005), but further work is needed to establish the relative contribution of farming system (e.g. level of agrochemical use) and landscape structure (Chamberlain et al., 1999) to this difference. Our study confirms farm-scale differences exist in the size and structure of hedgerow habitats between farm types, as a result of differences in annual management. These differences may be important in increasing biodiversity on organic farms but do not benefit all species. 4.1. Effect of hedgerow size on small mammals We predicted that the difference in hedgerow size between organic and conventional farms would have a significant effect on small mammal populations due to an increase in area for foraging and shelter, and potential increase in food sources. Whereas previous studies suggest that hedgerow size may influence small mammal numbers, the majority relied on samples from a limited number of farms (e.g. Kotzageorgis and Mason, 1997). Gelling et al. (2007) found that hedgerow connectivity was a positive predictor of A. sylvaticus, and that hedgerow width was a strong positive predictor of small mammal biomass. Pocock and Jennings (2008) used a matched-pairs design to assess the response of insectivorous mammals, including shrews, to other aspects of agricultural intensification, but to our knowledge there has not been a study using the matched-pairs design to isolate the effect of individual non-crop habitat variables on small mammals. Our results suggest that a difference in hedgerow size, comparable to that seen between organic and conventional farms, does not have a significant effect on small mammal populations. Tattersall et al. (2002) found no effect of the linearity of set-aside and hedgerow habitats on the abundance of A. sylvaticus, M. agrestris or S. araneus, or on small mammal diversity. Shore et al. (2005) found that the impact of field margin management under the ES varied between species. The abundance of A. sylvaticus did not differ between narrow margins and wider margins, although higher numbers of both C. glareolus and S. araneus were found on the ES-style grassy margins in autumn. 4.2. Small mammals on organic farms Hitherto, the vast majority of studies into the importance of hedgerows for small mammals have been carried out on
129
conventional farms, although a few small-scale studies suggest that aspects of organic agriculture may benefit small mammal populations; Macdonald et al. (2007), for instance, suggested that there is a difference in A. sylvaticus populations between organic and conventional farms, and Brown (1999) found increased activity levels of A. sylvaticus, C. glareolus and S. araneus in organic compared to conventional fields. However, Pocock and Jennings (2008) found that shrews were relatively insensitive to higher levels of agrochemical inputs, suggesting that exclusion of agrochemicals on organic farms does not benefit these species. Our study aimed to quantify the effect of a specific aspect of habitat management on organic farms, but further research is necessary into the effect of the organic farming system on all small mammal species, particularly to isolate the relative effects of agrochemical inputs and other aspects of farming system from the influence of habitat management. 4.3. Implications of the ES for hedgerow management The introduction of the ES since this study is likely to reduce variation in existing management practices between conventional and organic farms. Management prescriptions include maintaining hedge height to 1.5 m and above, or 2 m and above and cutting each hedge no more than once every 2 years with a staggered cutting regime (DEFRA, 2005). ‘Enhanced hedgerow management’ options include cutting no more than a third of all hedges per year, further increasing the variety of hedgerow cutting stages across the farm. Consequently, there will be an increase in the area of uncut hedgerows, particularly on conventional farms, contributing to an overall increase in hedge size, particularly where hedgerows were previously managed more intensively. Whilst the ES is expected to have an effect, predominantly beneficial, on taxa such as invertebrates and birds, Whittingham (2007) emphasizes the importance of monitoring the effects of an AES to ensure that the scheme’s prescriptions meet the needs of a greater range of species. It is important to understand the factors that will increase small mammal abundance, since this will have a significant impact upon predator populations (Love et al., 2000), as well as a range of ecosystem processes (Hayward and Phillipson, 1979). Our study suggests that increases in hedgerow size under the ES may have little or no effect on small mammal numbers. It may be more effective to place higher emphasis on increasing the area covered by hedgerows, through hedgerow planting and repair, than by prescribed management of existing hedgerows. Pocock and Jennings (2008) demonstrate the strong effect of boundary loss on shrew abundance and suggest that replanting of hedgerows will benefit these species. More research is needed into the use of planted hedgerows by small mammals, and it will also be important to examine the effect of a widespread shift from annual cutting to a 2 or 3 yearly staggered cut under the ES on small mammal populations, although the benefits of this may only be clear after a number of cutting cycles. 5. Conclusions We confirm that farm-scale differences in hedgerow size and management exist between organic and conventional farms, and examined the effect of this size difference on small mammal numbers in organic and conventional hedgerows. We focused on this group since small mammal populations influence a diversity of species at higher trophic levels, as well as a range of biotic and abiotic environmental factors. Thus increasing small mammal populations on farmland is crucial to improving the biodiversity of agricultural ecosystems. We show that increased hedgerow size on organic farms is not benefitting small mammals. Significant
130
F.S. Bates, S. Harris / Agriculture, Ecosystems and Environment 129 (2009) 124–130
population gains may be more effectively achieved by increasing the area of non-crop habitats. Acknowledgements We thank Paul Craze, Nancy Jennings and Michael Pocock for their advice, the volunteers who assisted with the field work, particularly Giles Manning and Phillip Paterson, the landowners for permission to work on their land and the Dulverton Trust for funding. References Barr, C.J., Gillespie, M.K., 2000. Estimating hedgerow length and pattern characteristics in Great Britain using Countryside Survey data. J. Environ. Manage. 60, 23–32. Brown, R.W., 1999. Margin/field interfaces and small mammals. Aspects Appl. Biol. 54, 203–206. Burel, F., 1996. Hedgerows and their role in agricultural landscapes. Crit. Rev. Plant Sci. 15, 169–190. Chamberlain, D.E., Wilson, J.D., Fuller, R.J., 1999. A comparison of bird populations on organic and conventional farm systems in southern Britain. Biol. Conserv. 88, 307–320. Croxton, P.J., Sparks, T.H., 2002. A farm-scale evaluation of the influence of hedgerow cutting frequency on hawthorn (Crataegus monogyna) berry yields. Agr. Ecosyst. Environ. 93, 437–439. DEFRA, 2002. Economic Evaluation of the Organic Farming Scheme. Department for Environment, Food and Rural Affairs, http://statistics.defra.gov.uk/esg/evaluation/organic/finalrep.pdf. DEFRA, 2005. Entry Level Stewardship Handbook. Department for Environment, Food and Rural Affairs, http://www.defra.gov.uk/erdp/pdfs/es/els-handbook.pdf. Fuller, R.J., Norton, L.R., Feber, R.E., Johnson, P.J., Chamberlain, D.E., Joys, A.C., Mathews, F., Stuart, R.C., Townsend, M.C., Manley, W.J., Wolfe, M.S., Macdonald, D.W., Firbank, L.G., 2005. Benefits of organic farming to biodiversity vary among taxa. Biol. Lett. 1, 431–434. Gelling, M., Macdonald, D.W., Mathews, F., 2007. Are hedgerows the route to increased farmland small mammal density? Use of hedgerows in British pastoral habitats. Landscape Ecol. 22, 1019–1032. Gibson, R.H., Pearce, S., Morris, R.J., Symondson, W.O.C., Memmott, J., 2007. Plant diversity and land use under organic and conventional agriculture: a wholefarm approach. J. Appl. Ecol. 44, 792–803. Gurnell, J., Flowerdew, J.R., 1994. Live Trapping Small Mammals—A Practical Guide, 3rd ed. The Mammal Society, London. Harris, S., McLaren, G., Morris, M., Morris, P.A., Yalden, D., 2000. Abundance/mass relationships as a quantified basis for establishing mammal conservation priorities. In: Entwhistle, A., Dunstone, N. (Eds.), Priorities for the Conservation of Mammalian Biodiversity: Has the Panda had its Day? Cambridge University Press, Cambridge, pp. 101–117. Hayward, G.F., Phillipson, J., 1979. Community structure and functional role of small mammals in ecosystems. In: Stoddart, D.M. (Ed.), Ecology of Small Mammals. Chapman and Hall, London, pp. 135–211.
Hole, D.G., Perkins, A.J., Wilson, J.D., Alexander, I.H., Grice, P.V., Evans, A.D., 2005. Does organic farming benefit biodiversity? Biol. Conserv. 122, 113–130. Kotzageorgis, G.C., Mason, C.F., 1997. Small mammal populations in relation to hedgerow structure in an arable landscape. J. Zool. 242, 425–434. Lampkin, N., 1998. Organic Farming, 3rd ed. Old Pond, Ipswich. Love, R., Webbon, C., Glue, D.E., Harris, S., 2000. Changes in the food of British barn owls (Tyto alba) between 1974 and 1997. Mammal Rev. 30, 107–129. Macdonald, D.W., Tattersall, F.H., Service, K.M., Firbank, L.G., Feber, R.E., 2007. Mammals, agri-environment schemes and set-aside—what are the putative benefits? Mammal Rev. 37, 259–277. Magurran, A.E., 2004. Measuring Biological Diversity. Blackwell Publishing, Oxford. Met Office, 2007. UK Climate and Weather Statistics. The Met Office, http:// www.metoffice.gov.uk/climate/uk/. Michel, N., Burel, F., Butet, A., 2006. How does landscape use influence small mammal diversity, abundance and biomass in hedgerow networks of farming landscapes? Acta Oecol. 30, 11–20. Montgomery, W.I., Dowie, M., 1993. The distribution and population regulation of the wood mouse Apodemus sylvaticus on field boundaries of pastoral farmland. J. Appl. Ecol. 30, 783–791. Nature Conservancy Council, 1990. Handbook for Phase 1 Habitat Survey—A Technique for Environmental Audit. Field manual. Joint Nature Conservancy Council, Peterborough. Newton, I., 2004. The recent declines of farmland bird populations in Britain: an appraisal of causal factors and conservation actions. Ibis 146, 579–600. Percival, S., 1991. Population trends in British barn owls. Br. Wildl. 2, 131–140. Pocock, M.J.O., Jennings, N., 2008. Testing biotic indicator taxa: the sensitivity of insectivorous mammals and their prey to the intensification of lowland agriculture. J. Appl. Ecol. 45, 151–160. Robinson, R.A., Sutherland, W.J., 2002. Post-war changes in arable farming and biodiversity in Great Britain. J. Appl. Ecol. 39, 157–176. Shore, R.F., Meek, W.R., Sparks, T.H., Pywell, R.F., Nowakowski, M., 2005. Will Environmental Stewardship enhance small mammal abundance on intensively managed farmland? Mammal Rev. 35, 277–284. Soil Association, 2002. Soil Association Organic Standards and Certification (revision 14 2002/03). Soil Association, Bristol. Tapper, S., 1979. The effect of fluctuating vole numbers (Microtus agrestis) on a population of weasels (Mustela nivalis) on farmland. J. Anim. Ecol. 48, 603– 617. Tattersall, F.H., Macdonald, D.W., Hart, B.J., Johnson, P., Manley, W., Feber, R., 2002. Is habitat linearity important for small mammal communities on farmland? J. Appl. Ecol. 39, 643–652. Todd, I.A., Tew, T.E., Macdonald, D.W., 2000. Arable habitat use by wood mice (Apodemus sylvaticus). 1. Macrohabitat. J. Zool. 250, 299–303. Tucker, G.M., Heath, M.F., 1994. Birds in Europe: Their Conservation Status. Birdlife International, Cambridge. Walker, M.P., Dover, J.W., Hinsley, S.A., Sparks, T.H., 2005. Birds and green lanes: breeding season bird abundance, territories and species richness. Biol. Conserv. 126, 540–547. Whittingham, M.J., 2007. Will agri-environment schemes deliver substantial biodiversity gain, and if not why not? J. Appl. Ecol. 44, 1–5. Wickramasinghe, L.P., Harris, S., Jones, G., Vaughan, N., 2003. Bat activity and species richness on organic and conventional farms: impact of agricultural intensification. J. Appl. Ecol. 40, 984–993.
Contents lists available at ScienceDirect
Agriculture, Ecosystems and Environment journal homepage: www.elsevier.com/locate/agee
Does hedgerow management on organic farms benefit small mammal populations? Felicity Siaˆn Bates *, Stephen Harris School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
A R T I C L E I N F O
A B S T R A C T
Article history: Received 24 November 2007 Received in revised form 31 July 2008 Accepted 5 August 2008 Available online 11 September 2008
Organic farming is a whole-farm management approach believed to encourage biodiversity by excluding the input of agrochemicals and introducing specific management regimes for non-crop habitats. We examined the impact of the hedgerow management regime encouraged for organic farms on small mammal populations, since small mammal numbers influence a range of species at higher trophic levels and, in particular, are key to the conservation of a range of mammalian and avian predators. We compared differences in management and structure of non-crop habitats at the farm-scale between organic and conventional farms, and used within-farm variations in hedgerow size to predict the effect of hedgerow size on small mammals on both farm types. There were no significant differences in the proportion of non-crop habitats between organic and conventional farms, although management differences produced larger hedgerows on organic farms and greater diversity of hedgerow growth stages. However, a difference in hedgerow size between the farm types did not have a significant effect on small mammal abundance or diversity. We conclude that increased hedgerow size is not benefiting small mammal populations on organic farms: significant gains in small mammal numbers may be more effectively achieved by increasing the area of non-crop habitats rather than by improving management regimes. ß 2008 Elsevier B.V. All rights reserved.
Keywords: Agricultural intensification Hedgerow management Agri-environment schemes Environmental Stewardship Apodemus sylvaticus Clethrionomys glareolus
1. Introduction Agricultural intensification in Britain since the 1940s has resulted in large increases in yields, although this process has led to an overall reduction in biodiversity in agricultural areas (Robinson and Sutherland, 2002), and the loss of key landscape features such as hedgerows (Barr and Gillespie, 2000). Whilst hedgerows play a critical role in maintaining agricultural biodiversity by providing habitats, refuges and corridors for large numbers of species (Burel, 1996), widespread hedgerow removal occurred between the 1960s and early 1990s, and there was an increasing trend to cut hedgerows much shorter and narrower (Newton, 2004). In the UK, financial support has been available for organic farming since 1994, most recently through a scheme run by the Department for Environment, Food and Rural Affairs (DEFRA), the Organic Entry Level of the Environmental Stewardship (ES) (DEFRA, 2002). The general consensus is that organic farming has, on average, a beneficial effect on biodiversity (Hole et al.,
* Corresponding author. Tel.: +44 1179 287593; fax: +44 1173 317985. E-mail address: [email protected] (F.S. Bates). 0167-8809/$ – see front matter ß 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2008.08.002
2005). Wickramasinghe et al. (2003) and Fuller et al. (2005) found increased bat activity on organic farms, but there have only been a few small-scale studies examining the benefits of organic agriculture for other mammals (Brown, 1999; Macdonald et al., 2007). Organic farming is a whole-system approach which aims to maintain a sustainable ecosystem, largely through replacing the use of agrochemicals by growing legumes and using crop rotations, animal manures and biological pest control (Lampkin, 1998). Whilst the exclusion of synthetic chemical inputs may contribute to increased biodiversity on organic farms, specific guidelines on the management of non-crop habitats (Soil Association, 2002) may also have significant benefits. For instance, the Soil Association prohibit the annual trimming of hedges, and encourages farmers to trim hedges in January and February, with each hedge cut every 2 or 3 years as part of a staggered cutting cycle, thereby increasing farm-scale diversity of hedgerow size and structure. Croxton and Sparks (2002) recommend a 3 year cutting cycle to benefit biodiversity by increasing the yield of hedgerow berries and more opportunities for shelter and nest sites for a range of species. Although several studies have shown that hedges are larger on organic than conventional farms (e.g. Fuller et al., 2005), and
F.S. Bates, S. Harris / Agriculture, Ecosystems and Environment 129 (2009) 124–130
hedgerow size may contribute to the increases in biodiversity on organic farms (Wickramasinghe et al., 2003), there has not been an intensive study of farm-scale differences in hedgerow size taking into account diversity of cutting stages and management practices. Small mammals on farmland are largely confined to areas of non-crop habitat and, therefore, are particularly vulnerable to agricultural intensification. In Britain, they represent an important prey source for around 20 species of mammals and birds (Harris et al., 2000), as well as influencing a range of biotic and abiotic environmental factors (e.g. Hayward and Phillipson, 1979). Many species of raptor have been negatively affected by prey declines associated with agricultural intensification (Tucker and Heath, 1994). Small mammal numbers have a significant impact on the breeding success of many avian and mammalian predators (e.g. Tapper, 1979; Percival, 1991), and so healthy small mammal populations are key to the conservation of many predators. The influence of hedgerow structure on numbers of farmland birds is well studied (Walker et al., 2005), yet there has been less research on the relationship between small mammals and field boundary characteristics. The bank vole Clethrionomys glareolus is largely restricted to non-crop habitats such as hedgerows, and may be negatively affected by characteristics such as the number of hedgerow gaps (Gelling et al., 2007). The wood mouse Apodemus sylvaticus utilises crop areas throughout the year, although hedgerows are the predominant over-wintering habitat (Todd et al., 2000), and Gelling et al. (2007) found hedgerow connectivity to be a positive predictive variable for this species. Hedgerow gaps also have a negative effect on the yellow-necked mouse Apodemus flavicollis, which prefers well-established hedges (Kotzageorgis and Mason, 1997). An increase in hedgerow size has the potential to benefit small mammals; wider hedges have a larger area of sheltered habitat at ground level, increasing the area for foraging, cover and shelter from predation and weather. A greater hedge surface area is likely to increase yields of the seeds or fruits which provide a food source for granivorous small mammals, particularly where increased hedgerow size is due to less frequent hedge trimming (Croxton and Sparks, 2002). Hedgerows on existing organic farms provide a good model for the management regimes to be introduced on both organic and conventional farms under the ES. This scheme aims to increase
125
biodiversity, including birds, mammals, butterflies and bees, by improving the management of field margins, set-aside and hedgerows, with an increase in hedge size and decrease in cutting frequency (DEFRA, 2005). We used a matched-pairs design to compare non-crop habitats on organic and conventional farms at the farm-scale and to link these habitat differences with small mammal abundance at the hedgerow-scale. To determine whether the larger hedges found on organic farms benefit small mammal populations, we compared small mammal numbers in hedgerows of different size on both farm types. The aims of the study were (i) to compare the structure and management of the non-crop habitats on organic and conventional farms; (ii) to compare the abundance and diversity of small mammals along hedgerows of different size on both farm types; and (iii) to determine whether a difference in hedgerow size of the magnitude found between farm types has an effect on small mammal numbers and diversity. 2. Methods 2.1. Study region The study was carried out in southwest England and southeast Wales, a ‘complex agricultural landscape’ with a mild climate dominated by grassland (Gibson et al., 2007). Over the last 20 years there has been a decline in the area of cereal crops and an increase in oilseed rape, linseed and maize. Soils in the study area are predominantly lime-rich or loamy and clayey. Average annual rainfall is 719.0 mm, with average rainfall in June and December of 58.5 and 77.4 mm, respectively. The average annual maximum temperature is 13.3 8C and the maximum temperatures in June and December are 18.5 and 7.4 8C, respectively (Met Office, 2007). 2.2. Farm-scale habitat surveys Habitat surveys were undertaken in 2005 on 15 pairs of farms (Fig. 1). Fifteen organic farms which had completed a ‘conversion’ period of 2 years organic management and a minimum of one additional year post-conversion were selected at random from a list of certified organic producers provided by the Soil Association and paired with conventional farms of the same land use type
Fig. 1. Map of paired farm sites used in farm-scale habitat surveys. The circles around farm pairs are 5 km in diameter. Open symbols represent farms where small mammal surveys were also carried out.
126
F.S. Bates, S. Harris / Agriculture, Ecosystems and Environment 129 (2009) 124–130
(arable only, pastoral only or mixed) within 5 km to standardize for geographical variation; farms were also matched for topography and elevation. Thirteen farm pairs were mixed, with beef, dairy and/or sheep herds, and one or more arable crops. One pair was arable only, one pair livestock only. Data were collected on management of non-crop habitats. Phase 1 habitat surveys (Nature Conservancy Council, 1990) were undertaken by one surveyor between January and June 2005 on whole farms up to 200 ha; farm buildings, yards and gardens were not included in area calculations. On larger farms, 200 ha was randomly selected from grid squares covering the main farm block. For farms with more than one farm block, where the main block was <200 ha, proportions of two blocks were randomly selected. Farm pairs were surveyed on consecutive days to avoid the effect of season. During the Phase 1 surveys all fields and field boundaries were mapped. Fields were either a crop or non-crop habitat. Set-aside, i.e. arable land removed from production for one cropping season or longer, was classified as non-crop, whereas crop habitats were either grassland (improved or unimproved pasture, grass leys) or land in arable rotation (cropped, harvested, ploughed). Other noncrop habitats were hedgerow, woodland and non-cropped arable margins. A hedgerow was defined as a more or less continuous line of woody vegetation <4.5 m high managed to maintain a linear shape (Barr and Gillespie, 2000). A continuous line of woody vegetation with an average height >4.5 m and dominated by woody stems at the base was classed as a treeline. A hedgerow was classified as ‘cut’ if there was evidence of a horizontal and/or vertical cut carried out within the current cutting season, or ‘uncut’. Hedge height and width were measured, at 50 m intervals, to the nearest 0.25 m, including both the basic woody framework of the hedge, and any substantial recent growth (very sparse new growth of a small number of shoots was excluded). All shrub species within 2 m either side of the data collection point recorded. The ‘quality’ of each hedgerow was assessed as the percentage of gaps along the total length (0, 5, 10, 20, 40 and >40%), because the frequency of hedgerow gaps has been shown to affect A. flavicollis and C. glareolus (Kotzageorgis and Mason, 1997). The number and size of hedgerow trees were recorded (10–40 cm diameter breast height (dbh) or >40 cm dbh), as standard trees within hedgerows can benefit granivorous species, including A. sylvaticus (Montgomery and Dowie, 1993). Areas of woodland, including established areas of trees and new plantations >0.005 ha, were mapped. Arable field margins were defined as an uncultivated area >0.5 m between the field boundary and the cultivated area. The width of uncropped arable field margins was measured to the nearest 0.25 m every 50 m along the field boundary. Georeferenced tiles of the study sites derived from digitized Ordnance Survey maps (http://digimap.edina.ac.uk) were put into Arcview version 3.2 and Arcview Spatial Analyst, Environmental Systems Research Institute, California, USA and used to calculate farm and field areas and the length of hedgerows.
hedgerows were matched per farm, one small and one large hedge, thus controlling for farm type and other between-farm management differences, such as time since conversion of organic farms. Large hedgerows selected were a minimum of 35% taller and/or 35% wider, with a cross-sectional area 35% greater than the paired small hedges, based on the average size difference we found between organic and conventional farms. Members of the pair were matched for other variables which may affect small mammal populations, for both sides of the hedge and the adjacent land. Hedgerows were matched for equal shrub species composition. Since species such as hawthorn Crataegus monogyna and hazel Corylus avellana may directly influence granivorous species, it was important to isolate the effect of increases in the volume of particular shrubs as hedge cross-sectional area increases from the effect of composition of shrub species along the hedge. Land use and crop type were matched since neighbouring land use (pasture or arable) can affect species such as A. sylvaticus (Montgomery and Dowie, 1993). The percentage live ground vegetation cover was measured because hedge-base ground cover is important, especially for C. glareolus. Where adjacent land was arable, margin width was matched; increased margin width has been shown to benefit C. glareolus and Sorex araneus (Shore et al., 2005). Flailing has been shown to have a negative effect on bank vole density and a positive effect on the density of field voles Microtus agrestis (Gelling et al., 2007), and so both members of a pair were cut or uncut. There was a size difference in the basic woody framework of two members of a pair, as well as total size including any recent growth. A maximum difference of 908 orientation was accepted within hedgerow pairs. A 100 m transect with <5% gaps was selected on each hedgerow with no hedgerow trees. Eight hedgerow pairs were adjacent to pastoral land only; two pairs adjacent to arable land. Hedge height and width were measured to the nearest 0.25 m at three points along the transect. To confirm that pairs were matched rigorously, ground vegetation cover (live ground flora and shrubs) at the hedge-base was estimated qualitatively to the nearest 10% within three 0.5 m 0.5 m squares along the hedgerow; shrub density 1 m from ground level was measured as a qualitative assessment of visibility through the hedge to the nearest 10% (whereby 100% represented zero visibility through the hedge, i.e. high density vegetation). Longworth trapping (Gurnell and Flowerdew, 1994) was carried out between August and December 2005, with two traps every 5 m along the transect on one side of the hedge, i.e. 42 traps per hedge, 84 traps per hedgerow pair per night; each pair of hedgerows was trapped simultaneously. Traps were baited with blow-fly pupae, crushed oats and carrot, with hay for bedding, and treadle weights set for 2 g to facilitate capture of juvenile rodents and shrews. Traps were left in place for three nights, set at dusk and checked at dawn; they were closed during the day. All captures were identified to species, weighed, sexed, aged (juvenile, adult) and fur-clipped on the left or right to identify recaptures from days 1 and/or 2, respectively.
2.3. Small mammal surveys
2.4. Data analysis
Small mammal surveys were conducted on a subset of five organic and five conventional farms which were not treated as farm pairs. A paired design was used at the scale of matched hedgerows to examine the effect of a difference in hedgerow size. To maintain a high standard of pairing, only farms where it was possible to match a pair of hedgerows closely were included. The matched-pairs design aims to exclude the effect of confounding variables including landscape variables, aspects of farming system, e.g. agrochemical inputs, as well as the time of season. Two
Hedge cross-sectional area was calculated as average height by average width, hedgerow area as average width by total length. For the analysis of the farm-scale habitat data, each farm was treated as the sample unit; farm averages were calculated for variables measured multiple times, e.g. hedgerow height, number of hedgerow trees per hedge. The area and structure of non-crop habitats were analyzed using a multivariate repeated measures general linear model (MANOVA) in SPSS 12.0, SPSS Inc., with farm type (organic or conventional) as treatment factors (see Gibson
F.S. Bates, S. Harris / Agriculture, Ecosystems and Environment 129 (2009) 124–130
et al., 2007). Where appropriate, related variables, e.g. hedge width, height and cross-sectional area, were analyzed together in a single test to reduce the risk of Type 1 errors. Variables considered unrelated to other dependent variables, e.g. number of hedgerow shrub species, were analyzed in a univariate repeated measure general linear model. Data were transformed where necessary to achieve normality of the residuals. Diversity indices were arc sine square root transformed prior to analysis. All figures quoted are untransformed means S.E. Small mammal abundance was the total number of individuals captured, excluding recaptures, and species richness the number of species captured. We calculated small mammal species diversity using the Shannon index (H0 ), the Shannon evenness measure (J) (Michel et al., 2006), Simpson’s index (D) and Simpson’s measure of evenness (1/D); the latter two measures take into account species dominance (Magurran, 2004). The effect of hedgerow size on small mammal numbers was analyzed using a repeated measures MANOVA. Related dependent variables, such as total small mammal abundance and the abundance of the three most common species, were analyzed in the same test. 3. Results 3.1. Farm-scale differences in the structure and management of noncrop habitats
127
their hedgerows on a yearly cycle. A higher proportion of organic than conventional farmers staggered the cutting over 2 or more years. Consequently, a significantly greater area of hedgerow was uncut on organic than conventional farms (F1,14 = 18.448, P = 0.001), leading to a significant difference in hedgerow size between farm types (Table 2); hedgerows on organic farms were significantly taller and had a greater cross-sectional area than those on conventional farms but were not significantly wider on organic than conventional farms. There was no difference in shrub species richness or in the number of trees in organic and conventional hedgerows. A higher proportion of organic than conventional farmers had carried out hedgerow planting, either to establish new hedgerows or to fill in gaps within existing low quality hedgerows (8 and 2 of 15 farmers, respectively). However, there was no significant difference in the proportion of farm area occupied by hedgerows of different quality (Table 2). Non-cropped arable margins tended to be wider on organic (3.0 0.61 m) than conventional farms (2.2 0.64 m) but this difference was not significant (F1,12 = 3.093, P = 0.104). When pairs including one or more farms involved in another Agri-Environment Scheme (AES) were excluded, no significant difference was found between margin width on organic (3.4 0.45 m) and conventional (1.4 0.03 m) farms (F1,5 = 0.592, P = 0.476). 3.2. Effect of hedgerow size on small mammal abundance
Organic farms had completed conversion 4.3 0.5 years prior to the study. Organic hedgerow management regimes were also implemented during the 2 year conversion period prior to certification. There was no significant difference in either the total size of organic (145 27.5 ha) and conventional farms (155.5 25.4 ha) selected (F1,14 = 0.321, P = 0.580) or the area included in the farmscale surveys: 124.8 14.4 and 130.4 15.6 ha, respectively (F1,14 = 0.342, P = 0.568). There was a significant difference in the area occupied by different landscape elements between farm types (Table 1 and Fig. 2). The percentage area of arable land was higher on conventional than organic farms, whereas the area of grass was significantly greater on organic farms. Uncut hedgerows formed a larger area of organic than conventional farms. Although conventional farms had a larger area of cut hedgerows, there was no difference in percentage area occupied by all hedgerows (cut and uncut) between farm types. Nor was there any difference between farm types in the percentage area of woodland or total area of noncrop elements (hedgerow, woodland and set-aside). Fourteen out of 15 organic farmers cut their hedges at intervals of 2 or more years, whereas 11 of 15 conventional farmers cut all Table 1 Proportion of crop and non-crop habitats on 15 pairs of organic and conventional farms Habitat
Grass fields Arable fields Set-aside All hedgerow Uncut hedgerow Cut hedgerow Woodland Total non-crop habitat
Mean percentage area (S.E.) Organic farms
Conventional farms
64.4 27.2 2.4 1.1 0.7 0.4 4.8 8.4
50.0 40.9 2.2 1.1 0.2 0.9 3.8 9.1
(6.6) (5.2) (2.3) (0.2) (0.1) (0.1) (1.2) (2.4)
(7.4) (6.8) (3.4) (0.2) (0.1) (0.2) (1.5) (2.4)
F1,14
8.652 8.731 N/A 0.351 16.254 8.799 1.346 0.063
P
0.011* 0.010* 0.563 0.001* 0.010* 0.265 0.806
Percentages represent proportion of total farm area. Prior to analysis, the percentage of woodland and total non-crop habitat were log10 transformed; the percentage of uncut and cut hedgerow were x3 transformed. Total non-crop habitat includes set-aside, hedgerow and woodland. N/A: data were not included in statistical analysis due to zeros in the data set. * P < 0.05.
Hedgerows were paired for a difference in size; a repeated measures MANOVA confirmed a significant difference in hedgerow size within the pairs. ‘Large’ hedgerows were significantly greater in height (2.7 0.31 m), width (2.5 0.22 m) and cross-sectional area (7.11 1.42 m2) than ‘small’ hedgerows (height, 1.8 0.71 m, width 1.76 0.15 m, cross-sectional area 3.34 0.54 m2) (height, F1,9 = 23.840, P = 0.001; width, F1,9 = 13.658, P = 0.005; cross-sectional area, F1,9 = 66.869, P < 0.001). Hedge-base ground cover and hedgerow shrub density were matched when selecting sites, and there was no significant difference in ground cover between large (64.0 5.06%) and small hedgerows (57.7 3.0%) or in the mean shrub density of large (83.3 4.01%) and small (81.3 3.38%)
Table 2 Differences in hedgerow characteristics on 15 pairs of organic and conventional farms Hedge variable
Mean (S.E.)
F1,14
P
Organic farms
Conventional farms
2.00 (0.02) 1.80 (0.01) 3.70 (0.05)
1.63 (0.01) 1.60 (0.01) 2.70 (0.03)
13.047 2.916 8.781
0.030* 0.110 0.010*
Shrub species per 100 m Trees per 100 m (10–40 cm dbh) Trees per 100 m (>40 cm dbh)
7.70 (0.03) 0.14 (0.001)
7.50 (0.03) 0.11 (0.001)
0.094 0.018
0.764 0.210
0.13 (0.001)
0.10 (0.001)
0.894
0.654
Area hedge (0–5% gaps) (m2) Area hedge (10–20% gaps) (m2) Area hedge (>40% gaps) (m2)
0.76 (0.11)
0.78 (0.16)
0.047
0.831
0.31 (0.16)
0.24 (0.03)
0.452
0.512
0.07 (0.01)
0.05 (0.01)
2.332
0.149
Hedge Hedge Hedge area
height (m) width (m) cross-sectional (m2)
Data for hedgerow size, hedgerow quality, and hedgerow shrubs and trees were analyzed in three separate repeated measures MANOVAs. Prior to analysis, hedge height, cross-sectional area and trees per 100 m were log10 transformed. All hedge area variables were square root transformed. * P < 0.05.
F.S. Bates, S. Harris / Agriculture, Ecosystems and Environment 129 (2009) 124–130
128
Fig. 2. Proportion of area occupied by different landscape elements on (a) organic and (b) conventional farms.
hedgerows (cover, F1,9 = 2.212, P = 0.171; density, F1,9 = 0.288, P = 0.604). We had 584 captures of 359 different small mammals (four rodents—A. flavicollis, A. sylvaticus, C. glareolus and M. agrestris, and three shrews—water shrew Neomys fodiens, common shrew S. Table 3 Small mammals trapped in small and large hedges Species
Number of individuals (%) Small hedges
Yellow-necked mouse Apodemus flavicollis Wood mouse Apodemus sylvaticus Bank vole Clethrionomys glareolus Field vole Microtus agrestris Water shrew Neomys fodiens Common shrew Sorex araneus Pygmy shrew Sorex minutus Total number
9 (5.2)
Large hedges 13 (7.0)
All hedges
62 (33.5)
115 (32.0)
47 (27.0)
45 (24.3)
92 (25.6)
8 (4.6)
3 (1.6)
2 (1.1)
0 (0)
11 (3.1) 2 (0.6)
47 (27.0)
55 (29.7)
102 (28.4)
8 (4.6)
7 (3.8)
15 (4.2)
185
Table 4 Abundance of small mammals along small and large hedges Species
22 (6.1)
53 (30.5)
174
araneus and pygmy shrew Sorex minutus) in 2520 trap nights (Table 3). There was no significant difference in the abundance of small mammals along large and small hedgerows (Table 4). Hedgerow size had no effect on species richness or species diversity (Table 5). Nor was there a significant interaction between hedgerow size and farm type on either abundance or diversity of small mammals (Tables 4 and 5).
359
Number of individuals excludes recaptures; figures in parentheses are percentages.
Hedge size All species Apodemus sylvaticus Clethrionomys glareolus Sorex araneus Hedge size farm type All species Apodemus sylvaticus Clethrionomys glareolus Sorex araneus
Mean (S.E.) Small hedges
Large hedges
17.4 5.3 4.7 4.7
18.5 6.2 4.5 5.5
(2.19) (1.05) (1.19) (1.44)
(2.28) (0.95) (1.27) (1.06)
F1,8
P
0.129 0.326 0.064 0.561
0.728 0.584 0.807 0.748
0.001 1.775 0.420 0.035
0.975 0.220 0.535 0.856
Data for abundance of C. glareolus were log10 transformed prior to analysis. Total abundance and the abundance of the three most common species were analyzed using a repeated measures MANOVA, with farm type included as a between subjects factor.
F.S. Bates, S. Harris / Agriculture, Ecosystems and Environment 129 (2009) 124–130 Table 5 Small mammal species richness and diversity in small and large hedges Diversity measure
Hedge size Number of species Shannon H0 Shannon J Simpson D Simpson 1/D
Mean (S.E.) Small hedges
Large hedges
3.80 0.45 0.76 0.39 2.95
3.90 0.50 0.86 0.33 3.25
(0.25) (0.05) (0.09) (0.07) (0.28)
(0.43) (0.03) (0.04) (0.03) (0.25)
Hedge size farm type Number of species Shannon H0 Shannon J Simpson D Simpson 1/D
F1,8
P
0.030 0.227 1.845 0.401 0.379
0.866 0.646 0.211 0.544 0.555
0.758 0.215 0.383 0.027 0.046
0.409 0.656 0.553 0.875 0.836
Before analysis, Shannon H0 and Shannon J were x2 transformed, Simpson D was x2 transformed. Data were analyzed using a repeated measures MANOVA, with farm type included as a between subjects factor.
4. Discussion A large number of studies have shown higher abundance and diversity of a range of species on organic farms (Hole et al., 2005), but further work is needed to establish the relative contribution of farming system (e.g. level of agrochemical use) and landscape structure (Chamberlain et al., 1999) to this difference. Our study confirms farm-scale differences exist in the size and structure of hedgerow habitats between farm types, as a result of differences in annual management. These differences may be important in increasing biodiversity on organic farms but do not benefit all species. 4.1. Effect of hedgerow size on small mammals We predicted that the difference in hedgerow size between organic and conventional farms would have a significant effect on small mammal populations due to an increase in area for foraging and shelter, and potential increase in food sources. Whereas previous studies suggest that hedgerow size may influence small mammal numbers, the majority relied on samples from a limited number of farms (e.g. Kotzageorgis and Mason, 1997). Gelling et al. (2007) found that hedgerow connectivity was a positive predictor of A. sylvaticus, and that hedgerow width was a strong positive predictor of small mammal biomass. Pocock and Jennings (2008) used a matched-pairs design to assess the response of insectivorous mammals, including shrews, to other aspects of agricultural intensification, but to our knowledge there has not been a study using the matched-pairs design to isolate the effect of individual non-crop habitat variables on small mammals. Our results suggest that a difference in hedgerow size, comparable to that seen between organic and conventional farms, does not have a significant effect on small mammal populations. Tattersall et al. (2002) found no effect of the linearity of set-aside and hedgerow habitats on the abundance of A. sylvaticus, M. agrestris or S. araneus, or on small mammal diversity. Shore et al. (2005) found that the impact of field margin management under the ES varied between species. The abundance of A. sylvaticus did not differ between narrow margins and wider margins, although higher numbers of both C. glareolus and S. araneus were found on the ES-style grassy margins in autumn. 4.2. Small mammals on organic farms Hitherto, the vast majority of studies into the importance of hedgerows for small mammals have been carried out on
129
conventional farms, although a few small-scale studies suggest that aspects of organic agriculture may benefit small mammal populations; Macdonald et al. (2007), for instance, suggested that there is a difference in A. sylvaticus populations between organic and conventional farms, and Brown (1999) found increased activity levels of A. sylvaticus, C. glareolus and S. araneus in organic compared to conventional fields. However, Pocock and Jennings (2008) found that shrews were relatively insensitive to higher levels of agrochemical inputs, suggesting that exclusion of agrochemicals on organic farms does not benefit these species. Our study aimed to quantify the effect of a specific aspect of habitat management on organic farms, but further research is necessary into the effect of the organic farming system on all small mammal species, particularly to isolate the relative effects of agrochemical inputs and other aspects of farming system from the influence of habitat management. 4.3. Implications of the ES for hedgerow management The introduction of the ES since this study is likely to reduce variation in existing management practices between conventional and organic farms. Management prescriptions include maintaining hedge height to 1.5 m and above, or 2 m and above and cutting each hedge no more than once every 2 years with a staggered cutting regime (DEFRA, 2005). ‘Enhanced hedgerow management’ options include cutting no more than a third of all hedges per year, further increasing the variety of hedgerow cutting stages across the farm. Consequently, there will be an increase in the area of uncut hedgerows, particularly on conventional farms, contributing to an overall increase in hedge size, particularly where hedgerows were previously managed more intensively. Whilst the ES is expected to have an effect, predominantly beneficial, on taxa such as invertebrates and birds, Whittingham (2007) emphasizes the importance of monitoring the effects of an AES to ensure that the scheme’s prescriptions meet the needs of a greater range of species. It is important to understand the factors that will increase small mammal abundance, since this will have a significant impact upon predator populations (Love et al., 2000), as well as a range of ecosystem processes (Hayward and Phillipson, 1979). Our study suggests that increases in hedgerow size under the ES may have little or no effect on small mammal numbers. It may be more effective to place higher emphasis on increasing the area covered by hedgerows, through hedgerow planting and repair, than by prescribed management of existing hedgerows. Pocock and Jennings (2008) demonstrate the strong effect of boundary loss on shrew abundance and suggest that replanting of hedgerows will benefit these species. More research is needed into the use of planted hedgerows by small mammals, and it will also be important to examine the effect of a widespread shift from annual cutting to a 2 or 3 yearly staggered cut under the ES on small mammal populations, although the benefits of this may only be clear after a number of cutting cycles. 5. Conclusions We confirm that farm-scale differences in hedgerow size and management exist between organic and conventional farms, and examined the effect of this size difference on small mammal numbers in organic and conventional hedgerows. We focused on this group since small mammal populations influence a diversity of species at higher trophic levels, as well as a range of biotic and abiotic environmental factors. Thus increasing small mammal populations on farmland is crucial to improving the biodiversity of agricultural ecosystems. We show that increased hedgerow size on organic farms is not benefitting small mammals. Significant
130
F.S. Bates, S. Harris / Agriculture, Ecosystems and Environment 129 (2009) 124–130
population gains may be more effectively achieved by increasing the area of non-crop habitats. Acknowledgements We thank Paul Craze, Nancy Jennings and Michael Pocock for their advice, the volunteers who assisted with the field work, particularly Giles Manning and Phillip Paterson, the landowners for permission to work on their land and the Dulverton Trust for funding. References Barr, C.J., Gillespie, M.K., 2000. Estimating hedgerow length and pattern characteristics in Great Britain using Countryside Survey data. J. Environ. Manage. 60, 23–32. Brown, R.W., 1999. Margin/field interfaces and small mammals. Aspects Appl. Biol. 54, 203–206. Burel, F., 1996. Hedgerows and their role in agricultural landscapes. Crit. Rev. Plant Sci. 15, 169–190. Chamberlain, D.E., Wilson, J.D., Fuller, R.J., 1999. A comparison of bird populations on organic and conventional farm systems in southern Britain. Biol. Conserv. 88, 307–320. Croxton, P.J., Sparks, T.H., 2002. A farm-scale evaluation of the influence of hedgerow cutting frequency on hawthorn (Crataegus monogyna) berry yields. Agr. Ecosyst. Environ. 93, 437–439. DEFRA, 2002. Economic Evaluation of the Organic Farming Scheme. Department for Environment, Food and Rural Affairs, http://statistics.defra.gov.uk/esg/evaluation/organic/finalrep.pdf. DEFRA, 2005. Entry Level Stewardship Handbook. Department for Environment, Food and Rural Affairs, http://www.defra.gov.uk/erdp/pdfs/es/els-handbook.pdf. Fuller, R.J., Norton, L.R., Feber, R.E., Johnson, P.J., Chamberlain, D.E., Joys, A.C., Mathews, F., Stuart, R.C., Townsend, M.C., Manley, W.J., Wolfe, M.S., Macdonald, D.W., Firbank, L.G., 2005. Benefits of organic farming to biodiversity vary among taxa. Biol. Lett. 1, 431–434. Gelling, M., Macdonald, D.W., Mathews, F., 2007. Are hedgerows the route to increased farmland small mammal density? Use of hedgerows in British pastoral habitats. Landscape Ecol. 22, 1019–1032. Gibson, R.H., Pearce, S., Morris, R.J., Symondson, W.O.C., Memmott, J., 2007. Plant diversity and land use under organic and conventional agriculture: a wholefarm approach. J. Appl. Ecol. 44, 792–803. Gurnell, J., Flowerdew, J.R., 1994. Live Trapping Small Mammals—A Practical Guide, 3rd ed. The Mammal Society, London. Harris, S., McLaren, G., Morris, M., Morris, P.A., Yalden, D., 2000. Abundance/mass relationships as a quantified basis for establishing mammal conservation priorities. In: Entwhistle, A., Dunstone, N. (Eds.), Priorities for the Conservation of Mammalian Biodiversity: Has the Panda had its Day? Cambridge University Press, Cambridge, pp. 101–117. Hayward, G.F., Phillipson, J., 1979. Community structure and functional role of small mammals in ecosystems. In: Stoddart, D.M. (Ed.), Ecology of Small Mammals. Chapman and Hall, London, pp. 135–211.
Hole, D.G., Perkins, A.J., Wilson, J.D., Alexander, I.H., Grice, P.V., Evans, A.D., 2005. Does organic farming benefit biodiversity? Biol. Conserv. 122, 113–130. Kotzageorgis, G.C., Mason, C.F., 1997. Small mammal populations in relation to hedgerow structure in an arable landscape. J. Zool. 242, 425–434. Lampkin, N., 1998. Organic Farming, 3rd ed. Old Pond, Ipswich. Love, R., Webbon, C., Glue, D.E., Harris, S., 2000. Changes in the food of British barn owls (Tyto alba) between 1974 and 1997. Mammal Rev. 30, 107–129. Macdonald, D.W., Tattersall, F.H., Service, K.M., Firbank, L.G., Feber, R.E., 2007. Mammals, agri-environment schemes and set-aside—what are the putative benefits? Mammal Rev. 37, 259–277. Magurran, A.E., 2004. Measuring Biological Diversity. Blackwell Publishing, Oxford. Met Office, 2007. UK Climate and Weather Statistics. The Met Office, http:// www.metoffice.gov.uk/climate/uk/. Michel, N., Burel, F., Butet, A., 2006. How does landscape use influence small mammal diversity, abundance and biomass in hedgerow networks of farming landscapes? Acta Oecol. 30, 11–20. Montgomery, W.I., Dowie, M., 1993. The distribution and population regulation of the wood mouse Apodemus sylvaticus on field boundaries of pastoral farmland. J. Appl. Ecol. 30, 783–791. Nature Conservancy Council, 1990. Handbook for Phase 1 Habitat Survey—A Technique for Environmental Audit. Field manual. Joint Nature Conservancy Council, Peterborough. Newton, I., 2004. The recent declines of farmland bird populations in Britain: an appraisal of causal factors and conservation actions. Ibis 146, 579–600. Percival, S., 1991. Population trends in British barn owls. Br. Wildl. 2, 131–140. Pocock, M.J.O., Jennings, N., 2008. Testing biotic indicator taxa: the sensitivity of insectivorous mammals and their prey to the intensification of lowland agriculture. J. Appl. Ecol. 45, 151–160. Robinson, R.A., Sutherland, W.J., 2002. Post-war changes in arable farming and biodiversity in Great Britain. J. Appl. Ecol. 39, 157–176. Shore, R.F., Meek, W.R., Sparks, T.H., Pywell, R.F., Nowakowski, M., 2005. Will Environmental Stewardship enhance small mammal abundance on intensively managed farmland? Mammal Rev. 35, 277–284. Soil Association, 2002. Soil Association Organic Standards and Certification (revision 14 2002/03). Soil Association, Bristol. Tapper, S., 1979. The effect of fluctuating vole numbers (Microtus agrestis) on a population of weasels (Mustela nivalis) on farmland. J. Anim. Ecol. 48, 603– 617. Tattersall, F.H., Macdonald, D.W., Hart, B.J., Johnson, P., Manley, W., Feber, R., 2002. Is habitat linearity important for small mammal communities on farmland? J. Appl. Ecol. 39, 643–652. Todd, I.A., Tew, T.E., Macdonald, D.W., 2000. Arable habitat use by wood mice (Apodemus sylvaticus). 1. Macrohabitat. J. Zool. 250, 299–303. Tucker, G.M., Heath, M.F., 1994. Birds in Europe: Their Conservation Status. Birdlife International, Cambridge. Walker, M.P., Dover, J.W., Hinsley, S.A., Sparks, T.H., 2005. Birds and green lanes: breeding season bird abundance, territories and species richness. Biol. Conserv. 126, 540–547. Whittingham, M.J., 2007. Will agri-environment schemes deliver substantial biodiversity gain, and if not why not? J. Appl. Ecol. 44, 1–5. Wickramasinghe, L.P., Harris, S., Jones, G., Vaughan, N., 2003. Bat activity and species richness on organic and conventional farms: impact of agricultural intensification. J. Appl. Ecol. 40, 984–993.