Testing Agricultural Impacts on Breeding Ground Food Resources As a Driver of Cuckoo Population Decline

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Testing Agricultural Impacts on Breeding Ground Food Resources As a Driver of Cuckoo Population Decline Testing agricultural impacts on breeding ground food resources as a driver of cuckoo population decline Submitted by Lowell John Mills to the University of Exeter as a thesis for the degree of Doctor of Philosophy in Biological Sciences, March 2019 This thesis is available for Library use on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. I certify that all material in this thesis which is not my own work has been identified and that no material has previously been submitted and approved for the award of a degree by this or any other university. 1 2 Image: Charles Tyler “The first picture of you, The first picture of summer, Seeing the flowers scream their joy.” - The Lotus Eaters (1983) 3 4 Abstract The common cuckoo Cuculus canorus has undergone a striking divergence in population trend between UK habitats since the 1980s. The breeding population in Scotland – in largely semi-natural open habitat – shows significant increase whereas there has been a significant decline in England. Here breeding numbers have remained stable or increased in semi-natural habitats, while woodland and farmland populations have plummeted. As a brood parasitic bird with a long-distance annual migration, the cuckoo has a unique network of relationships to songbird „hosts‟, prey and habitat; and a disconnection between adult and nestling ecology due to lack of parental care. This thesis investigated the role of breeding ground land-use factors in driving cuckoo population decline. In the first chapter information was synthesised from the literature on potential threats and environmental impacts facing cuckoo populations, which also highlighted knowledge gaps and a basis for hypotheses in later chapters. In chapters 3 and 4 I investigated land-use and habitat influences on the nestling ecology of the cuckoo and a key host the meadow pipit Anthus pratensis at field sites in Dartmoor, Devon, UK. I assessed provisioning behaviour at unparasitised nests of meadow pipit, and used this baseline to test how host provisioning differed between host broods and cuckoo nestlings and fledglings, as indicators of how resource requirements differ between cuckoo and host in a relative stronghold habitat. There was evidence that host foraging habitat selection and investment in provisioning per unit time were similar between raising a cuckoo nestling and a host brood; but the nestling and fledgling periods were longer in cuckoos and the rate of provisioning was higher for cuckoo fledglings. Pipits also provided cuckoos with different diversity and frequency of prey taxa, further indicating that cuckoo nesting success requires different resources to that of unparasitised nests. In chapters 5 and 6 I focused on the diet of adult and juvenile cuckoos. In the first application of DNA sequencing to the study of cuckoo diet, adults in a relative stronghold habitat consumed large moth caterpillars (Lepidoptera) but frequently consumed Orthoptera and some Diptera families not previously reported as important prey. Analysis of moth capture data in Devon suggested some key prey species have declined even in semi-natural upland areas. I conclude with analysis of key findings including how they direct future research and conservation. 5 Contents List of tables and figures………………………………………………………………8 1. The ecology of common cuckoos Cuculus canorus increases populations’ vulnerability to environmental change ……………………..…11 2. General materials and methods……………………………………………….68 Field methods……………………………………………………………………...…68 Study area and study sites…………………………………………………….……68 Nest finding, monitoring and brood handling procedures………………..………70 Parental provisioning observation…………………………………………….……72 Habitat recording……………………………………………………………………..77 Adult cuckoo faecal sampling……………………………………………………….77 Laboratory methods………………………………………………………………….80 Collection of reference avian faeces……………………………………………….81 Collection of reference invertebrate tissue………………………………………...81 Primer selection for DNA amplification………………………………………….…81 Protocol for preparing pipit nestling faeces for Sanger sequencing…………….84 Sanger sequence handling and species identification…………………………...87 Protocol for preparing bird faeces for Illumina MISEQ sequencing…………….89 Illumina MISEQ sequence handling and species identification…………………91 3. Vegetation correlates of nestling condition and provisioning of meadow pipits Anthus pratensis, a cuckoo host in semi-natural grassland…….....94 Introduction……………………………………………………………………………95 Methods……………………………………………………………………………...100 Results……………………………………………………………………………….116 Discussion…………………………………………………………………………...124 References…………………………………………………………………………..130 6 4. Provisioning of nestlings and parasitic common cuckoo Cuculus canorus nestlings in grassland by meadow pipits Anthus pratensis.…………………………………………………………………………...137 Introduction……………………………………………………………………….…138 Methods…………………………………………………………………………...…145 Results……………………………………………………………………………….156 Discussion………………………………………………………………………......179 References ………………………………………………………………………….189 5. Assessing breeding ground diet of the common cuckoo Cuculus canorus using two novel methods……………………………….…………….198 Introduction………………………………………………………………….………199 Methods……………………………………………………………………...………203 Results………………………………………………………………………….……209 Discussion…………………………………………………………………...………216 References ………………………………………………………………………….222 6. Temporal and land-use trends in key cuckoo prey moth species in Devon from historic moth trapping data…………………………………..….230 Introduction………………………………………………………………………….231 Methods……………………………………………………………………………...234 Results……………………………………………………………………………….243 Discussion…………………………………………………………………………...262 References ………………………………………………………………………….268 7. General discussion and conclusions………………………………………271 Appendices………………………………………………………………………….293 7 List of tables and figures Chapter 1 Table 1 (p 37) Feeding habitats used by tracked cuckoos from various breeding populations. Table 2 (p 38) Area sizes of individuals in common cuckoo breeding populations. Fig. 1 (p 13) Trends in adult cuckoo abundance 1995-2017 in England, Wales and Scotland, drawn from BTO BBS data (Harris et al. 2018). Fig. 2 (p 42) Trends in adult abundance of cuckoo and 3 farmland host species 1995-2011 drawn from BTO Birdtrends 2017 (Massimino et al. 2017). Chapter 2 Table 1 (p 76) Names, descriptions and shorthand codes of habitat variables surveyed around nests and on 10 x 10 m patches used for foraging by meadow pipits Fig. 1 (p 69) Map showing study area and location of Dartmoor National Park in UK Fig. 2 (p 75) Orientation of habitat survey plots 1-12 around meadow pipit nests Fig. 3 (p 82) Electrophoresis gel images showing amplification of avian COI DNA from faeces of cuckoo and four sympatric species by candidate PCR primer pairs Fig. 4 (p 85) Alignment of COI mitochondrial DNA sequence showing complements of invertebrate primers and their location. Chapter 3 Table 1 (p 103) Names, descriptions and codes of habitat variables surveyed around nests and on 10 x 10 m patches used for foraging by meadow pipits. Table 2 (p 118) Modelled increases and decreases caused by habitat cover variables, in log number of visits made by foraging meadow pipits to a given 50 m square within 100 m of the nest Table 3 (p 120) Results of Wilcoxon Signed Rank tests, comparing cover of habitat variables in 10 x 10 m foraging locations to cover in their enclosing 50 x 50 m square; at two study areas on Dartmoor. 8 Table 4 (p 123) Structures of final general linear model variables for provisioning visit rate and prey load size at meadow pipit nests not parasitized by cuckoo. Fig. 1 (p 101) Map showing study areas in Dartmoor National Park, UK. Fig. 2 (p 104) Orientation of habitat survey plots around meadow pipit nests. Fig. 3 (p 109-115) Photographic illustrations of habitat types surveyed. Fig. 4 (p 117) Histogram of foraging distances of meadow pipits during provisioning of unparasitised nests. Fig. 5 (p 122) Scatterplots of nest failure probability with provisioning rates. Chapter 4 Table 1 (p 160) Results of Wilcoxon Signed Rank tests, comparing cover of habitat variables in 10 x 10 m foraging locations to cover in their enclosing 50 x 50 m square; for parasitised and unparasitised pairs. Table 2 (p 164) Structures of final general linear model variables for provisioning visit rate, prey load size and foraging distance at meadow pipit nests not parasitized by cuckoo at Holne Moor study area. Table 3 (p 165-166) Structures of initial and final general linear model variables for provisioning visit rate, prey load size and foraging distance at both cuckoo parasitized and unparasitised meadow pipit nests. Table 4 (p 169-170) Structures of initial and final general linear model variables for provisioning visit rate, prey load size and foraging distance for cuckoo nestlings/fledglings and meadow pipit nestlings, Table 5 (p 173-177) Invertebrate prey taxa brought to cuckoo young and meadow pipit nestlings based on MISEQ and Sanger sequencing. Fig. 1 (p 157-158) Scatterplots showing occurrence of cuckoo parasitism relative to mean cover of bracken, tufted semi-natural grassland grasses, open water and Juncus rushes, within 100 m of nests, and modelled variation in probability of parasitism. Fig. 2 (p 161-162) Boxplots of provisioning visit rate, prey load size and foraging distance by meadow pipits to their own broods and to nestling cuckoos, plotted by feather growth stage. Fig. 3 (p 167-168)
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