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Many migratory bird species are undergoing population declines as a result of potentially multiple, interacting mechanisms. Understanding the environmental associations of spatial variation in population change can help tease out the likely mechanisms involved. Common Cuckoo Cuculus canorus populations have declined by 69% in England but increased by 33% in Scotland. The declines have mainly occurred in lowland agricultural landscapes, but their mechanisms are unknown. At both the local scale within the county of Devon (SE England) and at the national (UK) scale, we analysed the breeding season distribution of Cuckoos in relation to habitat variation, the abundance of host species and the abundance of moth species whose caterpillars are a key food of adult Cuckoos. At the local scale, we found that Cuckoos were more likely to be detected in areas with more semi-natural habitat, more Meadow Pipits Anthus pratensis (but fewer Dunnocks Prunella modularis) and where, later in the summer, higher numbers of moths were captured whose larvae are Cuckoo prey. Nationally, Cuckoos have become more associated with upland heath characterized by the presence of Meadow Pipit hosts, and with wetland habitats occupied by Eurasian Reed Warbler Acrocephalus scirpaceus hosts. The core distribution of Cuckoos has shifted from south to north within the UK. By the end of 2009, the abundance of macro-moth species identified as prey had also declined four times faster than that of species not known to be taken by Cuckoos. The abundance of these moths has shown the sharpest declines in grassland, arable and woodland habitats and has increased in semi-natural habitats (heaths and rough grassland). Our study suggests that Cuckoos are likely to remain a very scarce bird in lowland agricultural landscapes without large-scale changes in agricultural practices.