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The populations of many farmland birds, including the yellowhammer Emberiza citrinella L., have undergone major declines in Britain (Newton 2004). Several hypotheses have been proposed to explain the declines. None the less, decreases in the abundance of weeds (Firbank & Smart 2002), seeds (Robinson & Sutherland 2002) and arthropods (Ewald & Aebischer 1999) on farmland in lowland Britain are thought to be significant drivers of recent change, acting through a combination of survival rates (Siriwardena, Baillie & Wilson 1998; Siriwardena & Robinson 2002) and reproductive output (Siriwardena et al. 2000). The extent to which pesticides have contributed to the population declines by reducing the food supplies of birds to levels that impact on survival or breeding productivity is unclear. There are three possible routes by which this may occur: insecticides reducing arthropod food supplies (type 1); herbicides eliminating plants that are hosts for arthropods taken by farmland birds (type 2); herbicides reducing the abundance of weeds, which provide either green matter or seeds for herbivorous and seed-eating species, respectively (type 3).
In principle, these processes do not involve direct poisoning of birds and have been termed indirect effects of pesticides (Newton 1995; Burn 2000). Indirect effects may be additive. For example, seed-eating passerines, which rely upon arthropod food supplies in summer to provision their young, could be vulnerable to all three types.
As yet, few examples of indirect effects of pesticides have been demonstrated experimentally in the field, mainly because of the laborious data requirements. In Britain, only the long-term study of the grey partridge Perdix perdix L. has amassed enough data to establish links between pesticide applications, arthropod food supplies, chick survival and population change. Type 1 and type 2 effects have been demonstrated (Rands 1985; Potts 1986). Type 3 effects are suspected to have contributed to the declines of seed-eating birds (Newton 1995) but none has yet been demonstrated empirically, partly because of analytical difficulties (Boatman et al. 2004). Nevertheless, indirect effects of pesticides have been identified as possible agents of the decline of 18 farmland bird species in Britain (Campbell et al. 1997; Boatman et al. 2004).
In this study we focused on type 1 effects by considering the impact of summer applications of insecticides on the arthropod food and reproductive output of the yellowhammer. The yellowhammer was chosen because it is a declining species that is potentially vulnerable to type 1 effects (Morris et al. 2005) and because it is still sufficiently abundant to provide adequate sample sizes for nest-based studies (Bradbury et al. 2000). The diet of yellowhammer nestlings is dominated by arthropods (although unripe grain may also be consumed late in the breeding season; Morris et al. 2005) and the adults forage in crops where their food supplies may be affected by insecticides (Stoate, Moreby & Szczur 1998; Morris, Bradbury & Wilson 2002).
In a meta-analysis of yellowhammer studies from eight farms in central and eastern England, Morris et al. (2005) presented evidence for some but not all indicators of a type 1 indirect effect. Arthropod food of yellowhammers was less abundant in cereal fields that had been sprayed with insecticides in summer than in those that had only been sprayed in winter or not at all. When foraging, adults tended to avoid fields that had received insecticide applications in summer, unless cereal grain was available. A quadratic relationship between chick condition and the number of insecticide applications in adjacent fields was also demonstrated. Chick condition was poorest in nests adjacent to fields that had received three applications, the third application usually being made in summer.
Morris et al. (2005) could not show a relationship between insecticide applications and chick starvation. However, in a replicated farm-scale experiment, in which summer insecticide inputs were deliberately increased in a proportion of fields to vary the extent of spraying around individual yellowhammer nests, Boatman et al. (2004) were able to demonstrate an effect. Where insecticides had been applied within 20 days of the hatch date, the probability of brood reduction was positively correlated with the proportion of the 200-m foraging range around each nest that had been sprayed. The most likely explanation for the observed brood reduction was chick starvation as a result of food shortages induced by the insecticides. Lethal or sublethal poisoning of chicks or provisioning adults was very unlikely because the insecticides used in the experiment were mostly pyrethroids (Cypermethrin, Deltamethrin and Lambda Cyhalothrin), which have low toxicity to birds (Anonymous 1989, 1990a,b), and because pyrethroids, unlike organophosphorus and carbamate products (Grue, Hart & Mineau 1991), are not known to impair the breeding and foraging behaviour of birds by inhibiting cholinesterase activity in the brain.
The relationship between the extent and timing of insecticide applications and the probability of brood reduction (Boatman et al. 2004) implied the existence of relationships between insecticide application, arthropod abundance, chick development and fledging success. This study aimed to quantify the relationships between food abundance in the foraging range of individual yellowhammer nests and chick development, and between chick development and the probability of brood reduction as a result of chick starvation. A further aim was to demonstrate that insecticide applications depressed arthropod abundance to levels where impairment of chick development, and chick loss, was likely.
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The Pesticide Safety Directorate of Defra funded the work under Project PN0925.
We are very grateful to the landowners for generously granting permission to work on their estate, and to the farm staff for their co-operation. We are also grateful to the British Atmospheric Data Centre for providing us with meteorological data and thank Deborah Beaumont, Jo Marshall, Carl Wardill, Tim Drew, George Watola, Dave Parrott and Richard Walls for assisting in the collection and collation of field data. Additional thanks are due to Carola Deppe and Alain Zuur for statistical help, Nigel Boatman, Joe Crocker, Mark Clook and John Holland for useful discussion, and to Dan Chamberlain for comments on an earlier draft.