1. Foraging Bird Resource Requirements and Behaviour in Conventional and Alternative Arable

1. Foraging bird resource requirements and behaviour in conventional and alternative arable crop systems: a review of published research.

CONTENTS

1.1 Background...... 1 1.2 Aims...... 1 1.3 Introduction...... 1 1.4 Food availability...... 4 1.4.1 Introduction...... 4 1.4.2 Effects of crop type...... 5 1.4.3 Effects of management of non-crop habitats...... 6 1.4.3.1 Stubble...... 6 1.4.3.2 Set-aside...... 7 1.4.3.3 Conservation headlands...... 8 1.4.3.4 Field margins...... 9 1.4.4 Effects of position within a field...... 10 1.4.5 Effects of agricultural practices...... 11 1.4.5.1 Invertebrates...... 12 1.4.5.2 Plants...... 13 1.4.6 Effects of pesticides...... 15 1.4.6.1 Insecticide: factors affecting their impact on non-target taxa………………...15 1.4.6.2. Insecticide: levels of impact on non-target taxa...... 16 1.4.6.3. Herbicide: effects on weeds...... 18 1.4.6.4 Herbicide: indirect effects on invertebrates…………………………………...19 1.4.6.5. Fungicides...... 20 1.4.7 Effects of whole farm agricultural systems...... 20 1.4.7.1 Integrated farming systems...... 20 1.4.7.2 Systems using genetically-modified crops...... 21 1.4.7.3 Organic systems...... 22 1.4.8 Weather effects...... 22 1.4.9 Effects of food accessibility and predation risk...... 23 1.4.10 Discussion – food availability...... 25 1.5 Foraging preferences...... 26 1.5.1 Introduction...... 26 1.5.2 The preference of birds for farmland habitats...... 26 1.5.2.1 All year studies...... 26 1.5.2.2 Winter studies...... 27 1.5.2.3 Breeding season studies...... 28 1.5.3 Specific studies on the species being considered in this project...... 29 1.5.4 Foraging preferences and pesticide levels...... 36 1.5.4 Discussion – foraging preferences...... 37 1.6 Functional response...... 37 1.6.1 Introduction...... 37 1.6.2 Types of functional response...... 37 1.6.3 Factors affecting the functional response...... 38 1.6.3.1 Food availability...... 38 1.6.3.2 Relative profitability...... 38 1.6.3.3 Substrate...... 39 1.6.3.4 Interference...... 39 1.6.3.5 Search efficiency...... 39 1.6.3.6 Individual variation...... 39 1.6.3.7 Risk sensitivity...... 40 1.6.4 Discussion – functional response...... 40 1.7 Avian energetics...... 40

i 1.7.1 Introduction...... 40 1.7.2 Methods...... 41 1.7.3 Results...... 41 1.7.3.1 Daily energy expenditure...... 41 1.7.3.2 Moisture and energy contents of foods...... 42 1.7.3.2 Assimilation efficiency...... 42 1.7.3.3 Estimation of average daily food intake...... 43 1.7.5 Limitations of method...... 45 1.7.5.1 Appropriateness of data on food quality...... 45 1.7.5.2 Appropriateness of data on Daily Energy Expenditure...... 45 1.7.5.3 Plausibility of food intake predictions...... 45 1.7.6 Discussion – avian energetics...... 45 1.8 Discussion...... 46 1.9 References...... 48

ii 1. Foraging bird resource requirements and behaviour in conventional and alternative arable crop systems: a review of published research.

1.1 Background

In Britain, many species of farmland birds are undergoing long term population declines and range contractions (Fuller et al. 1995; Siriwardena, Baillie & Wilson 1998). A reduction in food availability at critical periods of the life cycle is likely to have been responsible for driving many of the observed population changes (Wilson et al. 1999; Marshall et al. 2001). Before models of the effects of pesticides on the food webs of farmland birds are considered, it is useful to review what is known about the relationship between farmland bird species and their food.

1.2 Aims

Using published literature this review aims to determine: (a) what is currently known about the availability of food for birds on arable farmland under different pesticide regimes, (b) what is known about the relative use made by farmland bird species of cropped areas receiving pesticide inputs and cropped and uncropped areas receiving no or reduced pesticide inputs, (c) the functional response of foraging birds to variation in their food supply and the effects of this variation on survival and fledging success of chicks and (d) how avian energetics may bridge the gap between our current understanding of behaviour and time budgets of foraging farmland bird species and their survival.

1.3 Introduction

This review addresses farmland bird species that feed primarily on plant material, seeds and on invertebrates dwelling on the ground or in crops and weeds. Twenty-one species fall into this category (Table 1.1). Invertebrates comprise a major component of the chick food of 16 out of 21 species listed. Of the remaining five species, four are pigeons or doves, which feed their young on crop milk and seeds. The final species, the linnet Carduelis cannabina, not only feeds its young on seeds but adults and juveniles rely on seeds throughout the year. Adults and juveniles of most of the remaining species take more than one food type, which varies seasonally. Eleven out of 17 resident species rely on invertebrates during the summer whereas only two out 17 do so during the winter. Seasonal variation in the incidence of seed taking is much less marked and fifteen out of the 17 residents feed on seeds in summer and winter. Invertebrates form a major component of the summer diet of three of the four summer migrants. The fourth summer migrant, the turtle dove Streptopelia turtur, feeds principally on seeds of weed species, fruits and cereal grain.

1 Table 1.1. Major food components of selected farmland bird species (chick food, summer & winter)(Cramp & Simmons (1977), Combreau, Fouillet & Guyomarc’h (1990), Evans (1997a), Buxton, Crocker & Pascual (1998)).

Bird species Chick food Summer food Winter food Chaffinch Invertebrates Invertebrates, seed Seeds, plant material Cirl Bunting Invertebrates, seeds Seeds, invertebrates Seeds Collared Dove Crop milk, grain Cereal grain, seeds Cereal grain, seeds Corn bunting Invertebrates, seeds Seeds, invertebrates Seeds Goldfinch Invertebrates, seeds Seeds, plant material,Seeds, plant material, invertebrates invertebrates Greenfinch Seeds, invertebrates Seeds, plant material Seeds, plant material Grey partridge Invertebrates, plant Plant material, seeds,Plant material, seeds material (seeds?) invertebrates House sparrow Invertebrates Seeds, invertebrates Seeds Linnet Seeds Seeds Seeds Quail* Invertebrates Seeds, invertebrates N/a Red-legged partridge Invertebrates, seeds Seeds, plant material Plant material, seeds Reed bunting Invertebrates Invertebrates, seeds Seeds Rook Invertebrates, cereal Invertebrates, cereals Cereals, invertebrates Skylark Invertebrates Invertebrates, plantPlant materials, seeds material, seeds Stock Dove Seeds, crop milk Seeds, plant material Seeds, plant material Stone Curlew* Invertebrates Invertebrates N/a Tree sparrow Invertebrates Seeds, invertebrates Seeds Turtle dove* Seeds Seeds, fruits of weeds,N/a cereals Wood Pigeon Seeds, plant material,Plant material, seeds,Plant material, seeds, crop milk fruit fruit Yellowhammer Invertebrates, unripe Invertebrates Seeds grain Yellow Wagtail* Invertebrates Invertebrates N/a * summer migrants.

The invertebrate taxa, which are known to comprise important components of farmland bird diets, are listed in Table 1.2. Important arable plants (weed species) in the diet of farmland birds are listed in Table 1.3.

2 Table 1.2 Important invertebrate taxa in the diet of farmland birds, and those especially associated with declining farmland species (from: Wilson, Arroyo & Clark 1996; Wilson et al. 1999). A taxon was rated as important if it comprised a quantitative mean of at least 5% in the diet.

Invertebrate taxa (order) Invertebrate taxa (familyFound to be prevalent in diet of or sub-order) declining bird species Arachnida * Araneae * Coleoptera Carabidae * Chrysomelidae * Curculionidae * Orthoptera * Acrididae * Diptera Tipulidae Hemiptera Aphididae Hymenoptera * Formicidae Symphyta * Lepidoptera *

Table 1.3. Important plant families and genera in the diet of farmland birds (Marshall et al. 2001).

Very important Important Family Poaceae Compositae Polygonaceae Labiatae Chenopodiaceae Boraginaceae Caryophyllaceae Violaceae Cruciferae Genus Stellaria Cerastium Chenopodium Sinapis Polygonum Viola Poa Rumex Senecio

This review will first consider food availability, and describe what is known about differences in food availability between different cropped and uncropped farmland habitats, especially in relation to pesticide management. Birds are often found not to use food resources in proportion to their availability (Olsson et al. 2001), i.e. they often exhibit preferences. The preference for different cropped and uncropped habitats will therefore be examined, in terms of the relative use made by farmland birds of these habitats. The functional response of birds to changes in food availability will then be considered, and examples given of the effects of these changes on survival and reproductive success. The amount of food available and the birds’ foraging behaviour (the functional response and any preferences) determine the amount of food eaten. The amount of food eaten in relation to the amount of food required may affect breeding

3 success and survival. Therefore, in the final section of this review we will consider the nutritional value of bird food in relation to the amount of food needed – avian energetics.

Other sections of this report will also consider some of the subjects covered by this review. Objective 2 (an analysis of available models) and Objective 8 (further work on functional responses needed for the depletion model) will consider the functional response. The nutritional value of bird foods will be reviewed for Objective 3 (ranking weed species in terms of food value) and Objective 5 (propose groupings of bird food in terms of their value and availability).

1.4 Food availability

1.4.1 INTRODUCTION

Food availability in this review is defined as the quantity of potential food resources present in an area, which may be utilised by a bird searching for food (adapted from Wolda 1990).

The difference between “abundance” and “availability” in terms of food resources has only recently been appreciated in studies of bird utilisation of farmland habitats (Moorcroft et al., 2002; Hart et al., 2002). Indeed, the terms seem to be interchangeable in many studies. For instance, Aebischer (1998) refers to food availability in equivalent terms to food abundance for species such as grey partridge Perdix perdix, lapwing Vanellus vanellus, skylark Alauda arvensis and corn bunting Miliaria calandra. Aebischer & Ward (1997) and Brickle et al. (2000) related corn bunting distribution to crop type and invertebrate abundance, rather than availability. Benton et al. (2002) linked farmland bird declines to insect abundance. Campbell et al. (1997) discussed trends in the abundance of food of farmland birds. Chamberlain & Wilson (2000) discussed invertebrate abundance on organic and conventional farms in relation to birds. Moreby & Southway (2002) referred to the availability of invertebrate groups in relation to cropping and year effects, but actually equated abundance to availability.

As the vast majority of studies relevant to this review equated abundance to availability, these are included, but with the proviso that the abundance of a group or taxa may not necessarily reflect its availability to a particular bird species or guild.

Hutto (1990) argued that measurements of food abundance may not reflect food availability, because of scale-of-measurement problems and measures of availability being equated with standing crops, even though bird behaviour can depend on the renewability of the resource. A bird’s perception also differs from measures of availability because of a food resource’s crypticity, inaccessibility, difficulty of capture, and mechanical or chemical defences (Hutto 1990). The size, life stage, palatability, coloration, activity patterns and other characteristics of arthropods act as “translators”, which relate abundance to availability (Cooper & Whitmore 1990).

Scale-of-measurement factors affect availability measurements, as food is not uniformly distributed throughout a bird’s feeding territory, so extrapolations of abundance may not be accurate. Some food resources (e.g. fruit and seeds) are not continuously renewing, whereas others (e.g. some invertebrates, by colonising an area), can renew. Bird behaviour is affected by the depletion/renewal of a food resource (Hutto 1990). Hutto (1990) suggested that quantitative measures of behaviour that are correlated with food abundance might provide a “check” on the reliability of food availability measurements. However, extensive fieldwork is usually required to quantify these measures (Poulin & Lefebvre 1997).

A knowledge of food availability, how it differs between habitats and in response to management, and how it changes over time, is a necessary prerequisite for both the depletion and deterministic models being considered in this project.

4 Food availability will therefore be considered here in terms of both food abundance and accessibility. The factors that affect food abundance include vegetation cover (crops and other farmland cover), the effects of crop management practices, pesticide usage, environmental and temporal effects.

1.4.2 EFFECTS OF CROP TYPE

It has been shown repeatedly that the abundance of arthropods taken by farmland birds during the breeding season varies between arable crop types (e.g. Reddersen 1994; De Cornulier et al. 1997). In some of the most recent studies, field data on the abundance of arthropod prey have been matched to the results of dietary studies for particular bird species, e.g. grey partridge and yellowhammer, to derive species-specific measures of food abundance.

Moreby & Southway (2002) showed that the combined abundance of key arthropod groups in the diet of grey partridge chicks varied between crops on a farm in Leicestershire. Densities of prey in wild bird food cover were much higher than in grazed grassland or any of four arable crops (winter wheat, winter barley, winter oilseed rape & winter beans). Within the arable crops, densities were similar in winter cereals and beans but they were much lower in winter oilseed rape. These differences were maintained between years.

Holland et al. (2002) estimated arthropod densities in a range of arable crops from two farms, in Hampshire and Lincolnshire. They derived measures of food abundance for grey partridge chicks and yellowhammer. The grey partridge Chick Food Index (CFI) varied seasonally but differed significantly between crops on both farms. It tended to be highest in peas and spring beans, and lowest in root crops (potatoes and sugar beet). Cereals had intermediate values. At both farms, the monthly CFIs for spring barley tended to be higher than that for winter wheat. Densities of arthropods taken by yellowhammers also varied between crops in Hampshire (field edge only) and in Lincolnshire (field centre and edge). The ranking of crops on the Hampshire farm, in descending order, by their mean monthly densities of yellowhammer prey (winter barley>winter oilseed rape>spring barley>winter wheat) differed markedly from that for the grey Partridge CFI (winter wheat>winter oilseed rape=winter barley>spring barley).

A third study examined differences between crops in the abundance of arthropod prey taken by corn buntings on arable farmland in Sussex (Ward & Aebischer 1994). Densities of key arthropod groups (caterpillars of Lepidoptera & Symphyta, spiders and harvestmen) were higher in spring than in autumn sown crops.

A finding common to all three studies was that spring-sown cereals tended to support higher densities of grey partridge chick food than winter cereals. However, the crop rankings were not consistent across farms. In particular, Moreby & Southway (2002) reported that the grey partridge CFI for winter oilseed rape was lower than those for cereals, whereas it was higher on the farms surveyed by Holland et al. (2002).

Comparative assessments of the abundances of individual arthropod taxa listed by Wilson et al. (1999) in different arable crops are numerous. Coleoptera: Several studies have reported that numbers of carabid and/or staphylinid beetles differ between cereals, brassicas and root crops (Booij & Noorlander 1992; Holland et al. 1994b; Thiele 1997). Spring-sown crops tend to have fewer carabids than winter-sown crops, and a different suite of species is present. Spring- breeding carabids (overwintering as adults) were more common in winter cereals than spring- sown crops (Luff & Sanderson 1992). Diptera: Reddersen (1994) found that winter cereals held more lauxaniid flies than spring cereals. Hymenoptera: Sawflies (Symphyta) are an important chick-food for some farmland species, including grey partridge, pheasant Phasianus colchicus, skylark, reed bunting Emberiza schoeniclus and corn bunting (Barker & Reynolds 2000). Sawflies differ in density between different crops. Densities of Dolerus and Pachynematus larvae were low in spring barley, winter wheat and heavily-grazed permanent pasture but much

5 higher in perennial rye-grass Lolium perenne crops (Barker, Brown & Reynolds 1999). Arachnida: Frank & Nentwig (1995) found that Araneae were found in greater numbers on oilseed rape than on bean or wheat crops.

Differences between crops in the densities of arthropods may be due differences in crop structure, the presence or absence of particular non-crop host plants, the micro-climate in the crop, and to crop management, including pesticide inputs and timing of sowing. In most cases, the relative importance of these factors has not been assessed but Booij & Noorlander (1992) found that carabid diversity and density was greatest in crops with early and persistent ground cover, and with no or reduced cultivations. These relationships were not contingent upon pesticide regime.

A change to winter cereals from spring cereals is likely to result in a 25% reduction in weed density and species diversity (Hald, 1999) In addition, plants that are important food resources for arthropod herbivores occurred at greater densities in spring rather than winter cereals.Barley crops have been found to have greater number of weed seeds than wheat crops, possibly because they receive fewer herbicide treatments (Thomas, Garthwaite & Banham 1996; Don 1997).

Summary: the diversity and abundance of arthropods taken as prey by birds differ between crops. This may be partially due to differences in vegetative structures between crops, and partially to the effects of management regimes specific to particular crops. Variation between crops in arthropod densities differ between taxonomic groups. For grey partridge chick food, spring sown cereals held higher densities than winter sown crops, whereas opposite applied to the densities of carabid beetles. There is some evidence that weed densities are higher in spring than in winter cereals.

1.4.3 EFFECTS OF MANAGEMENT OF NON-CROP HABITATS

1.4.3.1 Stubble

Stubble fields are often rich in spilt grain and weed seeds and comprise an important food resource for seed-eating farmland birds. Robinson & Sutherland (1997) showed that seed densities in the upper soil horizons on cereal (mean density = 1093 seeds m- 2) and linseed (4558 seeds m-2) stubbles were much higher than those on other crops including winter cereals (410 seeds m-2). However, Hart et al. (2002) found that other crop types (tilled fields, autumn-sown crops) had similar or higher seed densities to stubble. Seed densities also vary between different types of cereal stubble and are dependent on stubble management. Barley stubble had significantly higher seed abundance than wheat stubble (Moorcroft et al. 2002). Barley stubble is sparser and weedier than wheat stubble, as barley has a short straw and is harvested earlier. Undersowing may reduce seed densities. Non-undersown stubbles had seed densities of 1566 m-2 in November, whereas the equivalent density on undersown stubbles was 293 m –2 (Robinson & Sutherland 1999). Seed density was found to be high on organic stubble fields by Moorcroft et al. (2002), but food accessibility may be lower as a result of previous undersowing and greater ground cover inhibiting weed establishment. Stubbles, which had been sprayed post- harvest with herbicide, had the lowest seed densities (Robinson 2001).

The switch from spring to autumn sowing of most arable crops has reduced the availability of winter stubbles, thereby greatly reducing the amount of weed seed available during the winter (Campbell et al. 1997). This is believed to have affected the populations of seed-eating passerines, particularly corn bunting and cirl bunting Emberiza cirlus (Baillie et al. 1997). The quantity of seed available on the remaining stubble fields has also decreased significantly (Donald 1998; Robinson & Sutherland 1999).

6 The differences in seed densities between crop types reported by Robinson & Sutherland (1999) appeared to be sufficient to affect crop type preferences by foraging birds. Winter densities of four seed-eating species (skylark, yellowhammer, grey partridge and red-legged partridge) were positively correlated with seed density in the upper soil horizons and were often, but not always, highest in stubble fields. However, Hart et al. (2002) found yellowhammer and skylark field preferences were affected by crop type rather than seed density. Stubbles did not contain the highest seed densities but they was favoured by foraging birds possibly because the habitat provided better cover from potential predators than other crop types or because seeds in stubbles were more accessible to foraging birds.

Though undersown stubbles contain less food for seed-eaters in winter, they are of high value for invertebrate-feeding birds in spring and summer. Many invertebrates benefit from the lack of cultivation, as sown grass leys follow the harvesting of the arable crop (Barker, Vinson & Boatman 1997). The retention of overwinter stubbles was shown to increase carabid larvae numbers but did not affect adult abundance in the following summer (Gardner et al. 2001).

Summary: stubbles are generally perceived as an important winter food source for farmland birds. The switch from spring-sown to autumn-sown crops has reduced stubble area and food availability for many birds. Seed abundance may be similar to other crops, but it may also be more accessible for various reasons.

1.4.3.2 Set-aside

Set-aside was introduced as a voluntary scheme in 1988 as a means of reducing agricultural surpluses (Evans et al. 1997b). Set-aside was widely taken up in 1992 when Arable Area Payments to farmers became conditional on farmers leaving part of their land fallow as set- aside. Set-aside can be rotational (for one year only), or non-rotational (for longer periods). Set- aside must have a green cover over winter. The rotational set-aside is managed as part of the crop rotation, with non-rotational becoming semi-permanent. The vegetation cover on set-aside can be either naturally regenerated, industrial crops, sown grass or wild bird cover. Herbicides (usually glyphosate) may be used after April 15th on naturally regenerated set-aside to suppress weeds. Set-aside left to regenerate naturally is effectively traditional stubble, but remains fallow all summer, unlike crop stubbles.

Seed rain from set-aside can be very high (Jones & Naylor 1992). Set-aside can thus be a valuable source of seeds for birds, and of greater value than adjacent cropped farmland. Donald et al. (2001a) found that set-aside occupied by wintering skylarks had significantly higher weed seed availability than set-aside that was unoccupied, suggesting that there may be marked differences in food availability between different set-aside fields, possibly related to previous and current management. Draycott et al. (1998) found considerable variation in seed densities on set-aside in late winter, with many having very low densities. Even so, set-aside in general had significantly higher numbers of weed seeds, compared to arable fields. Chenopodium spp. and Polygonum spp. were the most common weed species found on all field types (spring sown, autumn sown and set-aside). These are important diet components of many farmland birds (Marshall et al. 2001).

Set-aside often supports a greater abundance and diversity of invertebrates compared to other crop types (Kennedy 1992; Moreby & Aebischer 1992; Holland et al. 1994b; Poulsen et al. 1998; Henderson et al. 2000b; Henderson, Vickery & Fuller, 2000a) but this is not always the case. For example, Gates et al. (1997) found that numbers of invertebrates were generally lower on set-aside than in adjacent field boundaries.

Skylark broods reared on set-aside were found to be fed more on soft-bodied invertebrates than those reared on grassland or spring cereals (Donald 1999; Poulsen, Sotherton & Aebischer 1998). More Hemiptera, spiders, Araneae and sawfly larvae were provisioned, and fewer adult

7 Lepidoptera, Coleoptera, Diptera and other Hymenoptera. This may reflect differences in prey availability between the crop types, as the abundance of skylark nestling food was also found to be much greater in set-aside than in grassland or spring cereals (Poulsen et al. 1998).

The invertebrate fauna of set-aside may depend on its cover, age and management (Moreby & Aebischer 1992; Moreby & Southway 2002; Moreby & Southway 2000). Cutting set-aside has been found to reduce densities of most arthropod groups (Moreby & Southway 2000). First-year set-aside has large numbers of small invertebrates that are preferred by skylarks whereas cirl buntings and yellowhammers prefer older set-aside, which has more large prey items such as orthopterans (Evans et al. 1997b). Rotational set-aside was preferred by birds to non-rotational set-aside, as the diversity and structure of the former type probably supported a greater abundance and availability of food (Henderson et al. 2000b).

Wild bird cover comprises a small but important proportion of set-aside cover. Boatman, Stoate & Watts (2000) showed that wild bird cover is preferred to farm crops by farmland seed-eaters. Seed abundance and variety is greater in wild bird cover than in other crops. A greater number of chick-food invertebrates were also found in wild bird cover. Moreby & Southway (2002) found that wild bird cover (either a cereal-based mixture, or a kale-based mixture) contained the highest numbers of invertebrates, followed by wheat and barley crops.

Summary: set-aside often supports higher abundances and diversities of arthropods compared to arable crops and grassland. Management regimes and enhancement (eg. wild bird cover) of set-aside affect the availability of food on set- aside, and some bird species may prefer one type to another.

1.4.3.3 Conservation headlands

Conservation Headlands are cereal crop edges (6m strips) that are not treated with insecticides in summer, and receive only selective herbicides (Potts 1997). They support more weed species, higher weed densities, and a greater weed biomass than fully-sprayed headlands. Sotherton (1992) found a 10-fold increase in broad-leaved weed diversity, with an attendant increase in weed numbers, in conservation headlands because of reduced spraying.

By not spraying 6m wide crop margins with herbicides and insecticides, insect abundance was found to increase by three times (de Snoo & de Leeuw 1996). Densities of partridge chick-food arthropods in conservation headlands may be two or three times as high as those of fully- sprayed headlands (Rands 1985; Sotherton, Rands & Moreby 1985; Sotherton, Boatman & Rands 1989; Chiverton & Sotherton 1991; Aebischer 1998). Aphid predator numbers also increased in relation to the number of aphids present (Chiverton & Sotherton 1991; de Snoo & de Leeuw 1996). Hassall et al. (1992) found carabid density and diversity greatest on Conservation Headlands, compared to control field margins. However, a more recent study found no effect on carabid activity when Conservation Headlands were present, compared to control field margins (Gardner et al. 2001), while Chiverton & Sotherton (1991) also found no significant differences in numbers of the two most common carabids between sprayed and unsprayed headlands. Butterfly numbers increased on Conservation Headlands compared to sprayed headlands (Dover, Sotherton & Gobbett 1990). Spring emerging butterflies also foraged more on field margins containing unsprayed headlands than on field margins lacking headlands (Dover 1997).

Summary: the reduced pesticide applications on conservation headlands appear to positively affect the abundance of non-crop plants and arthropods taken by farmland birds.

1.4.3.4 Field margins

8 Field margins can be categorised as “boundaries” (eg. hedges, windbreaks, verges, ditches etc; separating one field from the next), “boundary strips” (eg. grass margins, herbaceous strips, farm tracks; situated between the boundary and the crop) and “crop margins” (crop edges, the outer edge of the crop, sometimes cultivated separately as conservation, managed or unfertilised headlands) (Greaves & Marshall 1987; Thomas 1996). This section refers to the first two categories.

Field margins are important refuges for biodiversity on arable farmland (Boatman 1994; Hopkins 1997; Thomas & Marshall 1999; Pfiffner & Luka 2000). Several farmland bird species can be regarded as hedgerow specialists: eg. Whitethroat Sylvia communis, Linnet, Greenfinch Carduelis chloris and Yellowhammer (Fuller et al. 2001), indicating the importance of field margins to farmland birds.

The lack of suitable overwintering sites, such as field margins, may influence arthropod predator densities (Thomas, Wratten & Sotherton 1992). Sotherton (1984) found that densities of overwintering polyphagous predators were significantly higher on field boundaries (1.39/m- 2), wintersown cereals (1.41/m-2) and established grass leys (1.36/m-2), than on woodland (0.78/m-2), cereal stubbles (0.60/m-2), stubble turnips (0.77/m-2) and first-year leys (0.61/m-2). Individual species differed in their habitat preferences.

Butterflies tend to be associated with field margins rather than crops, as food and shelter are provided in the former (Hopkins & Feber 1997). Higher numbers of Lepidoptera larvae were thought to occur in adjacent mature field boundaries and grassy headland strips than in the crops themselves (Boatman 1998).

Andersen (1997) found that carabids and staphylinids were significantly more abundant in the boundaries between spring cereals and grass fields, than in the fields themselves. In a review of carabid densities, a range of 14. 5 to 1113 beetles m -2 (average of 233 beetle m-2) was found in field boundaries (Lovei & Sunderland 1996). Field margins have been shown to be significant in benefiting carabid populations (Hawthorne & Hassall 1995; Hopkins 1997; Lys & Nentwig 1994). Factors such as boundary structure (vegetation and soil characteristics, which influence micro-climate), pre-winter crop husbandry, food supply and parasitism may affect the dispersal and abundance of arthropods within field margins, indicating the complex interactions that determine overall densities in these areas (Thiele 1964; Coombes & Sotherton 1986; Dennis, Thomas & Sotherton 1994).

There is considerable movement between field margins and crop fields (Wratten & Thomas 1990). Field margins provide refugia for many arthropods, so their presence can affect the abundance of certain groups within crops, as well as within field margins. Crops had significantly higher numbers of predatory arthropods when adjacent to field margins (Dennis & Fry 1992). Variation in densities of over-wintering arthropods may also be related to the “landscape” scale matrix of field margins, so that abundances may need to be related to a farmscale, rather than a single-field scale (Dennis & Fry 1992).

Management techniques influenced the abundance of butterflies in field margins, with grass- cutting, herbicide use and sowing the most important factors (Feber, Smith & Macdonald 1996).

The provision of grass margins to arable fields can restore Orthoptera populations locally in intensive farmland (Hill et al. 1995). If wide field margins, seeded strips and good edge management are employed in a farm regime, arthropod diversity and abundance will be enhanced (Gardner & Brown 1998).

Beetle banks are raised strips planted with tussocky grasses, located across the centre of fields (Thomas et al. 1992; Thomas, Goulson & Holland 2001). They support large numbers of predatory insects, which move into the adjacent crop during the summer (Thomas et al. 1992).

9 Carabids are the most important group of epigaeic arthropods found in agro-ecosystems (Tischler 1980). Experimental studies by Lys & Nentwig (1994), Nentwig (1989) and Thomas, Wratten & Sotherton (1991) showed that beetle banks supported greater numbers of carabids than the surrounding crop, with densities of up to 1500 beetles/m2. Fields with 1.5 m wide beetle bank strips had 12 times the arthropod activity level of non-strip fields (Lys & Nentwig 1994). Thomas et al. (2001) found that beetle banks had lower overall densities of chick-food invertebrates than conventional field margins, but are important in the absence of well-managed hedgerows. However, the numbers of many key invertebrate groups did not differ significantly between beetle banks and other types of field margins (Thomas et al. 2001).

Field margins are vulnerable to pesticide spray drift. The effects of herbicide on spiders in an arable field margin were studied by Haughton et al. (1999). An arable field margin was sprayed with three rates of glyphosate (90 g active ingredient/hectare (a.i/ha), 180 g a.i./ha & 360 g a.i./ha) and control plots left unsprayed. The highest rate of glyphosate consistently reduced the total number of spiders, and the numbers of web-spinners, but not numbers of wandering spiders. Changes in vegetation structure and microclimate caused by the glyphosate were implicated in the reduction of numbers of spiders in plots receiving the highest rate of glyphosate. De Snoo (1994) found that weed cover and butterfly abundance increased significantly in unsprayed margins, though soil invertebrates such as carabids were less affected. High rates of mortality in butterfly larvae have been attributed to spray drift of pesticides (Longley et al. 1997; Longley & Sotherton 1997).

Summary: non-crop field margins tend to have higher numbers of invertebrates than the adjacent crop. They are also an important source of colonising and re- colonising invertebrates into an adjacent crop. The presence or absence of field margins, and their structure, are important determinants of a crop’s invertebrate fauna. Field margins also have to be viewed in a landscape context, rather than at a single-field scale.

1.4.4 EFFECTS OF POSITION WITHIN A FIELD

The variability of invertebrate abundance within a field can often be shown to be greater than the variability between fields under different management systems (e.g. Green et al. 1995). Within a cropped area, arthropod densities may differ between micro-habitats. Arthropod density was found to be highest within spring barley crops, compared to the tramline and edge of tramline areas of the crop (Odderskaer et al. 1997). However, food availability was reduced in the cropped areas, because of vegetation cover, and foraging areas reduced to some 5% of the field area. The spatial heterogeneity of arthropod distribution has important implications for appraising pesticide effects (Holland, Winder & Perry 2000). Most groups of beneficial arthropods show such distributions, and this may be why some large-scale trials do not detect expected reductions after pesticide applications.

Reddersen (1997) found that arthropod density, abundance and biomass decreased with increasing distance from the crop margins. This edge effect disappeared after 9 m, in both organic and conventional crops. Gardner & Brown (1998) found the edge effect less distinct on conventional fields than on integrated fields, the reverse of the results found in other studies (Reddersen 1997). Panek (1997) found higher numbers of Heteroptera in small arable fields (<10 ha.) than in large arable fields (10-50 ha.) He related this to a diverse crop mosaic, as well as less intensive pesticide use. In small fields there was no difference in Heteropera numbers between the edge, 100m in the field, or the field centre. In large fields, bug numbers were higher at the edge, compared to 100m in, and the centre. Green (1984) found higher insect densities 5m into a cereal field, compared to 50m into a field. Heteropterans were at higher densities 3m from the edge, compared to further in (Moreby 1995). These higher densities are probably related to

10 the presence of permanent cover at the field edge, acting as a reservoir for insects (Panek 1997). Insect densities, as exemplified by predatory arthropods, vary spatially within a crop, although a crop may appear to be a uniform habitat (Kromp 1999). Soil factors, prey densities, and heterogeneity of vegetation density and microclimate all influence arthropod densities (Powell et al., 1995).

Summary: arthropod densities vary spatially within a field because of soil factors, prey densities, vegetation structure and heterogeneity, microclimatic influences, crop management, and colonisation from edges. Because of this variability, it may be difficult to assess the impact of different management regimes and pesticide applications on arthropods.

1.4.5 EFFECTS OF AGRICULTURAL PRACTICES

Wilson et al. (1999) reviewed current knowledge of the effects of modern agricultural practices on invertebrate and plant foods found in the diets of farmland granivorous birds. Information on the effects of agricultural practices was collated from 900 references (Table 1.4). Table 1.4 also indicates the most-researched topics relating to farmland practices, with the effects of pesticides being particularly dominant. Agricultural practices varied in their effects on invertebrate orders and plant families. Pesticide applications, specialisation of farmland, loss of uncultivated field margins and increasing frequency of tillage generally reduced invertebrate abundance. Gardner & Brown (1998) also summarised the effects of agricultural practices on plants and invertebrates. Invertebrate numbers were negatively affected by inversion ploughing and pest control (chemical and biological). Numbers increased comparatively with practices such as direct drilling, green manure/intercropping, set-aside and stubbles, rotation with grass leys and the provision of permanent pasture.

Synthetic fertiliser, non-organic slurry and weed control (mechanical and chemical) decreased plant and seed abundance. Weed seed abundance was enhanced by the use of post-cropping incorporation and the presence of set-aside and stubbles. The loss of invertebrate-rich pastures is thought to have affected several bird species (e.g. cirl bunting: Campbell et al. 1997). Food availability has been found to be lower in solely arable areas than in areas of mixed farming (Aebischer 1998). In heterogeneous farming landscapes, there is a higher biomass of most insect groups compared to simplified landscapes (Panek 1997). Simplified landscapes are characterised by large fields and a lack of permanent cover. Intensification reduces non-cropped areas, which are important as refugia and food sources for invertebrates (Dennis et al. 1994; Andersen 1997).

11 Table 1.4. Number of references to specific agricultural operations and practices (adapted from Wilson et al. 1999).

Agricultural operation Number of references Application of insecticides 173 Application of fertilisers 154 Application of herbicides 138 Application of unspecified agricultural sprays 20 Application of fungicides 17 Use of avermectins 4 Application of manures 17 Ploughing regime 89 Management of uncropped field margins 29 Crop rotation/monocultures 28 Sowing grasses 10 Sowing arable crops 29 Field drainage 6 Biological control 5 Mechanisation 5 Seed-cleaning techniques 3 Pollutants 1

1.4.5.1 Invertebrates

Benton et al. (2002) found that changes in arthropod abundance were linked to changes in agricultural practice in Scotland, and that their findings were probably applicable to Britain overall. Intensive farm practices such as fertiliser input, pesticide usage and increased winter wheat sowing reduced arthropod abundance. Ewald & Aebischer (1999) also found that intensification (increased outputs per unit area of crop) of farming resulted in a decrease in biodiversity and abundance of many arable weeds and invertebrate species, affecting food availability. The loss of traditional rotational cropping is thought to have decreased invertebrate numbers in both autumn and spring-sown cereals. Aebischer & Ward (1997) showed that numbers of large Coleoptera, Lepidoptera/Symphyta and Arenae/Opiliones were significantly lower in both types of crops in 1994, compared to 1970. The difference may be related to the increasing use of foliar fungicides and insecticides over time on cereal crops (Aebischer, 1998). Krooss & Schaefer (1998) studied the effects of varying farming practices on rove beetles. Reduced tillage and fewer pesticide applications enhanced abundance, whereas no fertilisation led to reduced population densities because of sparse crops with unfavourable microclimates. All these studies considered the effects of a range of agricultural practices and it is often difficult to isolate the effects of particular ones.

Crop cultivation may reduce soil invertebrate populations, by direct mechanical damage, loss of insulating vegetation and the use of pesticides (Wilson, Taylor & Muirhead 1996a). Tillage often reduces arthropod populations, as many insects spend a life stage (eg. pupa) in the soil (Norris & Kogan 2000). Ploughing was shown to reduce numbers of linyphiid spiders by 89% whereas, over the same period, numbers on unploughed fields increased by 43-105% (Thomas & Jepson 1997). Inversion ploughing, a common practice on both organic and conventional farms, reduced invertebrate, particularly earthworm, abundance (Fuller 1998; Edwards & Lofty 1982b). The recent change from spring ploughing to later summer ploughing of cereal stubbles has adversely affected invertebrate food availability for birds in spring, by removing the fresh spring till (Newton 1998). Autumn ploughing has an adverse effect on carabid beetles overwintering as adults (Holland et al., 1996). Minimal tillage, where the soil is not turned over, results in increased survival of polyphagous predators, such as carabids, which are important in

12 bird diets (Reddersen 1994). Increased applications of farmyard manure increased earthworm densities on cultivated fields (Tucker 1992).

Under-sown leys once covered almost 25% of the arable area of Europe (Potts 1997). Increased land usage, the decline in under-sowing, and the reduction of fallow periods for land, has very probably resulted in decreases in the survival of insects such as sawflies that over-winter as eggs or larvae. These insects are important components of farmland bird diets (Barker et al. 1997; Wilson et al. 1999). Vickerman (1978) found that three times as many adult sawflies emerged from under-sown fields in the subsequent year, compared to cultivated fields. Potts (1986) attributed this effect to the damage caused by ploughing and cultivation. Where fields are undersown, sawfly densities remain high, as over-wintering insect pupae are not affected by cultivation after harvest (Aebischer 1998). Under-sown crops are weedier and more attractive to invertebrates than conventional crops (Aebischer 1998). Under-sowing may increase natural enemy abundance (Burn 1989).

The adoption of pure arable systems instead of mixed farming may be associated with declines in Coleoptera, Lepidoptera, Orthoptera and Arachnida populations (Wilson et al., 1999). Conversely, some common tipulids (Diptera) may increase in improved grassland swards, as do many hemipterans in arable monocultures (Wilson et al. 1999). Aebischer (1998) suggested that food availability is lower in purely arable areas, compared to areas of mixed farming.

Bruce et al. (1999) assessed the effects of sewage sludge on euedaphic and hemiedaphic Collembola in grassland. Five different treatments: uncontaminated (i.e. low levels of heavy metals) digested sludge; uncontaminated undigested sludge; zinc-rich digested sludge; copper- rich undigested sludge and no sludge control did not influence the overall abundance of Collembola in the study area, but significant differences were found at the species level. Seasonal and successional effects were also found and, for most species, these were more pronounced than the effects of sludge treatment.

Summary: modern farmland practices relating to the increasing intensification of farmland, generally have an adverse effect on invertebrates. Practices such as increased pesticide usage, loss of uncultivated field margins, increased tillage, and the decline in under-sown crops have all been shown to decrease food availability.

1.4.5.2 Plants

Important plant items in the diet of granivorous farmland birds include: cereal grain, knotgrasses and persicarias (Polygonum), chickweeds (Stellaria) and goosefoots (Chenopodium). Asteraceae, Fabaceae and Brassicaceae are also widely taken (Wilson et al., 1999). The latter include crop components, such as clovers and oilseed rape. Late summer ploughing has removed much of the spilled grain and other seeds that were formerly available (Newton 1998). There have been widespread reductions and declines in the diversity and abundance of many food plants on farmland as a result of modern farm techniques, such as frequent tillage, grassland management, herbicides and competition from farmland crops (Sotherton & Self 2000). Wilson et al. (1999) suggested that the main factors affecting grass seed and cereal grain availability for birds have been more efficient harvesting and storage of cereals, more frequent harvesting of grass, grazing intensification, early cultivation of cereals, and the elimination of under-sowing.

In contrast, some food plants may have increased in availability: e.g. Poa spp., curled dock (Rumex crispus), chickweeds, mouse-ears (Cerastium), and some Asteraceae, as they respond well to practices such as increased nitrogen application, frequent cutting or grazing (Wilson et al. 1999). Black-grass (Alopecurus myosuroides) and Barren Brome (Bromus sterilis) have increased in abundance because of the failure to bury seed during non-inversion cultivation (Sotherton & Self 2000). Improved harvesting efficiency and birds being unable to access grain

13 stores because of measures to improve hygiene have also reduced grain availability (Brickle & Harper 2000). The major change in the number of weed species in the most important arable crop (winter wheat) occurred in the late 1970s, with the introduction of ioxynil + bromoxynil, which controlled a broad spectrum of weeds (Marshall et al. 2001).

Crop sowing date may also affect some broad-leaved weed species. Species that set seed over autumn and early winter may not set seed when winter cereal is sown immediately, but will on stubble prior to spring-drilling (Sotherton 1991; Sotherton & Self 2000). Spring sowing of wheat significantly increased weed germination and performance, and thereby the availability of weed seeds and invertebrates (Cosser et al. 1997). The introduction of continuous cropping is likely to have resulted in an increase in some weed populations, as annual rotations were an efficient method of controlling weed infestations (Rademacher, Koch & Hurle 1970).

Sowing practices may influence the availability of exposed cereal seed on fields (Pascual et al. 1999). Sowing depth, seedbed condition, and sowing method influence seed densities on cereal fields. Headlands often have higher surface seed densities than the main-field, due to poor soil conditions caused by more traffic, and double sowing and unintentional broadcasting of seed.

Application of fertilisers, especially nitrogen, has a major effect on plant species composition, and reduces the abundance of some plant species (Wilson, Boatman & Edwards 1990; Marshall et al. 2001). Fertiliser drift is thought to have a greater impact than herbicide drift on margin flora (Marshall et al. 2001).

Intensive management leads to a rapid decrease in abundance of weed species in the seed-bank (Roberts 1962), but numbers soon increase again if management is relaxed. In the TALISMAN project, spring sowing of crops was re-introduced, and herbicide usage halved (Squire, Rodger & Wright 2000). Most weed species increased in abundance, and some species increased dramatically. These latter were economically important weed species (Alopecurus myosuroides, Galium aparine, Papaver sp., Anagallis arvensis and Chenopodium album), which increased to such massive abundances (>10,000 m-2) as to have a potentially detrimental effect on the crop.

The trend to minimal cultivation of cereal crops will encourage annual grass weeds, but annual broad-leaved weed abundance will decline (Froud-Williams, Chancellor & Drennan 1984). Herbicides and species-specific periodicity of germination were thought to be important factors influencing these trends. More recent studies have, however, found that there is a general increase in weed species with reduced tillage (Torresen & Skuterud 2002). Tillage has different effects on broad-leaved weeds, depending on the particular species’ ecological characteristics (Pollard & Cussans 1981). Separate studies have found contrasting results on the same weed species (eg. Froud-Williams et al. 1984; Torresen & Skuterud 2002).

Summary: as for invertebrates, modern farming practices have significantly reduced weed plant and seed (both crop and weed) availability. Frequent tillage, increased fertiliser usage, improved harvesting and storage of cereals, increased herbicide usage and the switch to autumn-sown crops all adversely affect broad- leaved weed populations. A few weed species may have increased as a response to some of these practices.

14 1.4.6 EFFECTS OF PESTICIDES

1.4.6.1. Insecticides: factors affecting their impact on non-target taxa

The effects of insecticides on arthropod diversity and abundance may vary depending upon weather effects, crop type and growth stage, and differences in arthropod species ecology (e.g. Vickerman 1992; Young et al. 2001). Spatial distribution, the scale of the trial and natural population fluctuations also influence test results (Holland et al. 2000). The impact of an insecticide is also mediated by a combination of chemical, toxicological, ecological and operational factors (Jepson 1989). Many studies have, however, indicated an adverse effect on non-target arthropods (Barrett 1968; Vickerman & Sunderland 1977; Potts 1986; Theiling & Croft 1989; Inglesfield 1989a; Everts et al. 1989; Davis, Lakhani & Yates 1991; Wilson et al. 1999).

Holland et al. (2002) found insecticide effects only in spring beans, and not in winter wheat, potatoes, peas, sugar beet, linseed and lucerne. Spring beans were sprayed twice (mid-May and mid-June); other crops were sprayed once in mid-May. Invertebrate numbers subsequently recovered as a result of reinvasion from surrounding fields. Although carabids are affected by pesticides in laboratory tests, other factors in the natural environment such as temperature, scale and re-immigration may be important in determining numbers (Heimbach & Baloch 1994; Heimbach & Abel 1994; Purvis 1992). Chiverton (1984) found that pitfall catches of carabids increased after pesticide treatment, even though prey species declined. The apparent increase was perhaps due to increased activity of hungry survivors.

Basedow (1991) found the main factors affecting carabids included crop rotations, field size and margins, as well as insecticides. Booij & Noorlander (1988) and Hance, Gregoire-Wilbo & Lebrun (1990) also considered that carabids were more affected by crop type than by pesticide applications. Luff, Clements & Bale (1990) found that grassland carabid populations were affected by insecticide use and other management, but that soil water and density were the main factors affecting numbers.

Impact of particular insecticides may vary depending upon the timing and frequency of application but the evidence is not consistent. For example, Brickle et al. (2000) showed that corn bunting invertebrate chick-food density was negatively correlated with the number of insecticide applications, both on cereal fields and on other crop types. However, Holland et al. (2002) found that raising the number of insecticide applications did not always result in a decrease in invertebrate abundance. Indeed, for winter oilseed rape, there was an increase in invertebrate abundance, and for other crops (winter wheat, spring barley, winter barley) no discernible effect was apparent. A significant decrease was noted only in spring beans when extra insecticides were applied.

Different types of pesticides differ in their impact depending upon the type of active ingredient and formulation. For example, Jepson, Efe & Wiles (1995) recorded that dimethoate (an organo-phosphate) and deltamethrin (a pyrethroid) had similar levels of toxicity in the laboratory. However, in the field, it was found that dimethoate had a severe impact on invertebrates, whereas the impact of deltamethrin was far less (Vickerman et al. 1987). Similarly, Cole et al. (1986) found that c.10% of non-target species showed significant reductions in numbers, which persisted for two months after autumn spraying of dimethoate, whereas a summer application of cypermethrin affected 4-6% of non-target species for a month. Pyrethroid sprays could have a greater effect on flying insects, because of their contact knock- down action. Pyrethroids also have repellent effects on some insects, particularly Hymenoptera. Pirimicarb is a selective insecticide, controlling aphids, but not affecting other non-target arthropods (Ewald & Aebischer 1999). Granular insecticides incorporated in the soil before crop

15 planting can have a major impact on soil invertebrates, but less so on flying or foliage invertebrates (Tones et al. 2000).

Thieling & Croft (1988; 1989) reviewed the effects of pesticides on arthropods, from the analysis of their SELCTV database. Comparisons were made between the various pesticides, and their effects on arthropods. Sub-lethal effects were also reviewed, as these also influenced population densities. Burn (1989) showed that groups of arthropod predators, defined by their dispersal abilities and over-wintering habitats, differed in their susceptibility to long-term effects of pesticides. Poorly-dispersing predators were highly susceptible, whereas groups that were more dispersive were less affected. Indirect effects were also discussed. Reductions in prey availability, reproductive rate and alterations in micro-habitats may also indirectly reduce arthropod populations.

Vickerman (1992) found that dispersal ability was the most important factor affecting long-term susceptibility to pesticides. Recovery times on farmland may be longer than surmised from small-scale trials, if large contiguous areas are sprayed. Many trials are carried out on smaller areas, where recolonisation may occur more readily (Campbell et al. 1997). Trials on differing sizes of plots showed that the scale of treatment affects the recovery of the invertebrate population (Duffield & Aebischer, 1994). Groups of arthropods also differed in their patterns and rates of recovery. Staphylinidae recovered the fastest, followed by Linyphiidae then Carabidae, due to their relative mobility. These groups colonised from the outside in, whereas aphids and springtails recovered from the inside outwards, as predation pressure was less (Duffield & Aebischer 1994).

Summary: The effects of insecticides on arthropod diversity and abundance may vary depending upon weather effects, crop type and growth stage, differences in arthropod species ecology, the active ingredient in the insecticide, and spatial scale of application.

1.4.6.2. Insecticide: levels of impact on non-target taxa

Wilson et al. (1999) reviewed the effects of insecticides on invertebrates. The number of detrimental (d) and non-detrimental (n) effects was given by the notation (d: n), to indicate the overall effects of insecticides on each group. Coleoptera (48:14), Diptera (8:1), Lepidoptera (5:0), Hymenoptera (22:11), Hemiptera (7:1), Orthoptera (2:0), Arachnida (17:6), and Annelida (5:3) were all generally reduced in numbers by insecticides.

Three long-term projects funded by MAFF (now Defra) have studied the environmental effects of contrasting pesticide regimes. The Boxworth project indicated that some species were susceptible to intensive pesticide use in winter, whilst others appeared to benefit (Greig-Smith, Frampton & Hardy 1992). The SCARAB project found that polyphagous predators were not affected over the long-term, although chloropyrifos did cause short-term reductions in some groups (Young et al. 2001). The TALISMAN project found only limited and short-term effects on non-target arthropods by insecticide spraying (Young et al. 2001). It was suggested that spring and summer spray applications are intercepted by crop foliage, and non-target invertebrates are, therefore, protected. Also, in winter arthropods are less active, and less susceptible to treatments. Spring and summer applications of deltamethrin had no effect on autumn-breeding carabids, but winter applications reduced carabid numbers by 30% (Matcham & Hawkes 1985). Other studies have also shown either decreased invertebrate food availability, or little effect (Rands 1985; Cigli & Jepson 1995; Moreby et al. 1994).

De Snoo (1999) found that phytophage insect presence and abundance increased significantly on unsprayed margins of winter wheat, sugar beet and potato crops. Butterflies in hedgerows have been shown to be susceptible to spray drift from insecticides such as deltamethrin (Davis

16 et al. 1991; Cilgi & Jepson 1995). Initial mortality in Coleoptera after spraying may be high, between 60-90%, but some taxa may recover their abundance after a month, while others may remain suppressed for several months (Brown, White & Everett 1988). Purvis, Carter & Powell (1988) recorded a 70% decrease in carabid numbers after pyrethroid spraying, but complete recolonisation occurred within 2 months. Pyrethroids are generally considered to have no long- term adverse effects on entomophagous arthropods (Inglesfield, 1989b). Some autumn-breeding carabids had summer populations reduced by 50%, but rapid dispersal recovered these populations. Barrett (1968) found that Sevin (a carbamate insecticide) reduced arthropod biomass and numbers by 95%, but after seven weeks biomass, though not total numbers, recovered.

Casteels & de Clercq (1990) studied the effects of insecticides on epigeal arthropods in winter wheat. Parathion and dimethoate reduced carabid numbers by 28-29%, whilst pirimicarb, fenvalerate and phosaline had a non-significant effect. Parathion and dimethoate also reduced staphylinids by 67% and 31% respectively. Fenvalerate was most toxic to spiders (30% reduction), and phosalone to springtails (23-47% reduction). Effects were most important in the first weeks after application.

Cole et al. (1986) found that winter pesticide applications reduced Carabidae and Linyphiidae populations only until the following spring. Recolonisation is an important factor in population recovery. A reduction in beetle larvae did not affect the numbers of adults trapped the following spring (Cole et al., 1986). Basedow (1987) found an 81% decline in trapping rates, and a 90% decrease in biomass in carabids between 1971-1974 and 1978-1983, caused by increases in insecticide applications, particularly parathion.

Aebischer (1990) found that the use of dimethoate, an aphicide, suppressed sawfly numbers to such an extent that it would take seven years for numbers to fully recover. Sawflies are an important component of partridge and pheasant chick diets. Sotherton (1990) also found that synthetic pyrethroids adversely affected sawfly caterpillar numbers. The impact of a single treatment of a broad-spectrum insecticide can last several years because of the sawfly’s slow reproductive rate (Aebischer, 1990).

Some pesticides may have favourable indirect effects on some species (Frampton et al. 1992). Their predators may be reduced in numbers, thereby enhancing the prey’s survival and numbers. Springtail abundance was reduced by chloropryifos, but not by cypermethrin and pirimicarb (Frampton 1999). Springtails actually increased after cypermethrin applications. Competitive interactions may also result in some groups or life-stages increasing in abundance after pesticide use. Vickerman (1992) and Duffield & Aebischer (1994) found increased numbers of carabid larvae after spraying, possibly because adult numbers, and hence competition or predation, were reduced.

For aphid control, compounds containing pirimicarb were found to be less harmful to non-target arthropods (Anon. 1997). Insecticides differed in their effect on Heteroptera (Moreby, Sotherton & Jepson 1997). Phosalone and pirimicarb had little effect on heteropteran numbers, whereas demeton-S-methyl and dimethoate had significant short-term effects (Sotherton, 1991; Moreby et al., 1997). Dimethoate was also found to reduce densities of most non-target arthropods in cereals (Vickerman & Sunderland 1977). Dimethoate, parathion, phorate and fonophos are extremely toxic to carabids, whereas pirimicarb, fenvalerate, phosalone, chlorofenvinphos and carbofenothion had less or no effect (Casteels & de Clercq 1990; Campbell et al. 1997). However, dimethoate drift was found to have no long-term effect on non-target invertebrates, either in a crop or its field margin (Tones et al. 2000).

Summary: measuring the effects of insecticides on food availability is difficult to assess, due to bias in sampling methods caused by trap effectiveness, trap type, spatial variability, insect activity, temperature, ground cover, vegetation structure,

17 micro-habitat preferences, trial scale, natural population fluctuations and crop effects. Insecticide impact is also mediated by a combination of chemical, toxicological, ecological and operational factors. Many studies have found that insecticides reduce invertebrate numbers but this may be a short-term effect in some instances. Long-term (30 years) declines in selected arthropod taxa have been recorded from arable farmland.

1.4.6.3. Herbicide: effects on weeds

Recurrent use of herbicides can detrimentally affect the numbers and diversity of weeds over time (Fryer & Chancellor 1970), However, not all declines in weed numbers in fields can be attributed to changes in herbicide use, and some are due to changes in cropping patterns (Marshall et al. 2001). Wilson et al. (1990) considered that changes in sowing dates, seed cleaning improvements and increased fertilisation may be at least as important as herbicides in determining weed abundance. The effects of herbicides are mediated by herbicide characteristics, weather, soil, crop conditions (Boatman 1988).

Weeds are killed by herbicides before they can produce seeds, and this leads to progressive depletion of the seed bank. Linnets responded by switching to oil-seed rape as charlock Sinapsis arvensis and other species became rarer due to herbicide use (Campbell et al. 1997; Moorcroft & Bradbury 1998). Comparisons of organic v. conventional cereals (Brookes et al., 1995; Halberg 1997; Moreby et al. 1994), and sprayed v. unsprayed field headlands (Chiverton & Sotherton 1991; Sotherton et al. 1985), have demonstrated the scale of reduction of arable weed densities following herbicide application. Powell, Dean & Dewar (1985) found that autumn herbicide applications reduced weed numbers by over 90%, and that weed populations were still reduced the following April.

Ewald & Aebischer (1999) found that broad-leaved weeds were affected by dicotyledon- specific herbicide use, and grass weeds by broad-spectrum herbicide use. Contact and contact + residual herbicides reduced the abundance of both groups. No significant temporal trends were found in the 25 years of the Game Conservancy Trust (GCT) Sussex study, however. This may have been because herbicide use had already altered the weed flora at the beginning of the study. Herbicide use in spring and summer, rather than in autumn, reduced densities of Fallopia convolvus, Sinapsis arvenis, Viola arvensis, Chenopdium spp., mayweeds and Capsella bursa- pastoris, several of which are important in farmland bird diet (Table 1.3). However, Whitehead & Wright (1989) found that the weed species most widespread in 1967 had maintained their ranges since then, despite increased herbicide use.

Herbicides also have an effect on weed seeds in set-aside, as a result of their usage in the previous crop (Campbell et al. 1997). Robinson & Sutherland (2002) noted that there is evidence of declining seed banks in arable land in Britain, as a result of persistent herbicide use. A similar trend has been reported in Denmark (Jensen & Kjellsson 1995). Viable seed density declined by 50% in Danish arable fields between 1964 and 1989.

Summary: as with insecticide usage, herbicide effects are confounded by other variables such as crop management and natural variation. Generally, increased herbicide usage reduces overall weed and seed abundance, but some weed species may be more tolerant to herbicide effects.

18 1.4.6.4 Herbicides: indirect effects on invertebrates

Herbicides can reduce the availability of invertebrate food for birds (Moreby & Southway 1999) but the mechanisms by which this occurs, and the scale of the effects on bird populations are, in many cases, not fully understood (Campbell et al. 1997; Marshall et al. 2001). Herbicide application reduces the abundance and diversity of weeds, thereby affecting herbivorous insects, which are important chick-food diet components (Sotherton 1982; Sotherton 1991). Field experiments entailing the cessation of herbicide applications resulted in greater weed growth and insect densities in unsprayed plots than in those receiving herbicides (Sotherton 1991). Moreby & Southway (1999) found that herbicide-treated winter cereal headlands had significantly lower weed density and diversity, and lower numbers of invertebrates, particularly those important in farmland bird diet (Heteroptera, Auchenorrhyncha, Coleoptera), compared to non-herbicide treated headlands.

Southwood & Cross (1969) suggested that the introduction of herbicides in the 1950s destroyed many of the host plants of invertebrates, and probably halved their abundance within cereals. Four of the five most important partridge-chick food groups are dependent on broad-leaved weeds, and herbicide use thereby reduces their abundance (Potts 1997). Chiverton & Sotherton (1991) found large differences in gamebird chick-food arthropod abundance between herbicide- treated and untreated plots. Unsprayed plots also had higher densities and more species of weeds.

Weed species vary in the diversity of insect species supported. Three target weed taxa (Stellaria media, Poa annua and Polygonum spp. including Fallopia convolvulus) support a high diversity of insects. The Asterceae have a particularly rich fauna with Senecio vulgaris and Cirsium arvense having around 50 insect species associated with them. Sonchus oleraceus, Tripleurospermum inodorum and Sinapis arvense (latter in Brassicaceae) are also species rich (Marshall et al. 2001). Reducing or eliminating certain weed species thereby also reduces the abundance and availability of invertebrates in a crop. Arthropod density has been shown to be up to three times greater in weedy fields than weed-free fields (Potts & Vickerman 1974). The presence of weeds in cereal fields benefits many arthropods, including Carabidae and Staphylinidae (Vickerman 1974; Moreby et al. 1994).

Herbicide usage induces species replacement; as one weed species is eliminated, another replaces it, often from an entirely different family (Freemark & Boutin 1995). This can lead to marked effects on invertebrate abundance, many invertebrates being host-specific, and may influence food availability. Hald & Reddersen (1990) found that herbicides had an immediate negative effect on arthropod species diversity and abundance in conventional fields. Herbicides reduced the numbers of arthropods by 50%, and their biomass by 66%, in barley fields, compared to “weedy” barley fields (Southwood & Cross 1969).

Aebischer (1991) found that cereal invertebrate numbers halved between 1970 and 1990, and this was linked to an increasing use of herbicides. Sotherton (1982) found that knotgrass beetle Gastrophysa polygoni larvae had significantly higher mortality on host plants treated with 2-4D herbicide, than on untreated plants.

Effects of herbicide application on invertebrate prey of birds not always negative. For example, higher numbers of large beetles have been captured in cereal crops with few weeds, suggesting that clean (herbicide-treated) crops are easier for the beetles to colonise (Powell et al., 1985). Overall numbers of carabids caught were almost twice as high in herbicide-treated crops, as in untreated crops, and higher in crops treated twice. This was due to the larger species being more abundant, or possibly the capture methods used measuring increased activity rather than abundance. Movement is also easier in clean crops, so beetles may be easier to capture.

19 Increases in numbers of springtails after herbicide applications have been attributed to increased rates of litter input into the soil (Conrady 1986).

Differences in the type of herbicide used also affect insect food availability. Vickerman (1974) found that metoxuron + simazine control of rough meadow-grass Poa trivalis reduced insect biomass by 43% compared to weed control by mecocrop.

Summary: herbicides may reduce the abundance of arthropod prey through the destruction of host plants but other factors may also be important. Differences in invertebrate species ecology, such as mobility and over-wintering strategy, and interactions between species (e.g. predator-prey relationships) mean that some species may be more abundant in herbicide-treated crops than untreated crops.

1.4.6.5 Fungicides

Many fungicides have no significant effects on Heteropteran populations (Moreby et al. 1997). However, some formulations do significantly reduce populations of beneficial arthropods because of their insecticidal properties e.g. pyrazophos (Sotherton, Moreby & Langley 1987; Frampton 1988; Sotherton & Moreby 1988). Carbamate fungicides (and molluscides) are toxic to soil invertebrates, and reduce their populations (Tucker 1992). Sotherton (1989) reviewed the mortality effects of 27 single active-ingredient foliar fungicides on hoverfly and leaf beetle larvae. Most fungicides had very low mortality impacts, except for pyrozophos. Springtails have been found to be susceptible to fungicides (Frampton 1988). Rove beetles Tachyporus spp. declined substantially in numbers between 1970 and 1990 in a Sussex study, possibly because they feed on fungi as well as live prey, and foliar fungicides may have thus indirectly affected them (Aebischer 1991).

1.4.7 EFFECTS OF WHOLE FARM AGRICULTURAL SYSTEMS

1.4.7.1 Integrated farming systems

Integrated farming systems are defined as “farming systems that produce high quality food and other products by using natural resources and regulating mechanisms to replace polluting inputs and to secure sustainable farming” (IOBC 1993). Chemical and other inputs are minimised, and farming managed on an integrated structure that minimises environmental impacts. Several research projects studying integrated farming systems have been conducted in recent years (Holland et al. 1994a). The results of these projects in relation to food availability are outlined below.

The Boxworth project: Three pesticide regimes were applied to three separate blocks of fields. These were high input, “supervised” and “integrated” (see Greig-Smith & Hardy (1992) for details). Overall, densities of arthropods were 50% lower in high input fields than under the other two regimes. Effects were variable, some groups such as Lepidoptera, thrips, and some dipterans were substantially reduced, but overall effects on beetles, aphids and plant bugs and cereal leaf miners were smaller (Vickerman 1992). Ground beetles, springtails and spiders showed a very slow recovery after pesticide input was reduced, indicating that pesticide effects can last for years (Holland et al. 1994a). Variations in life-cycle strategies among Coloepteran species affected their susceptibility to pesticides (Vickerman 1992).

The SCARAB project: SCARAB was designed to follow Boxworth, over a wider range of conditions, and was concerned primarily with environmental effects (Holland et al., 1994a). Two pesticide regimes, current practice and reduced input were applied. Broad-spectrum insecticides caused reductions in some invertebrate groups. The severity of pesticide effects varied between years, species, crops and locations. No significant differences between weed cover in conventional and reduced-input fields were found (Green et al. 1995). Holland et al.

20 (1996) found that there were no significant differences in carabid activity between conventional and integrated systems. Differences in activity were due to site and field characteristics, rather than treatments (insecticide input, crop type and rotation). However, a case study of integrated v. conventional fields found the greatest carabid diversity and densities on conventional fields (Gardner & Brown 1998).

The TALISMAN project: This was more concerned with the economic impacts of low input regimes (agrochemicals and nitrogen). Pesticides affected invertebrate numbers, but also, in the absence of pesticides, invertebrate catches showed considerable variation. This made it difficult to evaluate the importance of the pesticide effects (Hancock et al. 1995). In general, yearly variation and crop rotation affected invertebrate populations more than pesticide applications (Young & Ogilvy 2001). Differences in weed seeds were found between oilseed rape and linseed plots: higher densities of Brassica seeds were found in oilseed rape plots, and higher densities of Poa seeds in linseed plots.

The RISC project: RISC was similar to TALISMAN in design, but took into account the different farming practices utilised in Northern Ireland. Carabidae catches differed between treatments. Individual species differed in their responses to treatments, with some having higher densities, and some lower under the same treatment (Holland et al. 1994a).

The LIFE project: This project compared conventional and fully integrated farming systems. Catches of some beneficial invertebrates (Carabidae, Staphylinidae, Linyphiidae, Diplopoda) increased markedly under the lower input regimes. Rotation, chemical inputs, field and crop factors did not significantly affect overall invertebrate numbers (Holland et al. 1994a).

LINK (Integrated Farming Systems). Holland et al. (1996) studied the effects of integrated farming systems, as opposed to conventional systems, on Carabidae. The overall results were that non-target arthropods and earthworms had higher populations in lower-input and integrated regimes, compared to conventional regimes (Holland et al. 1994a).

Summary: integrated farming systems, with reduced chemical and nitrogen inputs, generally showed increased non-target invertebrate populations compared to conventional farms. These increases could also be attributed to other factors such as greater weed species diversity and abundance, improved field management and a change to non-inversion tillage practices. Site and field characteristics, as well as yearly variation and crop rotations, were also important modifiers of invertebrate abundance in some studies.

1.4.7.2 Systems using genetically-modified crops

Genetically-modified (GM) crops may influence food availability, by reducing insect and seed- food abundance within fields (Fuller, 2000). Watkinson et al. (2000) simulated the effects of the introduction of genetically modified herbicide-tolerant (GMHT) crops on weed populations and the consequences for seed-eating birds, using fat-hen Chenopodium album as the model weed. They predicted that weed populations might be reduced to low levels or practically eradicated, depending on the exact form of management. Buckelew et al. (2000) have shown that herbicide- resistant soybean crops tend to have lower insect population densities. The effect is mediated through the impact of weed management, rather than the direct effects of herbicides.

21 1.4.7.3 Organic systems

Organic farmland comprises only 3% of UK agricultural land. Nonetheless, it is believed to support a greater diversity and abundance of species [plants, invertebrates, birds] than conventional farmland (Azeez 2000). A comparison of organic vs. an integrated arable system in Germany indicated that the abundance and diversity of weed flora increased on the organic system (Gruber, Handel & Broschewitz 2000). No-plough tillage increased weed abundance, notably grass species. Food abundance is often higher than on conventional farms (Fuller, 1998). For example, Hald & Reddersen (1990) found that 1.4 - 1.8 times the number of bird- food arthropods were present on organic farms compared to conventional farms. Brookes et al. (1995) found total numbers of invertebrates to be similar on organic and conventional cereals, but different groups differed in abundance on each type. A study of the carabid beetle fauna in fields undergoing conversion to organic production in Europe, demonstrated that increased activity-density could occur (Andersen & Eltun 2000). The increase in the number of carabids could in part be explained by the increase in the number of weed species present. Staphylinid beetles tended to show the opposite effect, which may be a response to competition from Carabidae.

Azeez (2000) summarised the results of research on organic farms, and that there were three times as many non-pest butterflies in organic crop areas, and one to two times as many species of spiders. Feber et al. (1997) found that vegetation differed significantly between organic and conventional sites, and this had a significant impact on spider communities. Abundance and diversity of spiders increased with increasing understorey vegetation. Higher densities of earthworms have also been found on organic than conventional cereal fields (Brookes et al. 1995).Numbers of aphids on organic are also thought to be lower than those on conventional farms (Azeez 2000).

Azeez (2000) has suggested that there are five times as many wild plants in arable fields, and 57% more species. Brookes et al. (1995) found weed cover to be higher in organic than in conventional cereals. Also, broad-leaved weeds dominated in organic cereals, and grasses dominated in conventional cereals. However, they found no difference in overall seed abundance. Intercropping is a common practice on organic farms, and results in a greater diversity of polyphagous predators compared to conventional wheat monocultures (Altieri & Letourneau 1982). Feber et al. (1997) considered that the pattern of cropping, rather than crop management, was the important factor in maintaining butterfly populations on organic farms. Oilseed rape is rarely found on organic farms, whilst grass clover leys, which are more attractive to butterflies, are more frequent on organic farms. Organic fields are considered to be more beneficial to birds because of their greater seed and invertebrate food availability (Brookes et al. 1995; Fuller, 1998; Reddersen 1997). Fuller (1998) listed the mechanisms by which food availability is enhanced on organic farms compared to conventional farms: reduced pesticides, use of animal and green manures, and a higher diversity of crops including rotational grass.

Summary: organic farms often have greater food availability than conventional or integrated farms. This may be due to the prevalence of mixed farming, crop rotation, spring sown crops, the avoidance of agrochemical usage, the maintenance of non-crop habitats such as hedges and field margins, green manuring, and cereal crop undersowing.

1.4.8. WEATHER EFFECTS

Weather may affect the availability of arthropod prey. Temperature has a direct effect on invertebrate activity, and can account for much of the variation in sampling (Tones et al. 2000). Temperature affects insect abundance, with increases beginning in April (Bryant 1975). Weather was shown to affect arthropod abundance in Scotland by Benton et al. (2002).

22 Springtail numbers collapsed after two dry summers in Sussex, before recovering in subsequent years to pre-drought levels (Aebischer 1991). Grasshoppers are more active on warm days, and hence more available as prey (Brickle & Harper 1999). Some arthropod groups (Heteroptera, Pscoptera and Lepidoptera) were perhaps more susceptible to winter climatic factors (Benton et al. 2002).

High winds can influence penetration of pesticides, by opening up the crop canopy (Tones et al. 2000). Pesticide penetration can differ greatly between crops because of different canopy structure. In broad-leaved crops, pesticide penetration is more variable compared to thin-leaved crops such as cereals. Aebischer (1991) found that trends in invertebrate numbers were so similar on farms with different management methods and intensities, that either climatic factors were of over-riding importance, or that agricultural changes have occurred on such a wide scale as to affect even the least intensive farms.

Rainfall also affects invertebrate activity. In rain, corn buntings switched from provisioning invertebrates to provisioning cereal grain, presumably because insect activity, and thereby availability, was reduced (Aebischer, Green & Evans 2000). Fewer arthropods and more grain seeds are fed to cirl bunting chicks on wet days, as invertebrates become harder to find (Sitters 1991). Spring weather (specifically drought conditions in May) may affect the availability of arthropod prey, reducing arthropod abundance (Frampton, van den Brink & Gould 2000). Rainfall can also be a limiting factor in sampling. Micro-habitat requirements may also affect susceptibility to exposure to pesticides. Increasing dryness in recent years has reduced food availability for insectivorous birds in upland areas, as wet moorland areas with concentrations of insects have dried out (Fuller et al. 2002).

McCracken, Foster & Kelly (1995) studied leatherjacket (Tipula spp.) populations in Scotland. Numbers in pastures were related to aspect, silage use, tendency to waterlogging in the pasture, organic fertiliser use, sward height, numbers in previous years and prevailing wind direction. Standard soil characteristics did not have any effect. Studies such as this indicate the complex interactions of factors that determine abundance in arthropod populations.

In addition to immediate effects on arthropod behaviour, weather may have long-term effects on arthropod populations in arable crops. For example, annual sawfly density on some West Sussex farms was related, with a one-year lag, to summer rainfall and temperature, in addition to the proportion of cereal fields that were undersown (Aebischer 1990).

Summary: weather factors, such as rainfall, temperature and wind, can affect invertebrate food availability, and can mask the effects of other factors, such as pesticides. Weather variables also interact with other factors such as pesticide effects to influence arthropod populations.

1.4.9. EFFECTS OF FOOD ACCESSIBILITY AND PREDATION RISK

Resource-independent factors such as food accessibility and predation risk can also affect food availability. Many species of ground-feeding birds on agricultural land have been shown to forage preferentially in sites that are relatively sparsely vegetated, irrespective of food abundance (skylark: Buckingham 2001; granivorous passerines: Moorcroft et al. 2002; starling: Whitehead, Wright & Cotton 1995; waders: Milsom et al. 1998). Morris, Bradbury & Wilson (2002b) suggest that both abundance and accessibility may determine patch selection by foraging birds. They investigated invertebrate communities and crop structure at locations in cereal fields used by yellowhammers collecting food for nestlings. When these were compared to random locations, they found that foraging locations had sparser, shorter vegetation and more invertebrates. Odderskaer et al. (1997) found that skylarks preferred tramlines and unsown plots within spring barley fields. They suggest that this was probably due to unhindered ground

23 locomotion, facilitating detection of prey items, rather than prey density. Absolute density of arthropod food items was higher in the crop than in the more sparsely vegetated areas.

Vegetation may physically impede the movement of foraging birds (Brodmann, Reyer & Baer 1997) and may result in food items becoming inaccessible or more difficult to detect in dense swards. It has also been suggested that dense vegetation growth in modern cereal crops might impede movement and/or detectability of food items (Odderskaer et al. 1997). Similarly, crypticity may affect food availability; if a food is not easily located in a habitat, despite being abundant, intake rate may be low and the food effectively unavailable (Nystrand & Granström 1997).

Ausden, Sutherland & James (2001) found that the accessibility of soil macroinvertebrates to foraging waders was likely to increase following flooding of lowland wet grasslands, yet flooding also tended to reduce macro-invertebrate biomass. This probably explains why many of the highest densities of breeding wading birds are found on sites with low densities of soil macro-invertebrates.

Diaz & Telleria (1994) investigated the distribution and abundance of seed-eating overwintering birds in relation to seed abundance in central Spanish croplands. They found no relationship between bird distribution and seed abundance in habitats, even when both were converted to a common energy currency (kJ 10ha-1 seed abundance in January and whole winter food requirement of the bird assemblage). Seed abundances in all the habitats they studied were found to be a magnitude greater than whole winter food requirements of the birds. They cite studies in which summer seed crops and winter seed-eating bird abundances were found to be related, and also apparently contradicting studies in which they were not. They suggest that this might be explained by considering resource-independent factors such as food accessibility and predation risk, both of which are mediated by vegetation structure. They suggest that food is less accessible and predation risk greater in uncultivated habitats (which have a greater winter herb biomass) compared to cropped habitats.

Vegetation may conceal a feeding bird from a predator (or vice versa) and may affect the efficiency of foraging through its effects on detectability and accessibility of food items. Some species use vegetation as ‘cover’ from predators (e.g. house sparrows Passer domesticus: Harkin et al, 2000), others prefer to forage in more open locations in order to detect predators better (e.g. dark-bellied brent geese Branta bernicla bernicla: McKay et al, 1996). Lima & Dill (1990) reviewed predation risk as a factor determining choice of foraging habitat by passerines.

Whittingham & Markland (2002) found that the most likely reason canaries preferred bare earth to short grass as a foraging substrate was that scanning for predators was easier when feeding on bare earth, so seed intake rate was higher. Butler & Whittingham are currently investigating foraging by farmland birds in artificial stubbles of different heights. Preliminary results suggest that feeding rates are lower in obstructed habitats, and that the birds trade-off feeding with vigilance (Whittingham, Pers. Comm.).

Summary: it has recently been appreciated that food accessibility is an important component of the availability of food for farmland birds, and may help explain instances where bird are found to forage in areas of low absolute food abundance. Similarly, risk of predation may differ between foraging habitats, and also be an important aspect of food availability. Both accessibility and predation risk are mediated by vegetation structure.

1.4.10 DISCUSSION – FOOD AVAILABILITY

The availability of food to foraging farmland birds can be considered in terms of the abundance of that food and its accessibility. Food abundance is shown to vary depending on crop type,

24 through the vegetative structure and complexity of the crop, and the effects of the crop management regime. Generally, grassland has the highest numbers of invertebrates, followed by oil seed rape, compared to winter wheat, potatoes and sugar beet. Spring-sown crops usually have higher numbers of invertebrates than autumn- or winter-sown crops, though some studies contradicted others. Cropped areas generally have a lower diversity and abundance of invertebrates than non-cropped areas, with a concomitant decrease in food availability. Position within a field also influences food availability; for example, invertebrates are generally more abundant at field edges compared to the centre of fields.

Within non-cropped habitats, stubbles are generally perceived an important winter food source for farmland birds. Seed abundance can be shown to decline over the winter and under-sown stubble is an important food resource for invertebrate-feeding birds in the spring. The switch from spring-sown to autumn-sown crops has reduced stubble area and food availability for many birds. Seed abundance may be similar to other crops, but it may also be more accessible for various reasons. Set-aside generally has increased food abundance and availability compared to arable crops and grassland. Management regimes and enhancement (eg. wild bird cover) of set-aside affect the availability of food on set-aside. The reduced pesticide applications on conservation headlands appear to positively affect food availability in most studies.

Modern farmland practices relating to the increasing intensification of farmland, generally have an adverse effect on invertebrates. Practices such as increased pesticide usage, loss of uncultivated field margins, increased tillage, and the decline in under-sown crops have all been shown to decrease food availability. Farming practices have also significantly reduced weed plant and seed (both crop and weed) availability. Frequent tillage, increased fertiliser usage, improved harvesting and storage of cereals, increased herbicide usage and the switch to autumn- sown crops all adversely affect broad-leaved weed populations. A few weed species may have increased as a response to some of these practices. Grassland can have high numbers of invertebrates compared to arable crops, and this habitat is an important food source for birds such as lapwings. Inorganic fertiliser use, cutting and grazing of grassland all affect invertebrate abundance, mostly adversely.

It is difficult to separate the effects of pesticides from other confounding factors. However, it is generally assumed that the increasing use of pesticides in recent decades has had a detrimental effect on food availability for farmland birds. Insecticide impact is mediated by a combination of chemical, toxicological, ecological and operational factors. Many studies have found that insecticides reduce invertebrate numbers, but this may be a short-term effect in some instances. Ewald & Aebischer (1999), however, did find long-term declines in many invertebrates over 30 years. Generally, increased herbicide usage is thought to reduce overall weed and seed abundance, but some weed species may be more tolerant to herbicide effects. Herbicide use is considered to reduce insect food availability, through the destruction of host plants. Differences in invertebrate species ecology, such as mobility and over-wintering strategy, mean that some species may be more abundant in herbicide-treated crops than untreated crops. Fungicides seem to have reduced affects on invertebrate food abundance compared to herbicides or pesticides.

Integrated farming systems, with reduced chemical and nitrogen inputs, showed increased non- target invertebrate populations compared to conventional farms. These increases could also be attributed to other factors such as greater weed species diversity and abundance, improved field management and a change to non-inversion tillage practices (Holland et al. 1994a). There is some evidence then the use of GM crops may lead to reduced abundances of weed seeds and invertebrates. Organic farms have greater food availability than conventional or integrated farms in general. This is due to the prevalence of mixed farming, crop rotation, spring sown crops, the avoidance of agrochemical usage, the maintenance of non-crop habitats such as hedges and field margins, use of green manure, and cereal crop under-sowing (Azeez 2000).

25 Climatic factors, such as rainfall, temperature and wind, can affect invertebrate food availability. Climatic variables also interact with other factors such as pesticide effects to influence arthropod populations. Invertebrates also show a wide range of within-year and between-year variation in population abundance. This temporal variation can confound studies into the effects of other factors such as crop and pesticide effects. Weather conditions, crop- stage and spatial variation contribute to temporal variations. In regard to seed availability, farming practices and seed predation can reduce availability over time.

Resource-independent factors such as food accessibility and predation risk can also affect food availability, both of which are mediated by vegetation structure. There is evidence that food is less accessible and predation risk greater in uncultivated habitats (which have a greater winter herb biomass) compared to cropped habitats, and differences in preference for different crop types, such as spring cereals over winter cereals by foraging skylarks, may be due to density of vegetation/food accessibility factors.

1.5 Foraging preferences

1.5.1 INTRODUCTION

This section reviews information on the foraging preferences or relative use of habitats by farmland birds, concentrating on the 21 species being considered in this project. Foraging preferences for food items in terms of their value, are covered by Objectives 3 (ranking of weed species in terms of their food value) and 5 (groupings for different taxa in terms of food value and availability). Data reviewed in this section are typically obtained by undertaking surveys of the habitats, or by radio-tracking. Data comprises the number or density of birds observed in a specific habitat at a specific time, or the proportion of time spent by radio-tagged individuals in a specific habitat, and sometimes the behaviour of the individuals.

The relative number of birds observed in a habitat is compared to a model in which birds randomly select a habitat in proportion to its availability. This is illustrated using selection indices (e.g. Jacob’s index: Jacobs 1974) and tested statistically using logistic regression (e.g. using Genstat: Payne et al. 2000 or SAS: SAS institute Inc. 2001) or compositional analysis (Aebischer, Robertson & Kenward 1993).

1.5.2 THE PREFERENCE OF BIRDS FOR FARMLAND HABITATS

1.5.2.1 All year studies

Pascual, Crocker & Hart (1998) investigated the availability of information on the proportion of time spent in key crops by selected species of birds in order to estimate exposure to pesticides. He found that most bird surveys were conducted in the breeding season and in winter cereals. There was much less information on birds’ use of all crops in the winter and on crops other than winter cereals in the summer. This information was used by the UK Pesticides Safety Directorate (PSD) to decide on further research needed. As a result of this review, Crocker et al. (2000) radio-tracked linnets, skylarks and yellowhammers on arable farmland, throughout the year. They found that mean time spent on crops was usually well below 50%. Crocker et al. (2001) investigated preferences of different bird species between different crops, and used this information to prioritise radio-tracking. They found that where birds showed a preference, they almost always avoided wheat and barley in all seasons. Oilseed rape, however, was found to be preferred by some species. This work is currently on-going.

Parish, Lakhani & Sparks (1994) studied birds in 131 200m field boundary lengths in Swavesey fen, Cambridgeshire. Species numbers were greater in grass boundaries than in arable boundaries and this was true both in winter and summer censuses and for nesting birds. The

26 diversity of birds was also greater on hedges between grassland. Breeding corn buntings and skylarks were the only species to show a significant preference for arable boundaries (Sparks, Parish & Hinsley 1996). Boutin, Freemark & Kirk (1999) examined the activity patterns of birds using four different crops in southern Canada throughout the year, to identify which species were vulnerable to pesticide use. Results were analysed with respect to foraging location (and hence risk of exposure to pesticides) rather than to crop preferences, but give an indication of the extent to which arable crops are used by birds. The crops were corn, soybean, apple orchards and vineyards. Of 138 species present, 25 were recorded during 50% of visits, and 13 were considered most at risk. Foraging was the most important activity for most species in all months. Most species were found to use field edges more than the interior, although the extent to which they used edges differed between crops and species of bird.

The use of cereal field margins by birds has been reviewed by Vickery et al. (1998). They reviewed data from three studies (one winter and two breeding season) and found that a number of species of birds use field margins: gamebirds (red-legged and grey partridge and pheasant), starling, blackbird, robin Erithacus rubecula dunnock Prunella modularis, house sparrow, chaffinch Fringuilla coelebs, greenfinch, goldfinch Carduelis carduelis, yellowhammer, skylark, meadow pipit Anthus pratensis, pied wagtail Motacilla alba yarellii and song thrush Turdus philomelos. Several of these species showed a clear preference for foraging at the edges of fields, and few avoided them. Conservation headlands and set-aside strips seemed to be used by higher numbers of birds of a wider range of species than grass strips. This may also reflect a seasonal difference as grass strips were studied in winter and the other margins in summer.

Henderson & Evans (2000) review studies investigating the use of set-aside fields by farmland birds in winter and summer. They report that in winter there is evidence that several declining species select set-aside stubble over crops and grassland and avoid winter cereals and ploughed fields. In summer, bird densities were significantly higher on set-aside than winter cereals for a wide range of species. The vegetation characteristics of set-aside influenced its usage by birds, with a heterogeneous composition (typically seen in younger set-aside) tending to be preferred.

1.5.2.2 Winter studies

Wilson et al. (1996a) investigated field use by 26 farmland bird species on mixed farmland in Oxfordshire in the winter. They found marked differences between species. In general, grazed grass fields were preferred by insectivorous birds and avoided by seed feeders, which favoured ungrazed fields. Stubbles (cereal and oilseed) were strongly preferred by seed-feeding birds. Winter cereal fields were almost universally avoided. Given the large areas of conventionally managed winter cereals, they were used significantly less often than expected by skylarks, crows, meadow pipits, woodpigeons Columba palumbus, magpies Pica pica, jackdaws Corvus monedula, rooks Corvus frugilegus, yellowhammers, blackbirds, linnets, song thrushes, pied wagtails, starlings, black-headed gulls Larus ridibundus, reed buntings, goldfinches, chaffinches, and greenfinches. Only fieldfares Turdus pilaris, red-legged partridge Alectoris rufa, greypartridge, kestrels Falco tinnunculus, mistle thrushes Turdus viscivorus, pheasants, snipe Gallinago gallinago and stock doves Columba oenas showed no significant avoidance of winter cereals. Song thrushes and pheasants preferred broad-leaved crops while skylarks, yellowhammers, linnets, rooks, magpies, jackdaws, crows, chaffinches and goldfinches avoided them.

Tucker (1992) investigated field use by invertebrate-feeding birds in winter. He found that permanent grass fields supported the highest bird densities. Cereal stubbles and grass leys supported moderate densities of some species but were generally avoided. Bare tilled fields, winter cereals and oilseed rape were little used.

Evans et al. (1997b) carried out winter surveys of birds on 20 arable farms in Devon and 20 in East Anglia. They report only on red-list species, and found that grey partridges, skylarks, song

27 thrushes, linnets, cirl buntings and yellowhammers all avoided winter cereals, and all except song thrush preferred set-aside and stubbles. Song thrushes and linnets were also significantly more likely to be found among brassicas.

Robinson and Sutherland (1997) surveyed seed-eating birds on two farms in North Norfolk and showed that seed densities can determine winter bird distribution and explain habitat preferences. Robinson and Sutherland (1999) confirmed that habitat preferences of seed-eaters were related to seed density, which differed markedly between habitats. Foraging location within habitats could also partly be explained by seed density.

Perkins et al. (2000) investigated the influence of variation in sward structure, grassland management and landscape variables on field use by 14 field-feeding bird species wintering on lowland mixed farmland in southern England. They found that variation in sward height and density were associated with frequency of occurrence for 12 bird species and larger areas of bare earth and occurrence of grazing by stock animals were correlated with frequency of occurrence for 11 bird species. Skylark and yellowhammer were more frequent on fields with seeding grasses.

1.5.2.3 Breeding season studies

Green, Osborne & Sears (1994) studied the distribution of passerines in hedgerows during the breeding season. They found that willow warblers Phylloscopus trochilus, blue tits Parus caeruleus and goldfinches preferred hedges adjacent to grass rather than tilled land, whereas greenfinches and yellowhammers preferred till. Of 18 species considered, only the blackbird showed a significant preference for particular crops (peas and beans preferred, cereals avoided) but there was consistency in the general trend for birds to select hedges that bordered crops in the following order from most to least preferred: oilseed rape, potatoes, autumn-sown cereals, peas, beans, sugar-beet, spring cereals. Fourteen of the 18 species preferred hedges by autumn cereals rather than by spring cereals and 14 species also preferred hedges by headlands which were conventionally sprayed rather than by conservation headlands.

Crocker et al. (1998a) surveyed 109 orchards from April to September 1996 to investigate the use made of this habitat, and bordering hedges, by farmland birds. They found that the ten most numerous species in the orchards were the blue tit, chaffinch, blackbird, woodpigeon, robin, great tit Parus major, jackdaw, tree sparrow Passer montanus, greenfinch and magpie (in decreasing order). The top ten for hedges omitted the jackdaw, magpie and tree sparrow and instead included the wren Troglodytes troglodytes, dunnock and chiffchaff Phylloscopus collybita. Crocker et al. (1998b) radio-tracked 130 birds (blackbirds, blue tits, chaffinches and robins) in 21 Herefordshire apple orchards to investigate the birds’ exposure to pesticides in the summer. They found that birds of all four species spent less than a quarter of their active time among orchard fruit trees.

Henderson et al. (2000a) measured the abundance and distribution of breeding birds on 11 intensive arable farms in eastern and western England, comparing crops to set-aside. They found that set-aside supported higher densities and more species of birds than fields of wheat, brassicas, root crops and seed rye. They suggest that most birds would have been foraging and that this distribution probably reflects greater food abundance on set-aside. The majority of birds utilised the outer margin of fields.

Henderson et al. (2000b) conducted an extensive survey of 92 arable farms in England in summer, and examined field type preferences across bird functional groups (representing non- passerines, passerines, insectivores and granivores). They found that bird abundances were higher on set-aside than on winter cereals for all six of their functional groups, and were highest

28 on rotational set-aside for all groups except crows. Winter cereals or grassland were generally the least preferred habitat.

1.5.3 SPECIFIC STUDIES ON THE SPECIES BEING CONSIDERED IN THIS PROJECT

Table 1.6 was compiled from intensive studies (farmland surveys or radio-tracking), in which the observed distribution of birds is compared to the observed availability of crops or farmland habitat. Extensive studies, such as those comparing the geographical distribution of a population with the overall distribution of habitats or crops (e.g. Kyrkos, Wilson & Fuller 1998), are not included. If intensive studies were lacking for the particular species, information reported in the review by Buxton et al. (1998) is given.

29 Table 1.6. Habitat and crop preferences of the farmland bird species considered in this review.

Species Preference Reference

Chaffinch In spring, avoid cropped areas and prefer trees (oak and willow), hedges and bushes for foraging. Whittingham et al. (2001) In winter, avoid grassland, winter cereals and broad-leaved crops and prefer stubble. Wilson et al. (1996a) Prefer cereals, stubble, oilseed rape and orchards. Reported in Buxton et al. (1998)

Cirl bunting Stubble fields with more weeds were selected in winter. Evans and Smith (1992) Stubble fields selected in winter. Grassy margins of fields preferred, near hedgerow. Evans & Smith (1994) In spring, provisioning adults preferred rough or semi-intensive grassland and avoided intensive Evans et al. (1997a) pasture. In winter, avoided winter cereals and preferred set-aside and stubble Evans et al. (1997b)

Collared dove Make little use of cereal stubbles, preferring to feed around grain stores. Reported in Buxton et al. (1998)

Corn bunting Summer corn bunting density was found to be greatest in areas of rotational grass and spring-sown Ward & Aebischer (1994) barley, which was related to the number of caterpillars. In the breeding season, areas of high corn bunting density also contained more set-aside, ungrazed Aebischer & Ward (1997) grass and winter wheat. In spring, provisioning corn buntings preferred grassy field margins, but also used spring-sown Brickle et al. (2000) barley, low-intensity grass and set-aside. Winter wheat and intensively managed grass were avoided. In breeding season prefer winter cereals and oats and avoid sugar beet and beans. Gillings & Watts (1997) Preferred spring-sown oilseed rape and barley for nesting. In winter prefer oilseed rape stubble. Watson & Rae (1997) Preferred winter habitat weedy stubbles. Donald & Evans (1994) Iberian corn buntings select grasslands and shrublands in spring and stubble fields in winter, Diaz & Telleria (1997) apparently responding to food availability. In an area with arable reversion grassland, densities of wintering corn buntings were highest on Wakeham-Dawson & Aebischer cereal stubbles, reflecting the availability of broad-leaved weed seeds. (1998) Preferred cereal stubbles in winter, avoiding other stubble, grass ley and set-aside. Robinson & Sutherland (1999)

30 Species Preference Reference

Goldfinch In a census of breeding birds in lowland woods among arable land, goldfinches were more common Hinsley et al. (1995) where buildings were nearby. In spring, prefer hedges next to grass rather than tilled land. Green et al. (1994) In winter, avoid grassland, bare till, winter cereals and broad-leaved crops and prefer stubble. Wilson et al. (1996a) Prefer stubbles and orchards. Reported in Buxton et al. (1998)

Greenfinch In spring, prefer hedges next to tilled land rather than grass. Green et al. (1994) In winter, avoid ungrazed grass, conventionally-grown winter cereals and prefer stubble. Reported in Buxton et al. (1998) Prefer cereals, stubble and oilseed rape.

Grey partridge Radio-tracked broods preferred winter wheat and avoided sugar beet, and preferred to feed at field Green (1984) edges. Preferred cereal stubble and avoided growing cereals, set-aside and grass leys in winter. Robinson & Sutherland (1999) In winter, avoid grazed grass and prefer stubble. Wilson et al. (1996a)

House sparrow Prefer cereals and stubble. Reported in Buxton et al. (1998)

Linnet Radio-tagged birds spent most time in non-cropped habitats (hedges, set-aside and stubble) in Crocker et al. (2001) summer. Of crops, more time was spent foraging in oilseed rape and root crops than cereals or grass. Birds in the breeding season avoided cereal and potato fields preferring fallow fields, meadows and Eybert, Constant & Lefeuvre (1995) rape. Robinson & Sutherland (1999) Preferred cereal stubbles in winter, avoiding other stubble, grass ley and set-aside. Mason & Macdonald (2000) Preferred winter oilseed rape, salad crops and set-aside in spring, and avoided winter cereals, spring- sown oilseed rape, sugar beet and grass. Evans et al. (1997b) In winter, avoided winter cereals and preferred set-aside, stubble and brassicas. Wilson et al. (1996a) In winter, avoid grassland, winter cereals and broad-leaved crops and prefer stubble.

Quail In a French study, in spring, quail were found to prefer winter wheat, spring and fallow lands in one Aubrais, Hemon & Guyomarc’h area and to prefer grassland to crops in another. Predation risk may affect habitat choice. (1986) In a 15 yr study in a mountainous area of Germany, quail were found to prefer spring crops and crop George (1996) mixtures and avoid beet crops and pasture.

Red-legged Radio-tracked broods preferred sugar beet and carrots and avoided winter and spring barley, and Green (1984) partridge preferred to feed at field edges. In Portugal, preferred wheat fields and olive groves in spring. Borralho, Stoate & Araujo (2000) No preference shown for any crop type. Robinson & Sutherland (1999) Do not avoid winter cereals in winter, avoid grazed grass and prefer organically-grown cereals. Wilson et al. (1996a)

Reed bunting Selected oilseed rape for nesting. Wheat and grass were also used but linseed and peas were avoided. Burton et al. (1999) In winter, avoid grazed grass and winter cereals and prefer stubble. Wilson et al. (1996a) Prefer cereals, barley, stubble, and oilseed rape. Reported in Buxton et al. (1998)

Rook Cereal stubbles and ploughed fields important feeding habitats. Aerts & Spaans (1987) In winter, avoid stubble, bare till, winter cereals and broad-leaved crops and prefer grazed grass. Wilson et al. (1996a)

Skylark Preferred set-aside and legumes in spring, and fields with short hedges and trees. Chamberlain et al. (1999b). In spring, set-aside and organically-cropped fields had higher densities than intensively managed Wilson et al. (1997) fields or grazed pasture. Tended to avoid tall crops. Set-aside held high territory densities, permanent pasture low densities. Spring cereals held higher Donald et al. (2001b) densities than winter cereals, possibly due to differences in crop structure. In spring, preferred set-aside and conservation grassland and avoided other grassland. Mason & Macdonald (2000) Preferred cereal stubble and avoided growing cereals and grass leys in winter. Robinson & Sutherland (1999) Cereal stubble most strongly preferred winter habitat, but breeding territory density higher in set- Donald & Vickery (2000) aside, spring-sown cereals and some non-cropped habitats. Wintering skylarks in Oxfordshire preferred cereal stubble fields (barley>wheat), growing cereal was Donald et al. (2001a) weakly selected and sugar beet stubbles had high bird densities. Rotational set-aside was occupied more frequently than non-rotational. Larger fields and those not enclosed by hedges were preferred. Relationships with seed availability were found. Winter censuses on 125 mixed farmland fields indicated preference for stubbles and avoidance of Wilson et al. (1996a) grazed grass, broad-leaved crops and winter cereals. In an area with arable reversion grassland, densities of wintering skylarks were highest on cereal Wakeham-Dawson & Aebischer stubbles and chalk downland arable reversion, reflecting the availability of broad-leaved weed seeds. (1998) On grass, 10 cm high swards preferred. Radio-tagged birds spent most time in non-cropped habitats (set-aside and stubble) in summer. Of Crocker et al. (2001) crops, more time was spent foraging in oilseed rape and cereal than grass or root crops. In spring prefer non-rotational set-aside to sugarbeet, potatoes, winter cereals and carrots. Avoided Chaney et al. (1997) tall cereals and naturally regenerated set-aside. In winter strongly preferred stubble followed by set- aside. Birds showed a strong preference for winter stubbles and avoided cover strips managed for game- Brickle (1997) birds. In winter, avoided winter cereals and broadleaved crops and preferred set-aside and stubble. Evans et al. (1997b)

Stock dove In winter, did not avoid winter cereals, avoided ungrazed grass and preferred bare till. Wilson et al. (1996a) In a census of breeding birds in lowland woods among arable land, stock doves were more common Hinsley et al. (1995) where buildings were nearby.

Stone curlew Short grass and short Calluna heath preferred for nesting. Autumn-sown crops, tall unimproved grass Green & Griffiths (1994) and heather and improved grass were avoided. Density higher on sparse than dense spring-sown crops. Stone curlew most likely to breed on spring-sown arable fields if the crop became tall late in the Green et al. (2000) summer and if it was situated close to grassland and was distant from a road.

Tree sparrow Preferred cereal stubbles in winter, avoiding other stubble, grass ley and set-aside. Robinson & Sutherland (1999) In a census of breeding birds in lowland woods among arable land, tree sparrows showed an aversion Hinsley et al. (1995) to wooded landscapes. Prefer cereals. Reported in Buxton et al. (1998)

Turtle dove Preferred residential areas, scrub and woodland in spring. Hedgerows and orchards were avoided. Of Mason & Macdonald (2000) crops, grass was strongly preferred and winter cereals and salad crops avoided. Preferred spilt grain around buildings and roads early in the breeding season, and harvested crops Browne & Aebischer (2001) (except peas) late in the season. Prefer cereals and stubble. Reported in Buxton et al. (1998)

Woodpigeon Newly drilled cereal fields and root waste preferred in autumn. Growing cereals, ploughed fields, McKay et al. (1999) stubble and root crops were avoided. In spring, newly drilled cereal fields sometimes preferred to growing cereal, ploughed fields, stubble and onions. Preference for newly sown cereal fields in autumn, oilseed rape for most of the winter, and pasture Inglis et al. (1990) and spring-sown cereals from March. In winter, avoid conventionally-grown winter cereals and prefer grazed grass and bare till. Wilson et al. (1996a)

Yellowhammer Weak preference for peas, grass and set-aside in spring. Mason & Macdonald (2000) Broad-leaved crops and sparsely vegetated areas preferred early spring and ripening cereals later. Stoate, Moreby & Szczur (1998) Radio-tagged birds spent most time in hedges in summer. Of crops, more time was spent foraging in Crocker et al. (2001) cereals, root crops and oilseed rape (in that order) than grass, set-aside or stubble. In winter, most time was spent in hedges and on stubble. In spring, prefer hedges next to tilled land rather than grass. Green et al. (1994) Territories associated with hedgerows, vegetated ditches and wide uncultivated grassy margins Bradbury et al. (2000) around fields. Pasture and silage leys are avoided Preferred cereal stubbles in winter, avoiding other stubble, grass ley and set-aside. Robinson & Sutherland (1999) In winter, avoided winter cereals and preferred set-aside and stubble. Evans et al. (1997b) In winter, avoid grazed grass, conventionally-grown winter cereals and broadleaved crops and prefer Wilson et al. (1996a) stubble.

Yellow wagtail Preference for spring-sown crops for nesting, especially potatoes. Autumn-sown crops and grassland Mason & Macdonald (2000) were avoided. Prefer meadow and pasture. Reported in Buxton et al. (1998)

35 1.5.4 FORAGING PREFERENCES AND PESTICIDE LEVELS Studies in which the distribution or behaviour of farmland birds are shown to be related to pesticide applications were reviewed. In field studies, such as those comparing organic to conventional farms (e.g. Chamberlain et al, 1999c), pesticide application is often correlated with a variety of other factors. In large-scale field experiments, such as those involving conservation headlands (e.g. Sotherton 1992), the effects of pesticide application can be tested and treatments replicated and compared to a control. In aviary studies, pesticide effects can also be tested in isolation, but captive birds may not be good models for wild birds. For example, they are generally fed ad libitum, are not subject to time constraints when foraging, and do not feed in flocks.

Field-scale studies of birds foraging in sprayed and unsprayed plots provide the most convincing examples of the response of foraging birds, under field conditions, to pesticide applications. Using radio-tracking methods, Rands (1986) showed that grey partridge broods feeding in cereal fields with headlands that were left unsprayed with pesticides had a higher proportion of the headland within their home range compared to broods in fields with sprayed headlands. Related studies showed that broods of grey partridge and pheasant were larger, insect food was more abundant and grey partridge brood survival was greater in fields with conservation headlands (Rands 1985; 1986). Another study by de Snoo, Dobbelstein & Koelewijn (1994) examined the use of the margins of winter wheat fields during the breeding season by blue-headed wagtails (Motacilla flava flava). The frequency of visits by foraging wagtails to unsprayed margins was 3-4.5 times greater than that to margins treated with either herbicide or insecticide.

A second group of field studies have compared birds’ use of different fields receiving different pesticide inputs. Morris, Bradbury & Wilson (2002a) showed that adult yellowhammers provisioning their young used arable fields with summer applications of insecticide less than those receiving no summer application. The preference for fields receiving no summer insecticides disappeared later in the breeding season, when cereal grain was exploited rather than insects. In addition, the body condition of yellowhammer chicks was negatively related to insecticide use in fields adjacent to the nest and chick mortality tended to be greater in nests situated next to sprayed fields. This suggests that adults from nests surrounded by sprayed fields were not able to compensate for the negative effects of the insecticides on the food supply, although the alternative possibility of direct toxic effects of pesticides on the chicks or sublethal effects on the provisioning behaviour of adults was not ruled out.

The remaining field-scale studies have compared bird densities in conventionally managed arable crops with those managed under organic systems, which receive no pesticide inputs (Wilson et al. 1996a, 1997; Chamberlain et al. 1999c; Chamberlain & Wilson, 2000). Densities of particular species were often higher on organic cereal crops than on those managed conventionally. However, most of these studies were not able to isolate pesticide effects from other changes to crop husbandry and farm structure resulting from organic conversion. Chamberlain & Wilson (2000) found that 19 species of birds were more abundant on organic farms than on conventionally managed farms in at least one season of the year. However, for eight species, hedgerow management rather than differences in pesticide inputs appeared to explain most of the differences in bird densities between organic and conventional farms.

The studies by Rands (1985; 1986), de Snoo Dobbelstein & Koelewijn (1994) and Morris et al. (2002a) imply that individuals of at least some farmland bird species prefer to forage in unsprayed fields, or portions of fields, because food is more abundant there. However, other behavioural responses may sometimes be involved. For example, McKay et al. (1999) found that fewer fields drilled with cereal seed treated with insecticide (fonophos) were used by foraging

36 woodpigeons than untreated fields for the first week after drilling. This short-lived avoidance of fields receiving fonophos was attributed to the repellency of the treated seed.

Summary: There is evidence that a few well-studied farmland bird species, e.g. grey partridge and yellowhammer, prefer to forage in fields, or parts of fields, that receive reduced inputs of insecticide. Survival of grey partridge and yellowhammer broods was related to access to crops or field margins with reduced or no insecticide inputs during summer.

1.5.4 DISCUSSION – FORAGING PREFERENCES

The published information on the relative use of farmland habitats (foraging preferences) is reviewed. Such data typically consist of comparisons between the numbers of birds or time spent by individuals in a habitat, and the relative availability of that habitat. These studies involve either intensive field surveys or radio-tracking.

In general, farmland bird species are found to vary in their preferences for different crops or habitats. Preferences are generally determined by diet, and differ between winter and the breeding season. Radio-tracking studies tend to show that individual farmland birds spend much less than 50% of their time foraging in arable habitats as opposed to woodland, hedges and other semi-natural habitats.

Insectivorous species tend to prefer permanent grassland, in particular grazed grass, and seed- eaters prefer stubble and sometimes set-aside. Winter cereal fields are almost universally avoided. Broadleaved crops and bare tilled soil are preferred by some species and avoided by others. Some studies show a preference of some species for oilseed rape over other crops, at particular times of the year. Within arable fields, most species tend to use the margins more than the centre. Information relating to the species being considered in this project is summarised.

Studies on the influence of pesticide applications on farmland bird distribution and behaviour are reviewed. In general, there are limited data supporting a relationship, and if anything, the effect appears to be small. However, short-term effects of pesticides on bird foraging preferences may be difficult to detect in the field.

1.6 Functional response

1.6.1 INTRODUCTION

The functional response describes the consumption rate of prey by a predator in relation to prey density. When applied to farmland birds, it involves the birds’ response (change in consumption rate) as the density of food changes. It describes constraints on the consumption rate as well as forming a basis for understanding the spatial and temporal dispersion of the consumer across a gradient of prey densities. The functional response is therefore important when attempting to understand the effects of changes in food availability (for example due to pesticide use) on the intake rate of farmland birds, and ultimately on population sizes. The functional response is central to the depletion model being considered in this project (Objectives 2, 7, 8 and 9).

1.6.2 TYPES OF FUNCTIONAL RESPONSE

The detailed nature of the response varies and has been classified into three types, by Holling (1959). Begon, Harper & Townsend (1986) summarised the responses as follows: Type I - the consumption rate shows a linear rise with food density and then a plateau after a certain food density is surpassed. The plateau forms at a maximum ingestion rate, below which handling times are zero, for example herbivores (Batzli, Jung & Guntenspergen 1981). Type II - the consumption rate rises with food density but gradually decelerates to a plateau. This response

37 occurs when finding food becomes easier as food density increases but food handling times remain constant e.g. seed-eating birds (Robinson 2000) and waders (Norris & Johnstone 1998). Type III - here the response is similar to Type II but at low food densities consumption rate accelerates initially before showing a typical Type II deceleration at higher food densities. This response can occur when the preference for a food or prey type changes with a change in its density, e.g. the rate of parasitism (Hassell, Lawton & Beddington 1977).

1.6.3 FACTORS AFFECTING THE FUNCTIONAL RESPONSE 1.6.3.1 Food availability Food availability can have important consequences for the nature of the functional response. For example, in an agricultural setting, the rate at which seeds are consumed by seed-eating birds depends on the seed density (Robinson & Sutherland 1999) but also on whether the seeds occur on the surface or are buried (Robinson 2001). Seed-eating birds foraging on surface and buried cereal grain are presented with a choice of alternatives differing in their profitability.

Robinson (2001) showed that the functional responses of skylarks and yellowhammers foraging within arable fields differed according to seed availability. In an experiment that compared the intake rates of grain supplied on the surface with grain buried just below the soil surface Robinson showed that both species had a ‘Type II’ response. However, for each species, the point at which the intake rate became constant was lower for the buried grain. In both species the handling time was significantly increased for buried grain. Robinson (2000) also showed that the importance of seed availability may differ between species. When the intake rates were compared between food patches with the same seed densities but different availabilities (due to some seeds being buried below the surface) Robinson showed that availability may be important for yellowhammers but less so for skylarks. Yellowhammers tended to restrict their foraging to surface grains. Surface foraging was characterised by lower handling times and higher search efficiencies. Differences between the distributions of skylark and yellowhammer on farmland over winter could well be explained by each species different functional response to food availability.

The historic decline in the amount of weed seeds and unharvested cereal grain caused by agricultural changes is well known (Shrubb, 1997). Robinson (2000) speculates that at current seed densities intake rates will be well below the maximum possible. Robinson calculated that the asymptotic intake rates of skylark and yellowhammer have been possibly reduced by 35% and 65%, respectively since the mid-seventies. This reduction is likely to have affected overwinter survival. Curiously, although larger flocks resulted in higher intake rates due to reduced vigilance, Robinson (2000) observed that when seed densities were low skylarks (when another bird was present) showed reduced intake rates but yellowhammers did not. Robinson provided no explanation but speculated that perhaps there was a difference in the degree of vigilance behaviour between the two species. Behavioural differences may affect species and individuals’ vulnerability to changes in food supply.

1.6.3.2 Relative profitability

Holmes, Norris & Froud-Williams (unpub.) investigated the functional response of chaffinches to weed seed density in multiple-prey trials. They found that chaffinches selected the most profitable seeds more than expected from their density. Consumption rate was also found to be affected by handling time – which limited the amount of the preferred seed that chaffinches could consume. The functional response may also have been affected by the birds’ inability to judge the relative profitability of the different species of seeds.

38 1.6.3.3 Substrate Substrate variation may also influence the functional response and the intake rate of seeds from the surface by granivorous birds. Whittingham & Markland (2002) showed that food accessibility affected intake rates. Seed intake rates of captive canaries were always higher on bare earth than from on vegetated substrate regardless of the crypticity of the seed. Getty and Pullman (1993) also reported that sparrows Zoonotrichia albicollis search where ‘prey’ was detectable rather than where it was most abundant.

1.6.3.4 Interference Skylarks are possibly more vulnerable to interference than yellowhammers. Yellowhammers willingly exploit edge habitats and spilt grain, sometimes in preference to natural food sources (Ziswiler 1965). Although skylarks, unlike yellowhammers, are able to exploit shallow buried seed and green-leaf (Green 1978), skylarks still much prefer surface seed. Green (1978) reported that green leaf was a less profitable food source than cereal grain and Robinson (2000) found that seed density on the field surface was the best correlate of skylark density. The number of foraging tactics a species is capable of and the efficiency with which individuals conduct them are probably important in defining their vulnerability and survival (Partridge & Green 1985; Sutherland & Dolman 1994).

1.6.3.5 Search efficiency Search efficiencies have been studied for various avian species. These studies have been reviewed in Robinson (2000) and categorised into studies where 1) food was equally available, 2) food was likely to be equally available and 3) food was not equally available.

When different ‘prey’ types are available the profitability of each is dependent on its density (Stephens & Krebs 1986). At high food densities birds may restrict their searching to the most available prey e.g. knot Calidris canutus preying on different sized bivalves Macoma balthica (Zwarts & Blomert, 1992). Wanink & Zwarts (1985) observed that at high prey densities oystercatchers Haematopus ostralegus maintained higher than predicted intake rates as they were able to reduce handling times by ignoring closed bivalves. Robinson (2000) reported that cereal grain size within arable fields varied between 20mg and 70mg in his study, the effects of this size variation on ‘prey’ choice by foraging birds is not known. Some studies suggest that there can be significant costs imposed on birds that attempted to maximise their intake rates by always selecting the largest prey e.g. Norris and Johnstone (1998) and Draulans (1982).

Robinson (2000) was able to explain why yellowhammers restricted their foraging to surface grains when he compared the search efficiencies of yellowhammer with skylark. Krebs & McCleery (1984) stated that to maximise their rate of energy gain individuals should forage on the less profitable alternative only when the more profitable food is scarce. In Robinsons’ study search efficiences for skylark were similar for surface and buried grain, but yellowhammer search efficiency declined for the deeper grains. The threshold seed density at which skylark should specialise on surface grains only was much higher than for yellowhammer.

1.6.3.6 Individual variation The functional response is also affected by individual variation in foraging ability. For example adults and immature birds may differ in their foraging ability (Marchetti & Price 1989). Individuals differ in their search efficiences (Espin, Mather & Adam 1983; Sutherland, Jones & Hadfield., 1986) and handling times (Greig-Smith & Crocker 1985). Ritchie (1988), using small mammals, calculated the optimal diet (based on maximising energy gain, subject to digestive constraints) of individuals based on their weight and found that for most individuals, diet did not differ from the optimal predicted. However, 28% of the sampled individuals diets did deviate from the optimum. Ritchie (1990) noted that individuals that deviated from the optimal diet tended to show poorer breeding performance. In seed-eating birds preference for different

39 seed types differs between individuals, time of day, period of year and moisture of the seed (Pinowski, Tomek & Tomek 1973).

1.6.3.7 Risk sensitivity Risk sensitivity i.e., how a forager assesses the probability of finding food/prey given that the distribution and density of its food will be variable, is another factor that affects the functional response.

Caraco, Martindale & Whitham. (1980), using yellow-eyed juncos Junco phaenotus, illustrated that the functional response may be affected by a birds energy budget. Birds with positive energy budgets, i.e. birds that have access to sufficient food to meet their daily requirements, were risk averse. In contrast birds with negative energy budgets, i.e. birds that have access to insufficient food to meet their daily requirements, were risk prone. When a foraging bird was offered a choice between a certain source of food or an uncertain alternative that may provide more or less food than the certain source (but on average no difference) then the risk averse bird always took the certain food and the risk prone bird the uncertain alternative. Stephens & Krebs 1986 summarised Caraco et al.’s. work stating that if a bird’s expected daily energy budget was positive then it should be risk averse, but if the expected daily energy budget was negative then it should be risk prone. Caraco was able to repeat his findings using two other species of granivorous birds (Caraco 1981, 1983). Risk sensitivity may well explain Ziswilers’ (1965) observation that yellowhammers preferred spilt grain from human sources than weed seeds foraged from within fields.

A model derived by Stephens & Krebs (1986) proposed that the switch in risk sensitivity (from risk-averse to risk-prone) occurs because it minimises the probability of an energetic shortfall. Stephens & Krebs (1986) also describe other models that show how temporal patterns of energy gain maybe important. A delayed reward may be perceived as being less valuable than an immediate gain, even if the delayed reward is actually more valuable (Kagel, Green & Caraco 1986).

1.6.4 DISCUSSION – FUNCTIONAL RESPONSE

The effect of changes in food availability on the consumption rate by farmland birds is described by the functional response. This differs between species and food types. It is also affected by the range of foods available and the densities of those foods. It is clear that the net result of a decrease in the availability of a species’ normal food will depend on the alternatives available; their relative profitability, density, handling time, predictability and crypticity as well as the individual’s foraging ability and competitive ability.

1.7 Avian energetics

1.7.1 INTRODUCTION

The availability of food to farmland birds is affected by the abundance of that food in habitats in which birds forage, together with factors such as accessibility of the food and predation risk in that habitat. The amount of food eaten is affected by the availability of that food and the bird’s preference for it. Both availability and preference have already been reviewed. In order to assess the likely effect of changes in food availability caused by modern farming practices (such as the use of pesticides) on the population size of that species, as well as a knowledge of the functional response (also reviewed previously), it would be useful to be able to compare the amount of food available to the amount of food eaten or ideally, the amount of food required to breed successfully or survive the winter.

40 Information on food intake is difficult to obtain as it is rarely possible to follow a wild bird closely enough to monitor what foods it eats and in what quantities. There is, however, increasing information on the Daily Energy Expenditure (DEE) of free-ranging birds. When combined with the information on the energetic values of farmland bird foods and the efficiency with which they are assimilated, it is possible to estimate the likely daily food intake (DFI).

Estimates of this type published by Nagy (1987) are widely used in ecological risk assessment. He found a strong relationship between body weight and DEE, with significant differences between taxonomic groups and species occupying different habitats. Nagy’s equations can therefore be used to predict DFI for most species.

DFI of wildlife species is important information when estimating exposure to pesticides and hence in assessing the risk of pesticides for pesticide regulation purposes. It is for this reason the Pesticides Safety Directorate of DEFRA (PSD) commissioned a study on methods for estimating daily food intake of wild birds and mammals (Crocker et al., 2002). This section summarises the information in that report relevant to farmland birds. The food value of weed seeds to farmland birds is also being considered under Objective 3 of this project.

1.7.2 METHODS Since Nagy’s original publication, energy requirement studies have been published for a number of additional species and Nagy himself has updated and revised his original estimates (Nagy, Girard & Brown 1999). In addition, since the 1980s, the method using Doubly-Labelled Water (DLW) has been available. This involves catching an animal, injecting it with isotopically- labelled water, catching it again at a later date and taking a blood sample to determine the relative turn-over of the hydrogen and oxygen isotopes. From this, a figure for CO2 production can be calculated and in turn an estimate made of daily energy requirements. The advantage of this method is that it reveals the energy expenditure of an animal living in its natural habitat engaging in its normal activities and feeding on its normal foods.

Crocker et al. (2002) reviewed the more recent literature on metabolic rate of free-living birds and found estimates of field metabolic rates, from studies using DLW isotopes, for 96 bird species. They used this information to generate a new set of allometric equations linking body weight with DEE. They also collated information on the energy and moisture contents of various wildlife foods. More than 2000 measurements of potential wildlife foods were grouped into 15 broad categories. Finally, they collated data on the efficiency with which wildlife assimilated food. They then used these data to estimate DFI for a range of species/food scenarios, some of which are of relevance to farmland birds.

1.7.3 RESULTS

1.7.3.1 Daily energy expenditure

There is a strong relationship between body weight and DEE. As previously reported (Nagy, 1987; Nagy et al., 1999), there are significant differences between taxonomic groups and between species occupying different habitats.

The following is the equation linking body weight to DEE for passerines:

Log10(DEE) = 1.0017 + 0.7034(Log10(body weight))

This was generated using data for 38 species, and excludes marine and desert passerines. For birds other than passerines, desert birds, hummingbirds and sea birds, the equation is:

Log10(DEE) = 0.6768 + 0.7723(Log10(body weight))

41 This was generated using data for 11 species.

Further analysis of the data suggested that the relationship between body weight and DEE scaled differently within a species than between species. The same point has been argued by Tinbergen & Dietz (1994) who found that among breeding great tits, the slope linking small individuals with heavy individuals is close to 2, much steeper than the value of 0.7 Crocker et al. (2002) found linking light species with heavy species. To illustrate this, the authors make the following point: it is energetically very costly to be an overweight great tit at least during the breeding season. During this time great tits feeding young spend much time in hovering flight taking small caterpillars. This may be a proportionately more strenuous activity for heavier birds. Therefore, the equations derived in Crocker et al. (2002) use mean bodyweight for a species and do not attempt to model the effects of individual variation in bodyweight.

Within species, the breeding status of the individual had an important influence on DEE. As might be expected, birds feeding young used more energy than incubating birds. Data of this sort were, however, insufficient to derive separate equations.

1.7.3.2 Moisture and energy contents of foods

Information on food quality was found to be widely dispersed through the literature, and was far from comprehensive. The particular foods used in these studies did not precisely match those in the diets of wildlife species. Therefore, it was necessary to combine the food items into broad categories. Means for major groupings of food types relevant to farmland birds are presented in Table 1.7

Table 1.7. Energy and moisture contents for general categories of food type.

Food type Energy content Moisture content (Kj/g dry weight) (%) Dicotyledenous crop leaves 11.2 88.6 Grasses and cereal shoots 18.0 76.4 Non-grass herbs 18.0 82.1 Orchard top fruit 11.6 83.7 Cereal seeds 16.7 13.3 Weed seeds 21.0 11.9 Arthropods 21.9 70.5 Caterpillars 21.7 79.4 Soil invertebrates 19.3 84.6

1.7.3.2 Assimilation efficiency

The literature on avian digestive efficiency has been reviewed by Castro, Stoyan & Myers (1989), Karasov (1990) and most recently by Bairlein (1999). The latter author has collated data on more than 1000 examples of avian assimilation efficiencies reported in the literature and summarised them into 22 taxonomic groupings and six food types. Crocker et al. (2002) relied mainly on Bairlein’s summary for birds in their study. Two of the categories used by Crocker et al. (2002) to calculate mean assimilation efficiencies are relevant to farmland birds: pigeons and passerines. The data on pigeons were of four species, from 36 studies and the data on passerines were of 67 species, from 441 studies (Table 1.8).

42 Table 1.8. Assimilation efficiencies relevant to farmland birds, from Barlein (1999).

Order % assimilation efficiencies of food type Animal Fruits Herbage Seeds Sugars Artificial Columbiformes 76 Passerriformes 76 67 76 80 90 72

1.7.3.3 Estimation of average daily food intake

Crocker et al. (2002) estimated DFI for 82 scenarios of typical UK birds and mammals consuming typical foods that could potentially be contaminated with pesticides. In each case, they used the most relevant subset of the available information. DEE has not been measured directly for most of the species of concern in pesticide risk assessment, or for most farmland birds. In these cases, they used the general equations to estimate DEE, estimating the mean DEE for a species from its mean bodyweight. It should be remembered that there is additional variation between species within the habitat groups, and there are also differences due to breeding status and variation over time, but these sources of variation are not sufficiently well characterised by existing data to be included in general equations

As an example, Crocker et al. (2002) give the weight of insects a chaffinch would need to eat in a day in order to maintain it’s energy budget. A chaffinch is a small passerine, therefore, using the equation given earlier, it might expect to expend 85.2 kJ per day. Arthropods contain an average of 21.9 kJ/g dry weight and consist of 70.5% water (Table 1.7). Therefore arthropods contain 6.5 kJ/g fresh weight. A bird using 85.2 kJ a day will need 85.2/6.5 = 13.2g of arthropods, assuming it can digest its food completely efficiently. However, studies suggest that on average, passerines only manage to make use of 76% of the energy in animal foods (Table 1.8. Therefore, on average a chaffinch balancing its daily energy budget and feeding wholly on arthropods will need to eat 17.3g fresh weight a day. The results of similar calculations for other scenarios relevant to the species being considered within this project are presented in Table 1.9.

43 Table 1.9. Predicted fresh food intake for selected combinations of farmland bird species and food types.

Mean Energy Water Digestion food Body DEE content content E content efficiency intake Species wt (g) (kJ/day) Food (kJ/g dw) (%) (% fw) (%) (g) Chaffinch 20.9 85 arthropods 21.9 70.5 6.4605 76 17.3 20.9 85 weed seeds 21.0 11.9 18.501 80 5.8 Cirl bunting 22.8 91 cereal seeds 16.7 13.3 14.4789 80 7.8 22.8 91 arthropods 21.9 70.5 6.4605 76 18.4 Collared Dove 149 339 cereal seeds 16.7 13.3 14.4789 80 29.3 Corn Bunting 49 155 arthropods 21.9 70.5 6.4605 76 31.6 49 155 weed seeds 21.0 11.9 18.501 80 10.5 49 155 cereal seeds 16.7 13.3 14.4789 80 13.4 Goldfinch 15.6 69 weed seeds 21.0 11.9 18.501 80 4.7 Greenfinch 27.8 104 weed seeds 21.0 11.9 18.501 80 7.0 27.8 104 cereal seeds 16.7 13.3 14.4789 80 9.0 Grey partridge 390 667 cereal seeds 16.7 13.3 14.4789 80 57.6 390 667 arthropods 21.9 70.5 6.4605 76 135.9 House Sparrow 27.7 103 arthropods 21.9 70.5 6.4605 76 21.1 27.7 103 weed seeds 21.0 11.9 18.501 80 7.0 27.7 104 cereal seeds 16.7 13.3 14.4789 80 9.0 Linnet 15.3 68 weed seeds 21.0 11.9 18.501 80 4.6 15.3 68 rape seeds 21.6 15.5 17.407 80 4.9 Quail 100 256 arthropods 21.9 70.5 6.4605 76 52.2 Red-legged Partridge 436 722 arthropods 21.9 70.5 6.4605 76 147.0 436 722 weed seeds 21.0 11.9 18.501 80 48.8 436 722 cereal seeds 16.7 13.3 14.4789 80 62.3 Reed bunting 18.3 78 arthropods 21.9 70.5 6.4605 76 15.8 18.3 78 weed seeds 21.0 11.9 18.501 80 5.2 Rook 488 781 arthropods 21.9 70.5 6.4605 76 159.1 488 781 cereal seeds 16.7 13.3 14.4789 80 67.4 Skylark 40 134 arthropods 21.9 70.5 6.4605 76 27.4 40 134 rape leaves 11.2 88.6 1.2768 76 138.6 Stock Dove 291 543 cereal seeds 16.7 13.3 14.4789 80 46.9 Stone Curlew 450 738 arthropods 21.9 70.5 6.4605 76 150.3 Tree Sparrow 22 88 arthropods 21.9 70.5 6.4605 76 18.0 22 88 weed seeds 21.0 11.9 18.501 80 6.0 Turtle Dove 132 311 weed seeds 21.0 11.9 18.501 80 21.0 132 311 cereal seeds 16.7 13.3 14.4789 80 26.9 Woodpigeon 490 783 cereal seeds 16.7 13.3 14.4789 80 67.6 Yellowhammer 26.5 101 arthropods 21.9 70.5 6.4605 76 20.5 26.5 101 weed seeds 21.0 11.9 18.501 80 6.8 Yellow wagtail 17.6 75 arthropods 21.9 70.5 6.4605 76 15.4

44 1.7.5 LIMITATIONS OF METHOD

1.7.5.1 Appropriateness of data on food quality

1. We have imperfect information about the composition of wildlife diets 2. Data reflect information on foods that are available in the literature rather than foods present in diets. Values included may lean toward those that were reasonably easy to collect rather than those that best reflect what a particular animal actually eats. 3. The food items collected and measured by an experimenter may not match those selected by wildlife. 4. Food is not only a source of energy. It contains many other constituents, such as protein, minerals and vitamins, which animals may be selecting for rather than balancing their energy budget.

1.7.5.2 Appropriateness of data on Daily Energy Expenditure

1. Crocker et al. (2002) show that variance in DEE is high. Although the equations linking bodyweight with DEE often explain 90% or more of the variance, the correlation is based on log bodyweight against log DEE. Small variations along a log scale translate to large differences on the untransformed data. 2. DEE may be overestimated. The majority of DLW studies on birds have taken place when birds are nesting and it is easier to catch them repeatedly. 3. Animals may choose to expend less energy rather than seek more food (energy expenditure is not fixed). 4. Animals may choose not to balance their energy budgets in the short term, instead they may choose to make use of fat reserves. For example winter passerines appear to trade bodyweight for reduced predation risk even though the risk of starvation is thereby increased (Brodin 2001).

1.7.5.3 Plausibility of food intake predictions

Crocker et al. (2002) note that the predicted daily food intakes sometimes seem unreasonably large. For example, the model implies that a skylark weighing 37g will eat 225g of beet leaves a day – more than six times its own bodyweight. This seems unlikely. In practice, however, skylarks foraging on winter cereal fields have been shown to take a mixed diet (Donald et al., 2001a) comprising 54% cereal leaves (16kJ/g, 85% moisture, 45% assimilation) and 24% weed leaves (18kJ/g, 82% moisture, 45% assimilation) 13% cereal grain (17.3kJ/g, 13.7% moisture, 80% assimilation), 5% weed seeds (20.9kJ/g, 11.9% moisture, 80% assimilation) and 3% arthropods (21.9kJ/g, 70.5% moisture, 76% assimilation). Using Donald et al.’s data on dietary proportions and their own data on nutrient values and assimilation efficiencies, Crocker et al. (2002) show that a daily energy budget of 128kJ for a 37g skylark could be satisfied by eating 20.4g cereal leaves, 9.1g broadleaf weeds, 4.9g grain, 1.9g of weed seeds, and 1.1g arthropods: in all a daily food intake of 37.5g.

1.7.6 DISCUSSION – AVIAN ENERGETICS

The method used by Crocker et al. (2002) allows prediction of a species’ likely daily food intake of a given diet from its bodyweight. They show that their results are broadly in line with empirical data. The use of empirically derived equations allows the estimation of confidence limits on the predictions and it opens up the possibility of predicting not only the most likely food intake but also the unlikely or worst case scenarios, which are important in pesticide risk analysis.

45 Using Monte Carlo simulations, Crocker et al. (2002) also calculate that the 95% quantile for food intake is about twice the average intake. This suggests that a safety factor of two might be appropriate in estimating a species’ ‘worst case’ food intake from data based on a mean intake.

In conclusion, methods exist to predict the amount of food needed to balance the energy requirements of farmland birds from a knowledge of the species’ body weight and diet. This could theoretically be compared to the amount of food available in farmland habitats. However, these methods are based on several assumptions, and are subject to limitations, which reduce their usefulness in the modelling process. For example, there is incomplete knowledge of the variation in energy expenditure within a species, depending on sex, season and behaviour, among other factors. Also, birds may choose not to balance their energy budgets in the short term. A considerable amount of further work is therefore needed if avian energetics is to be useful in modelling farmland bird foods, reproductive performance and survival.

1.8 Discussion

The published literature on the resource requirements and behaviour of farmland birds in conventional and alternative arable crop systems is reviewed, concentrating on 21 selected species.

The availability of food to foraging farmland birds can be considered in terms of the abundance of that food and its accessibility. A good knowledge of the relationship between food abundance and species’ breeding performance is needed for the deterministic model. Food abundance is shown to vary depending on crop type and crop management regime. Cropped areas generally have a lower diversity and abundance of invertebrates than non-cropped areas. Position within a field also influences food availability; invertebrates generally are more abundant at field edges compared to the centre.

Within non-cropped habitats, stubbles are an important winter food source for farmland birds. Under-sowing reduces seed density in stubbles. However undersown fields comprise an important food resource for invertebrate-feeding birds in the spring. The switch from spring- sown to autumn-sown crops has reduced stubble area and food availability for many birds. Set- aside generally has increased food abundance and availability compared to arable crops and grassland. Management regimes and enhancement (eg. wild bird cover) of set-aside affect the availability of food on set-aside. The reduced pesticide applications on conservation headlands appear to positively affect food availability in most studies.

Modern practices relating to the increased intensification of farmland, generally have an adverse effect on food availability. Frequent tillage, increased fertiliser usage, improved harvesting and storage of cereals, increased herbicide usage and the switch to autumn-sown crops all adversely affect broad-leaved weed populations. A few weed species may have increased as a response to some of these practices.

It is difficult to separate the effects of pesticides from other factors. However, it is generally assumed that the increasing use of pesticides in recent decades has had a detrimental effect on food availability for farmland birds. Many studies have found that insecticides reduce numbers of non-target arthropods, but this may be a short-term effect because of recolonisation from unsprayed areas nearby. Ewald & Aebischer (1999), however, did find long-term declines in many invertebrates over 30 years. Generally, increased herbicide usage is thought to reduce overall weed and seed abundance, and to reduce insect food availability, through the destruction of host plants. Fungicides seem to have reduced affects on invertebrate food abundance compared to herbicides or pesticides.

46 Integrated farming systems, with reduced chemical and nitrogen inputs, showed increased invertebrate populations compared to conventional farms, although these increases could also be attributed to other factors (Holland et al. 1994a). There is some evidence that the use of GM crops may lead to reduced abundances of weed seeds and invertebrates. Organic farms, in general, have greater food availability than conventional or integrated farms. This is probably due to a combination of factors including the prevalence of mixed farming, crop rotation, spring sown crops, the avoidance of agrochemical usage, the maintenance of non-crop habitats such as hedges and field margins, use of green manure, and cereal crop under-sowing (Azeez 2000).

Weather factors, such as rainfall, temperature and wind, can affect invertebrate food availability. Weather variables also interact with other factors such as pesticide effects to influence arthropod populations. Arthropods show a wide range of within-year and between- year variation in population abundance.

Resource-independent factors such as food accessibility and predation risk can also affect food availability, both of which are mediated by vegetation structure. There is evidence that food is less accessible and predation risk greater in uncultivated habitats (which have a greater winter herb biomass) compared to cropped habitats, and differences in preference for different crop types, such as spring cereals over winter cereals by foraging skylarks, may be due to density of vegetation/food accessibility factors.

The published information on the relative use of farmland habitats (foraging preferences) is reviewed. Such data typically consist of comparisons between the numbers (or densities) of birds or time spent by individuals in a habitat, and the relative availability of that habitat. These studies involve either intensive field surveys or radio-tracking. A knowledge of a species’ foraging preferences may give an indication of the relative availability of food between habitats, and so could theoretically be useful for the deterministic model. A knowledge of foraging preferences in terms of the behavioural response to differences or changes in food availability, is also potentially useful for the resource limitation model. For either model, foraging preferences give an indication of where to sample food.

In general, farmland bird species are found to vary in their preferences for different crops or habitats. Preferences are generally determined by diet, and differ between winter and the breeding season. Radio-tracking studies tend to show that individual farmland birds spend much less than 50% of their time foraging in arable habitats compared to woodland, hedges and other semi-natural habitats. Insectivorous species tend to prefer permanent grassland, in particular grazed grass, and seed-eaters prefer stubble and sometimes set-aside. Winter cereal fields are almost universally avoided. Broadleaved crops and bare tilled soil are preferred by some species and avoided by others. Some studies show a preference of some species for oilseed rape over other crops, at particular times of the year. Within arable fields, most species tend to use the margins more than the centre. Estimates of food availability should take account of this behaviour. Information relating to the species being considered in this project is summarised.

Studies on the influence of pesticide applications on farmland bird distribution and behaviour are reviewed. There are few relevant studies, but field experiments with conservation headlands indicate that grey partridge broods preferentially forage in conservation headland areas, where broadleaved weeds and arthropod prey were more abundant. Blue-headed wagtails also foraged preferentially in unsprayed field margin strips. Foraging density of yellowhammers provisioning young was lower in crops which had received at least one insecticide application in summer than in those which had not.

The effect of changes in food availability on the consumption rate by farmland birds is described by the functional response. This differs between species and between food types and will also depend upon the range of foods available and the densities of those foods. It is clear that the net result of a decrease in the availability of a species’ normal food will depend on the

47 alternatives available; their relative profitability, density, handling time, predictability and crypticity as well as the individual’s foraging ability and competitive ability. A good knowledge of functional responses of farmland birds is needed for the development of the resource limitation model.

A species’ daily food intake can be predicted from a knowledge of its diet, bodyweight and digestive efficiency. Crocker et al. (2002) show that the results using this method are broadly in line with empirical data obtained using the doubly-labelled water method. Theoretically, therefore, avian energetics could be used in the modelling process, to relate changes in food availability in the farmland habitat to the food needed to meet a species’ energy requirements. The use of empirically derived equations also allows the estimation of confidence limits on the predictions and it opens up the possibility of predicting not only the most likely food intake but also the unlikely or worst case scenarios. These methods, however, are based on several assumptions, and are subject to limitations. A considerable amount of further work is needed if avian energetics is to be useful in modelling farmland bird foods, reproductive performance and survival.

1.9 References

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