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Conservation and Foraging Ecology of Bumble Bees In Conservation and Foraging Ecology of Bumble Bees in Urban Environments Roselle E. Chapman A thesis submitted for the degree of Doctor of Philosophy, University of London. Institute of Zoology, Zoological Society of London, Regent’s Park, London & University College London. April 2004 1 UMI Number: U602843 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. Dissertation Publishing UMI U602843 Published by ProQuest LLC 2014. Copyright in the Dissertation held by the Author. Microform Edition © ProQuest LLC. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 ABSTRACT The decline of British bumble bees has been attributed to the loss of their habitat through the intensification of agricultural practices. In the quest for information of use to bumble bee conservation the potential of our flower-rich cities has been overlooked. The overall aim of this study was to determine the status and foraging requirements of bumble bees in the urban environment provided by the city of London, U.K. My principal findings are as follows. Six common species and three rare species were identified. The greatest diversity of Bombus species was found in the east of London. Garden and wasteland habitats attracted the greatest abundance of workers and diversity of Bombus species. The distribution of Bombus humilis (a Biodiversity Action Plan Species) was found to follow the strip of derelict Thames-side industrial land on the eastern side of London as far west as the Millennium Dome, and the River Lea as far north as the Walthamstow Marshes. The phenology of B. humilis in London was established. The majority of all observations of foraging B. humilis were on flowers in the Lamiaceae family but species native to the U.K. were not necessarily its favoured forage. In a field experiment, the removal of potential competitors significantly increased the time that B. humilis workers spent foraging at patches of flowers. Microsatellite analysis was successfully employed to test three hypotheses concerning the movement patterns of foraging Bombus workers at three spatial scales. NeitherB. terrestris nor B. pascuorum workers were found to forage with their nest-mates on patches of flowers. Mean numbers of 96 and 66 colonies of B. terrestris and B. pascuorum respectively were identified foraging on sites with a mean area of 0.8 hectares. No inbreeding and little or no genetic differentiation could be detected in either species across London. 2 CONTENTS Title Page 1 Abstract 2 Contents 3 List of Tables 5 List of Figures 8 Acknowledgements 10 Chapter 1 12 Introduction Chapter 2 19 Species distribution and foraging ecology of bumble bees in a large urban area (London U.K.) Chapter 3 69 The distribution and foraging ecology of a rare bumble bee, Bombus humilis, in a large urban area (London U.K.) Chapter 4 110 A test for interspecific competition between a threatened {Bombus humilis) and non­ threatened bumble bee species Chapter 5 135 Genetic analysis of spatial foraging patterns and resource sharing in bumble bee pollinators Chapter 6 175 Discussion References 186 3 Appendix A 199 Environmental variables Appendix B 201 The list of flower species recorded during forage availability survey Appendix C 206 Genotypes used in analyses for B. terrestris and B. pascuorum nests. Appendix D 207 B. terrestris genotypes used in analyses. Appendix E 219 B. pascuorum genotypes used in analyses. Appendix F 229 Chapman, R.E., J. Wang and Bourke, A.F.G. 2003. Genetic analysis of spatial foraging patterns and resource sharing in bumble bee pollinators. Molecular Ecology 12: 2801- 2808. 4 LIST OF TABLES Chapter 2 Table 1 Thirty study sites visited showing their locations, 53 their habitat types and the dates they were surveyed. Table 2 A summary of rare Bombus species recorded on 54 Hampstead Heath between 1832 and 1947. Table 3 Summary of bumble bees, by caste and species 55 identified foraging in each round. Table 4a Plant species diversity at each transect, shown in 56 descending order according to their floral diversity in each round. Table 4b Plants species diversity at each transect, shown in 58 descending order according to their floral diversity in all rounds combined. Table 5 The top ten most visited flowers by workers of each 59 bumble bee species over all of the rounds combined. Table 6 The four flower species most preferred and least 60 preferred by workers of each bumble bee species. Chapter 3 Table 1 The dates on which each transect was surveyed. 93 Table 2 Site names and locations where B. humilis, B. 94 sylvarum and B. ruderarius were found in the years 2000 - 2002 . Table 3 Summary of the number of bumble bees, by species 95 and caste, identified foraging in each week of the study between 21st May and 19th August 2001. Table 4 A complete list of B. humilis forage accumulated over 96 the 2000,2001 and 2002 field seasons. Chapter 4 Table la. GLM results table for B. humilis foraging duration in 127 the presence and absence of competitors, 2001. 5 Table lb GLM results table for B. humilis foraging duration in 127 the presence and absence of competitors, 2002. Table lc GLM results table for B. humilis foraging duration 128 with and without competitors, 2002 and 2001 combined. Table Id GLM results table for ‘other species* in the presence 128 and absence of B. humilis, 2002. Table 2a The number of bumble bees observed and removed 129 from each patch, 2001. Table 2b The number of bumble bees observed and removed 129 from each patch, 2002. Chapter 5 Table 1 Samples of B. terrestris and B. pascuorum workers 163 collected from 11 sites across London for genetic analysis. Table 2 Microsatellite loci tested for amplification in B. 164 terrestris and B. pascuorum. Table 3 A summary of microsatellite variation in B. terrestris 165 and B. pascuorum, showing the mean number of alleles per locus, the number of alleles, observed heterozygosity and number of workers genotyped per study site. Table 4 A summary of Weir and Cockerham’s inbreeding 166 coefficient (Fis) for B. terrestris and B. pascuorum at all sites, tested for significant difference from zero. Table 5a B. terrestris within-patch relatedness. 167 Table 5b B. pascuorum within-patch relatedness. 168 Table 6 Estimated number of colonies per Bombus sampling 169 site. 6 Table 7a Multilocus pairwise Fst values between pairs of 170 sample sites for B. terrestris. Table 7b Multilocus pairwise Fst values between pairs of 171 sample sites for B. pascuorum. Table 8 Time in minutes taken to collect 10 workers at each 172 patch at each site. 7 LIST OF FIGURES Chapter 2 Figure 1 A map of London to show the location of the study sites, 61 their habitat and their geographical area. Figure 2 The phenology of each Bombus species and caste. 62 Figure 3 Percentage of Bombus species observations by region of 63 London over all rounds combined. Figure 4 Percentage of Bombus species observations by habitat over 64 all rounds combined. Figure 5 Floral abundance by habitat. 65 Figure 6 Observations of worker bumble bees by habitat shown as a 66 percentage of all observations. Figure 7 The proportion of native and non-native flower coverage 67 recorded at each habitat. Figure 8 Floral species diversity by habitat. 68 Chapter 3 Figure 1 Bombus humilis distribution map showing 19th Century 98 records, records for 1900 - 1969 and records for 1970 to present. Figure 2a A map of the Temple Mills site to show the location of the 99 transects. Figure 2b A map of the Thames Barrier Park site to show the 99 location of transects. Figure 3 A map of Bombus humilis distribution in London and the 100 Thames Corridor showing records collated by the Bees Wasps and Ants Recording Society (BWARS) and Roselle Chapman (RC). Figure 4 A map of Bombus sylvarum and B. ruderarius distribution 101 in London and the Thames Corridor showing records collated by the Bees Wasps and Ants Recording Society (BWARS) and Roselle Chapman (RC). 8 The phenology of each Bombus species and caste in order 102 of the peak in worker numbers for the two Thames Barrier Park transects combined. Total B. humilis observations by caste at the four study 105 transects. The phenology of flowering plant abundance. 106 B. humilis worker forage observations by plant family. 108 B. humilis queen forage observations by plant family. 109 A diagram to illustrate the treatments applied to each patch 130 of forage. The proportion of species recorded during the study 131 Results of the 2001 experiment. 132 Results of the 2002 experiment (comparison of treatments 132 A and B) Results of the 2002 experiment (comparison of treatments 133 A and C) Mean visit duration of B. humilis against the number of 134 competitors removed, 2001. Mean visit duration of B. humilis against the number of 134 competitors removed, 2002. A map to show the distribution of the genetic sampling 173 sites. Estimated median foraging distances as a function of nest 174 density for workers visiting a site attracting 20-100 colonies. 9 ACKNOWLEDGEMENTS This Ph.D. could not have been completed without the wisdom, patience, and organisational skills of my supervisor Andrew Bourke. I am indebted to him for his tremendous generosity with his time and unflappable nature.
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