, Volume 50, Issue 4, pp 497–514 | Cite as

A review of methods for the study of bumble bee movement

  • John M. MolaEmail author
  • Neal M. Williams
Review article


Understanding animal movement is critical for conservation planning, habitat management, and ecological study. However, our understanding is often limited by methodological constraints. These limitations can be especially problematic in the study of ecologically and economically important pollinators like bumble bees, where several aspects of their biology limit the feasibility of landscape-scale studies. We review the methods available for the study of bumble bee movement ecology, discussing common limitations and tradeoffs among several frequent data sources. We provide recommendations on appropriate use for different life stages and castes, emphasizing where recent methodological advances can help reveal key components of understudied parts of the bumble bee life cycle such as queen movement and dispersal. We emphasize that there is no one correct method and encourage researchers planning studies to carefully consider the data requirements to best address questions of interest.


foraging dispersal mark-recapture radio-tracking sibship assignment 



We thank H. Woodard, C. Stuligross, E. E. Crone, and N. Pope for helpful comments on an earlier draft of this manuscript. JMM was supported by NSF Graduate Research Fellowship Award 1049702. NMW and JMM were supported by NSF DEB 1354022.

Author contribution

JMM and NMW conceived and developed this review; JMM wrote the initial draft, and NMW participated in the revisions. Both authors read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13592_2019_662_MOESM1_ESM.docx (24 kb)
ESM 1. (DOCX 24 kb)


  1. Aizen, M. A., C. Smith-Ramírez, C. L. Morales, L. Vieli, A. Sáez, R. M. Barahona-Segovia, M. P. Arbetman, J. Montalva, L. A. Garibaldi, D. W. Inouye, and L. D. Harder. 2019. Coordinated species importation policies are needed to reduce serious invasions globally: The case of alien bumblebees in South America. J. Appl. Ecol. 56:100–106CrossRefGoogle Scholar
  2. Allen, A. M., and N. J. Singh. 2016. Linking Movement Ecology with Wildlife Management and Conservation. Front. Ecol. Evol. 3 Google Scholar
  3. Andrews, K. R., J. M. Good, M. R. Miller, G. Luikart, and P. A. Hohenlohe. 2016. Harnessing the power of RADseq for ecological and evolutionary genomics. Nat. Rev. Genet. 17:81–92CrossRefPubMedPubMedCentralGoogle Scholar
  4. Arbetman, M. P., I. Meeus, C. L. Morales, M. A. Aizen, and G. Smagghe. 2013. Alien parasite hitchhikes to Patagonia on invasive bumblebee. Biol. Invasions 15:489–494CrossRefGoogle Scholar
  5. Bell, K. L., J. Fowler, K. S. Burgess, E. K. Dobbs, D. Gruenewald, B. Lawley, C. Morozumi, and B. J. Brosi. 2017. Applying Pollen DNA Metabarcoding to the Study of Plant–Pollinator Interactions. Appl. Plant Sci. 5:1600124CrossRefGoogle Scholar
  6. Bell, K. L., N. de Vere, A. Keller, R. T. Richardson, A. Gous, K. S. Burgess, and B. J. Brosi. 2016. Pollen DNA barcoding: current applications and future prospects. Genome 59:629–640CrossRefPubMedGoogle Scholar
  7. Bhattacharya, M., R. B. Primack, and J. Gerwein. 2003. Are roads and railroads barriers to bumblebee movement in a temperate suburban conservation area? Biol. Conserv. 109:37–45.CrossRefGoogle Scholar
  8. Bowers, M. A. 1985. Bumble Bee Colonization, Extinction, and Reproduction in Subalpine Meadows in Northeastern Utah. Ecology 66:914.CrossRefGoogle Scholar
  9. Boyle, N. K., A. D. Tripodi, S. A. Machtley, J. P. Strange, T. L. Pitts-Singer, and J. R. Hagler. 2018. A Nonlethal Method to Examine Non-Apis Bees for Mark-Capture Research. J. Insect Sci. 18.Google Scholar
  10. Brown, L. M., R. K. Fuda, N. Schtickzelle, H. Coffman, A. Jost, A. Kazberouk, E. Kemper, E. Sass, and E. E. Crone. 2017. Using animal movement behavior to categorize land cover and predict consequences for connectivity and patch residence times. Landsc. Ecol. 32:1657–1670.CrossRefGoogle Scholar
  11. Cameron, S. A. 1981. Chemical signals in bumble bee foraging. Behav. Ecol. Sociobiol. 9:257–260.CrossRefGoogle Scholar
  12. Cameron, S. A., H. C. Lim, J. D. Lozier, M. A. Duennes, and R. Thorp. 2016. Test of the invasive pathogen hypothesis of bumble bee decline in North America. Proc. Natl. Acad. Sci. 113:4386–4391.CrossRefPubMedGoogle Scholar
  13. Cameron, S. A., J. D. Lozier, J. P. Strange, J. B. Koch, N. Cordes, L. F. Solter, and T. L. Griswold. 2011. Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. 108:662–667.CrossRefPubMedGoogle Scholar
  14. Capaldi, E. A., A. D. Smith, J. L. Osborne, S. E. Fahrbach, S. M. Farris, D. R. Reynolds, A. S. Edwards, A. Martin, G. E. Robinson, G. M. Poppy, and J. R. Riley. 2000. Ontogeny of orientation flight in the honeybee revealed by harmonic radar. Nature 403:537–540.CrossRefPubMedGoogle Scholar
  15. Cartar, R. V. 2004. Resource Tracking by Bumble Bees: Responses to Plant-Level Differences in Quality. Ecology 85:2764–2771.CrossRefGoogle Scholar
  16. Carvell, C., A. F. G. Bourke, S. Dreier, S. N. Freeman, S. Hulmes, W. C. Jordan, J. W. Redhead, S. Sumner, J. Wang, and M. S. Heard. 2017. Bumblebee family lineage survival is enhanced in high-quality landscapes. Nature 543:547.CrossRefPubMedGoogle Scholar
  17. Carvell, C., W. C. Jordan, A. F. G. Bourke, R. Pickles, J. W. Redhead, and M. S. Heard. 2012. Molecular and spatial analyses reveal links between colony-specific foraging distance and landscape-level resource availability in two bumblebee species. Oikos 121:734–742.CrossRefGoogle Scholar
  18. Carvell, C., D. B. Roy, S. M. Smart, R. F. Pywell, C. D. Preston, and D. Goulson. 2006. Declines in forage availability for bumblebees at a national scale. Biol. Conserv. 132:481–489.CrossRefGoogle Scholar
  19. Chapman, R. E., J. Wang, and A. F. G. Bourke. 2003. Genetic analysis of spatial foraging patterns and resource sharing in bumble bee pollinators. Mol. Ecol. 12:2801–2808.CrossRefPubMedGoogle Scholar
  20. Cnaani, J., J. D. Thomson, and D. R. Papaj. 2006. Flower Choice and Learning in Foraging Bumblebees: Effects of Variation in Nectar Volume and Concentration. Ethology 112:278–285.CrossRefGoogle Scholar
  21. Collett, T. S. 1996. Insect navigation en route to the goal: multiple strategies for the use of landmarks. J. Exp. Biol. 199:227–235.CrossRefPubMedGoogle Scholar
  22. Comba, L. 1999. Patch use by bumblebees (Hymenoptera Apidae): temperature, wind, flower density and traplining. Ethol. Ecol. Evol. 11:243–264.CrossRefGoogle Scholar
  23. Cooke, S. J., S. G. Hinch, M. Wikelski, R. D. Andrews, L. J. Kuchel, T. G. Wolcott, and P. J. Butler. 2004. Biotelemetry: a mechanistic approach to ecology. Trends Ecol. Evol. 19:334–343.CrossRefPubMedGoogle Scholar
  24. Crall, J. D., N. Gravish, A. M. Mountcastle, and S. A. Combes. 2015. BEEtag: A Low-Cost, Image-Based Tracking System for the Study of Animal Behavior and Locomotion. PLoS One 10:e0136487.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Crall, J. D., C. M. Switzer, R. L. Oppenheimer, A. N. F. Versypt, B. Dey, A. Brown, M. Eyster, C. Guérin, N. E. Pierce, S. A. Combes, and B. L. de Bivort. 2018. Neonicotinoid exposure disrupts bumblebee nest behavior, social networks, and thermoregulation. Science 362:683–686.CrossRefPubMedGoogle Scholar
  26. Cresswell, J. E., J. L. Osborne, and D. Goulson. 2000. An economic model of the limits to foraging range in central place foragers with numerical solutions for bumblebees. Ecol. Entomol. 25:249–255.CrossRefGoogle Scholar
  27. Darvill, B., M. E. Knight, and D. Goulson. 2004. Use of Genetic Markers to Quantify Bumblebee Foraging Range and Nest Density. Oikos 107:471–478.CrossRefGoogle Scholar
  28. Darvill, B., S. O’Connor, G. C. Lye, J. Waters, O. Lepais, and D. Goulson. 2010. Cryptic differences in dispersal lead to differential sensitivity to habitat fragmentation in two bumblebee species. Mol. Ecol. 19:53–63.CrossRefPubMedGoogle Scholar
  29. Dramstad, W. E. 1996. Do bumblebees (Hymenoptera: Apidae) really forage close to their nests? J. Insect Behav. 9:163–182.CrossRefGoogle Scholar
  30. Dukas, R., and L. Edelstein-Keshet. 1998. The Spatial Distribution of Colonial Food Provisioners. J. Theor. Biol. 190:121–134.CrossRefGoogle Scholar
  31. Elliott, S. E. 2009. Subalpine bumble bee foraging distances and densities in relation to flower availability. Environ. Entomol. 38:748–756.CrossRefPubMedGoogle Scholar
  32. Fabre, J.-H. 1918. The mason-bees. Dodd, Mead.Google Scholar
  33. Free, J. B. 1993. Insect pollination of crops. 2nd Edition. Academic Press Inc.Google Scholar
  34. Gill, R. J., O. Ramos-Rodriguez, and N. E. Raine. 2012. Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491:105.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Gillespie S. D., and Adler L. S. 2013. Indirect effects on mutualisms: parasitism of bumble bees and pollination service to plants. Ecology 94:454–464.CrossRefPubMedGoogle Scholar
  36. Gillespie, S. D., K. Carrero, and L. S. Adler. 2015. Relationships between parasitism, bumblebee foraging behaviour, and pollination service to Trifolium pratense flowers. Ecol. Entomol. 40:650–653.CrossRefGoogle Scholar
  37. Gosterit, A., and V. C. Baskar. 2016. Impacts of commercialization on the developmental characteristics of native Bombus terrestris (L.) colonies. Insect. Soc. 63:609–614.CrossRefGoogle Scholar
  38. Goulson, D. 2009. Bumblebees: Behaviour, Ecology, and Conservation. 2 edition. Oxford University Press, Oxford; New YorkGoogle Scholar
  39. Goulson, D., G. C. Lye, and B. Darvill. 2008. Decline and Conservation of Bumble Bees. Annu. Rev. Entomol. 53:191–208.CrossRefPubMedGoogle Scholar
  40. Goulson, D., E. Nicholls, C. Botias, and E. L. Rotheray. 2015. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Goulson, D., and J. Stout. 2001. Homing ability of the bumblebee Bombus terrestris (Hymenoptera: Apidae). Apidologie 32:105–111.CrossRefGoogle Scholar
  42. Greenleaf, S. S., N. M. Williams, R. Winfree, and C. Kremen. 2007. Bee foraging ranges and their relationship to body size. Oecologia 153:589–596.CrossRefPubMedGoogle Scholar
  43. Grixti, J. C., L. T. Wong, S. A. Cameron, and C. Favret. 2009. Decline of bumble bees (Bombus) in the North American Midwest. Biol. Conserv. 142:75–84.CrossRefGoogle Scholar
  44. Hadfield, J. D., D. S. Richardson, and T. Burke. 2006. Towards unbiased parentage assignment: combining genetic, behavioural and spatial data in a Bayesian framework. Mol. Ecol. 15:3715–3730.CrossRefPubMedGoogle Scholar
  45. Hagen, M., M. Wikelski, and W. D. Kissling. 2011. Space use of bumblebees (Bombus spp.) revealed by radio-tracking. PLoS One 6:e19997.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Hagler, J. R., S. E. Naranjo, S. A. Machtley, and F. Blackmer. 2014. Development of a standardized protein immunomarking protocol for insect mark–capture dispersal research. J. Appl. Entomol. 138:772–782.CrossRefGoogle Scholar
  47. Hanski, I. 1998. Metapopulation dynamics. Nature 396:41–49.CrossRefGoogle Scholar
  48. Harder, L. D. 1986. Influences on the density and dispersion of bumble bee nests (Hymenoptera: Apidae). Ecography 9:99–103.CrossRefGoogle Scholar
  49. Haskell, J. P., M. E. Ritchie, and H. Olff. 2002. Fractal geometry predicts varying body size scaling relationships for mammal and bird home ranges. Nature 418:527–530.CrossRefPubMedGoogle Scholar
  50. Heinrich, B. 1979. “Majoring” and “Minoring” by Foraging Bumblebees, Bombus Vagans: An Experimental Analysis. Ecology 60:246–255.CrossRefGoogle Scholar
  51. Hemberger, J., and C. Gratton. 2018. Floral resource pulse decreases bumble bee foraging trip duration in central Wisconsin agroecosystem. Ecol. Entomol. 43.Google Scholar
  52. Holyoak, M., R. Casagrandi, R. Nathan, E. Revilla, and O. Spiegel. 2008. Trends and missing parts in the study of movement ecology. Proc. Natl. Acad. Sci. 105:19060–19065.CrossRefPubMedGoogle Scholar
  53. Ims, R. A., and N. G. Yoccoz. 1997. Studying transfer processes in metapopulations: emigration, migration, and colonization. Pages 247–265 Metapopulation biology. Elsevier.Google Scholar
  54. Jacobson, M. M., E. M. Tucker, M. E. Mathiasson, and S. M. Rehan. 2018. Decline of bumble bees in northeastern North America, with special focus on Bombus terricola. Biol. Conserv. 217:437–445.CrossRefGoogle Scholar
  55. Jha, S., and C. Kremen. 2013. Resource diversity and landscape-level homogeneity drive native bee foraging. Proc. Natl. Acad. Sci. 110:555–558.CrossRefPubMedGoogle Scholar
  56. Jha, S., L. Stefanovich, and C. Kremen. 2013. Bumble bee pollen use and preference across spatial scales in human-altered landscapes. Ecological Entomology 38:570–579.CrossRefGoogle Scholar
  57. Jønsson, K. A., A. P. Tøttrup, M. K. Borregaard, S. A. Keith, C. Rahbek, and K. Thorup. 2016. Tracking Animal Dispersal: From Individual Movement to Community Assembly and Global Range Dynamics. Trends Ecol. Evol. 31:204–214.CrossRefPubMedGoogle Scholar
  58. Kadoya, T., and I. Washitani. 2010. Predicting the rate of range expansion of an invasive alien bumblebee (Bombus terrestris) using a stochastic spatio-temporal model. Biol. Conserv. 143:1228–1235.CrossRefGoogle Scholar
  59. Keller, A., N. Danner, G. Grimmer, M. Ankenbrand, K. von der Ohe, W. von der Ohe, S. Rost, S. Härtel, and I. Steffan-Dewenter. 2015. Evaluating multiplexed next-generation sequencing as a method in palynology for mixed pollen samples. Plant Biol. 17:558–566.CrossRefPubMedGoogle Scholar
  60. Kerr, J. T., A. Pindar, P. Galpern, L. Packer, S. G. Potts, S. M. Roberts, P. Rasmont, O. Schweiger, S. R. Colla, L. L. Richardson, D. L. Wagner, L. F. Gall, D. S. Sikes, and A. Pantoja. 2015. Climate change impacts on bumblebees converge across continents. Science 349:177–180.CrossRefPubMedGoogle Scholar
  61. Kerr, N. Z., E. E. Crone, and N. M. Williams. 2019. Integrating vital rates explains optimal worker size for resource return by bumblebee workers. Funct. Ecol. 33:467–478.CrossRefGoogle Scholar
  62. Kissling, W. D., D. E. Pattemore, and M. Hagen. 2014. Challenges and prospects in the telemetry of insects: Insect telemetry. Biol. Rev. 89:511–530.CrossRefGoogle Scholar
  63. Klein, A.-M., B. E. Vaissiere, J. H. Cane, I. Steffan-Dewenter, S. A. Cunningham, C. Kremen, and T. Tscharntke. 2007. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci. 274:303–313.CrossRefGoogle Scholar
  64. Kraus, F. B., S. Wolf, and R. F. A. Moritz. 2009. Male flight distance and population substructure in the bumblebee Bombus terrestris. J. Anim. Ecol. 78:247–252.CrossRefPubMedGoogle Scholar
  65. Kremen, C., N. M. Williams, M. A. Aizen, B. Gemmill-Herren, G. LeBuhn, R. Minckley, L. Packer, S. G. Potts, T. Roulston, I. Steffan-Dewenter, D. P. Vázquez, R. Winfree, L. Adams, E. E. Crone, S. S. Greenleaf, T. H. Keitt, A.-M. Klein, J. Regetz, and T. H. Ricketts. 2007. Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol. Lett. 10:299–314.CrossRefPubMedGoogle Scholar
  66. Kremen, C., N. M. Williams, and R. W. Thorp. 2002. Crop pollination from native bees at risk from agricultural intensification. Proc. Natl. Acad. Sci. 99:16812–16816.CrossRefPubMedGoogle Scholar
  67. Leonard, A. S., A. Dornhaus, and D. R. Papaj. 2011. Flowers help bees cope with uncertainty: signal detection and the function of floral complexity. J. Exp. Biol. 214:113–121.CrossRefPubMedGoogle Scholar
  68. Leonard, A. S., and D. R. Papaj. 2011. ‘X’ marks the spot: The possible benefits of nectar guides to bees and plants. Funct. Ecol. 25:1293–1301.CrossRefGoogle Scholar
  69. Lepais, O., B. Darvill, S. O’Connor, J. L. Osborne, R. A. Sanderson, J. Cussans, L. Goffe, and D. Goulson. 2010. Estimation of bumblebee queen dispersal distances using sibship reconstruction method: Estimation of bumblebee queen dispersal. Mol. Ecol. 19:819–831.CrossRefPubMedGoogle Scholar
  70. Li, J., W. Chen, J. Wu, W. Peng, J. An, P. Schmid-Hempel, and R. Schmid-Hempel. 2012. Diversity of Nosema associated with bumblebees (Bombus spp.) from China. Int. J. Parasitol. 42:49–61.CrossRefGoogle Scholar
  71. Lihoreau, M., N. E. Raine, A. M. Reynolds, R. J. Stelzer, K. S. Lim, A. D. Smith, J. L. Osborne, and L. Chittka. 2012. Radar Tracking and Motion-Sensitive Cameras on Flowers Reveal the Development of Pollinator Multi-Destination Routes over Large Spatial Scales. PLoS Biol. 10:e1001392.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Long, J. A., and T. A. Nelson. 2013. A review of quantitative methods for movement data. Int. J. Geogr. Inf. Sci. 27:292–318.CrossRefGoogle Scholar
  73. Makinson, J. C., J. L. Woodgate, A. Reynolds, E. A. Capaldi, C. J. Perry, and L. Chittka. 2019. Harmonic radar tracking reveals random dispersal pattern of bumblebee ( Bombus terrestris ) queens after hibernation. Sci. Rep. 9:4651.CrossRefPubMedPubMedCentralGoogle Scholar
  74. Malfi, R. L., J. A. Walter, T. H. Roulston, C. Stuligross, S. McIntosh, and L. Bauer. 2018. The influence of conopid flies on bumble bee colony productivity under different food resource conditions. Ecol. Monogr. 88:653–671.CrossRefGoogle Scholar
  75. Manning, A. 1956. Some Aspects of the Foraging Behaviour of Bumble-Bees. Behaviour 9:164–200.CrossRefGoogle Scholar
  76. Martin, A. P., N. L. Carreck, J. L. Swain, D. Goulson, M. E. Knight, R. J. Hale, R. A. Sanderson, and J. L. Osborne. 2006. A modular system for trapping and mass-marking bumblebees: applications for studying food choice and foraging range. Apidologie 37:341–350.CrossRefGoogle Scholar
  77. McFrederick, Q. S., and S. M. Rehan. 2016. Characterization of pollen and bacterial community composition in brood provisions of a small carpenter bee. Mol. Ecol. 25:2302–2311.CrossRefPubMedGoogle Scholar
  78. Menzel, R., U. Greggers, A. Smith, S. Berger, R. Brandt, S. Brunke, G. Bundrock, S. Hülse, T. Plümpe, and F. Schaupp. 2005. Honey bees navigate according to a map-like spatial memory. Proc. Natl. Acad. Sci. U. S. A. 102:3040–3045.CrossRefPubMedPubMedCentralGoogle Scholar
  79. Minter, M., A. Pearson, K. S. Lim, K. Wilson, J. W. Chapman, and C. M. Jones. 2018. The tethered flight technique as a tool for studying life-history strategies associated with migration in insects. Ecol. Entomol. 43:397–411.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Morales, C. L., M. P. Arbetman, S. A. Cameron, and M. A. Aizen. 2013. Rapid ecological replacement of a native bumble bee by invasive species. Front. Ecol. Environ. 11:529–534.CrossRefGoogle Scholar
  81. Nathan, R., W. M. Getz, E. Revilla, M. Holyoak, R. Kadmon, D. Saltz, and P. E. Smouse. 2008. A movement ecology paradigm for unifying organismal movement research. Proc. Natl. Acad. Sci. 105:19052–19059.CrossRefPubMedGoogle Scholar
  82. Nichols, J. D., and A. Kaiser. 1999. Quantitative studies of bird movement: a methodological review. Bird Study 46:S289–S298.CrossRefGoogle Scholar
  83. van Nieuwstadt, M. G. L. , and C. E. R. Iraheta. 1996. Relation between size and foraging range in stingless bees (Apidae, Meliponinae). Apidologie 27:219–228.CrossRefGoogle Scholar
  84. Nunes-Silva, P., M. Hrncir, J. T. F. Guimarães, H. Arruda, L. Costa, G. Pessin, J. O. Siqueira, P. de Souza, and V. L. Imperatriz-Fonseca. 2018. Applications of RFID technology on the study of bees. Insect. Soc. 66:15–24CrossRefGoogle Scholar
  85. O’Connor, S. A. 2013. The Nesting Ecology of Bumblebees. PhD Thesis, University of Stirling.Google Scholar
  86. O’Connor, S., K. J. Park, and D. Goulson. 2012. Humans versus dogs; a comparison of methods for the detection of bumble bee nests. J. Apic. Res. 51:204–211.CrossRefGoogle Scholar
  87. Ogilvie, J. E., and J. D. Thomson. 2016. Site fidelity by bees drives pollination facilitation in sequentially blooming plant species. Ecology 97:1442–1451.CrossRefPubMedGoogle Scholar
  88. Ollerton, J., R. Winfree, and S. Tarrant. 2011. How many flowering plants are pollinated by animals? Oikos 120:321–326.CrossRefGoogle Scholar
  89. Osborne, J. l., S. j. Clark, R. j. Morris, I. h. Williams, J. r. Riley, A. d. Smith, D. r. Reynolds, and A. s. Edwards. 1999. A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar. J. Appl. Ecol. 36:519–533.CrossRefGoogle Scholar
  90. Osborne, J. L., A. P. Martin, N. L. Carreck, J. L. Swain, M. E. Knight, D. Goulson, R. J. Hale, and R. A. Sanderson. 2008. Bumblebee Flight Distances in Relation to the Forage Landscape. J. Anim. Ecol. 77:406–415.CrossRefPubMedGoogle Scholar
  91. Ovaskainen, O., H. Rekola, E. Meyke, and E. Arjas. 2008. Bayesian Methods for Analyzing Movements in Heterogeneous Landscapes from Mark–Recapture Data. Ecology 89:542–554.CrossRefPubMedGoogle Scholar
  92. Papi, F. 2012. Animal homing. Springer Science & Business Media.Google Scholar
  93. Pasquet, R. S., A. Peltier, M. B. Hufford, E. Oudin, J. Saulnier, L. Paul, J. T. Knudsen, H. R. Herren, and P. Gepts. 2008. Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. Proc. Natl. Acad. Sci. 105(36):13456-13461CrossRefPubMedGoogle Scholar
  94. Plischuk, S., R. Martín-Hernández, L. Prieto, M. Lucía, C. Botías, A. Meana, A. H. Abrahamovich, C. Lange, and M. Higes. 2009. South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia), an emerging pathogen of honeybees (Apis mellifera). Environ. Microbiol. Rep. 1:131–135.CrossRefGoogle Scholar
  95. Pope, N. S., and S. Jha. 2017. Inferring the foraging ranges of social bees from sibling genotypes sampled across discrete locations. Conserv. Genet. 18:645–658. 1–14.CrossRefGoogle Scholar
  96. Pope, N. S., and S. Jha. 2018. Seasonal Food Scarcity Prompts Long-Distance Foraging by a Wild Social Bee. Am. Nat. 191:45–57.CrossRefPubMedGoogle Scholar
  97. Raine, N. E., and L. Chittka. 2007. The Adaptive Significance of Sensory Bias in a Foraging Context: Floral Colour Preferences in the Bumblebee Bombus terrestris. PLoS One 2:e556.CrossRefPubMedPubMedCentralGoogle Scholar
  98. Raine, N. E., and L. Chittka. 2008. The correlation of learning speed and natural foraging success in bumble-bees. Proc. R. Soc. B Biol. Sci. 275:803–808.CrossRefGoogle Scholar
  99. Rao, S., G. Hoffman, J. Kirby, and D. Horne. 2019. Remarkable long-distance returns to a forage patch by artificially displaced wild bumble bees (Hymenoptera: Apidae). J. Apic. Res. 0:1–9.Google Scholar
  100. Rao, S., and J. P. Strange. 2012. Bumble Bee (Hymenoptera: Apidae) Foraging Distance and Colony Density Associated With a Late-Season Mass Flowering Crop. Environ. Entomol. 41:905–915.CrossRefGoogle Scholar
  101. Rathcke, B. J., and E. S. Jules. 1993. Habitat fragmentation and plant–pollinator interactions. Curr. Sci. 65:273–277.Google Scholar
  102. Rau, P. 1929. Experimental studies in the homing of carpenter and mining bees. J. Comp. Psychol. 9:35.CrossRefGoogle Scholar
  103. Redhead, J. W., S. Dreier, A. F. Bourke, M. S. Heard, W. C. Jordan, S. Sumner, J. Wang, and C. Carvell. 2016. Effects of habitat composition and landscape structure on worker foraging distances of five bumblebee species. Ecol. Appl. 26:726–739.CrossRefPubMedGoogle Scholar
  104. Reynolds, A. M., A. D. Smith, R. Menzel, U. Greggers, D. R. Reynolds, and J. R. Riley. 2007. Displaced Honey Bees Perform Optimal Scale-Free Search Flights. Ecology 88:1955–1961.CrossRefPubMedGoogle Scholar
  105. Reynolds, D. R., and J. R. Riley. 2002. Remote-sensing, telemetric and computer-based technologies for investigating insect movement: a survey of existing and potential techniques. Comput. Electron. Agric. 35:271–307.CrossRefGoogle Scholar
  106. Riley, J. R., U. Greggers, A. D. Smith, D. R. Reynolds, and R. Menzel. 2005. The flight paths of honeybees recruited by the waggle dance. Nature 435:205.CrossRefPubMedGoogle Scholar
  107. Rossel, S. 1993. Navigation by bees using polarized skylight. Comp. Biochem. Physiol: A: Comparative physiology 104:695-708CrossRefGoogle Scholar
  108. Rundlöf, M., G. K. S. Andersson, R. Bommarco, I. Fries, V. Hederström, L. Herbertsson, O. Jonsson, B. K. Klatt, T. R. Pedersen, J. Yourstone, and H. G. Smith. 2015. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature.Google Scholar
  109. Samuelson, E. E. W., Z. P. Chen-Wishart, R. J. Gill, and E. Leadbeater. 2016. Effect of acute pesticide exposure on bee spatial working memory using an analogue of the radial-arm maze. Sci. Rep. 6:38957CrossRefPubMedPubMedCentralGoogle Scholar
  110. Schmid-Hempel, P., and S. Durrer. 1991. Parasites, Floral Resources and Reproduction in Natural Populations of Bumblebees. Oikos 62:342–350.CrossRefGoogle Scholar
  111. Schmid-Hempel, R., M. Eckhardt, D. Goulson, D. Heinzmann, C. Lange, S. Plischuk, L. R. Escudero, R. Salathé, J. J. Scriven, and P. Schmid-Hempel. 2014. The invasion of southern South America by imported bumblebees and associated parasites. J. Anim. Ecol. 83:823–837.CrossRefGoogle Scholar
  112. Schultz, C. B., and E. E. Crone. 2001. Edge-mediated dispersal behavior in a prairie butterfly. Ecology 82:1879–1892.CrossRefGoogle Scholar
  113. Silcox, D. E., J. P. Doskocil, C. E. Sorenson, and R. L. Brandenburg. 2011. Radio frequency identification tagging: a novel approach to monitoring surface and subterranean insects. Am. Entomol. 57:86–93.CrossRefGoogle Scholar
  114. Sirois-Delisle, C., and J. T. Kerr. 2018. Climate change-driven range losses among bumblebee species are poised to accelerate. Sci. Rep. 8:14464.CrossRefPubMedPubMedCentralGoogle Scholar
  115. Sivakoff, F. S., J. A. Rosenheim, and J. R. Hagler. 2012. Relative dispersal ability of a key agricultural pest and its predators in an annual agroecosystem. Biol. Control 63:296–303.CrossRefGoogle Scholar
  116. Southwick, E. E., and S. L. Buchmann. 1995. Effects of Horizon Landmarks on Homing Success in Honey Bees. Am. Nat. 146:748–764.CrossRefGoogle Scholar
  117. Sutcliffe, O. L., and C. D. Thomas. 1996. Open Corridors Appear to Facilitate Dispersal by Ringlet Butterflies (Aphantopus hyperantus) between Woodland Clearings. Conserv. Biol. 10:1359–1365.CrossRefGoogle Scholar
  118. Suzuki, Y., L. G. Kawaguchi, and Y. Toquenaga. 2007. Estimating nest locations of bumblebee Bombus ardens from flower quality and distribution. Ecol. Res. 22:220–227.CrossRefGoogle Scholar
  119. Switzer, C. M., and S. A. Combes. 2016. Bombus impatiens (Hymenoptera: Apidae) display reduced pollen foraging behavior when marked with bee tags vs. paint. J. Melittol. 0:1–13.CrossRefGoogle Scholar
  120. Thomson, J. D. 1982. Patterns of Visitation by Animal Pollinators. Oikos 39:241–250.CrossRefGoogle Scholar
  121. Thomson, J. D. 1996. Trapline foraging by bumblebees: I. Persistence of flight-path geometry. Behav. Ecol. 7:158–164.CrossRefGoogle Scholar
  122. Tomkiewicz, S. M., M. R. Fuller, J. G. Kie, and K. K. Bates. 2010. Global positioning system and associated technologies in animal behaviour and ecological research. Philos. Trans. Royal Soc. London B: Biol. Sci. 365:2163–2176.CrossRefGoogle Scholar
  123. Walther-Hellwig, K., and R. Frankl. 2000. Foraging habitats and foraging distances of bumblebees, Bombus spp.(Hym., Apidae), in an agricultural landscape. J. Appl. Entomol. 124:299–306.CrossRefGoogle Scholar
  124. Wang, J. 2004. Sibship Reconstruction From Genetic Data With Typing Errors. Genetics 166:1963–1979.CrossRefPubMedPubMedCentralGoogle Scholar
  125. Westphal, C., I. Seffan-Dewenter, and T. Tscharntke. 2006. Foraging trip duration of bumblebees in relation to landscape-wide resource availability. Ecol. Entomol. 31:389–394.CrossRefGoogle Scholar
  126. White, G. C., and R. A. Garrott. 2012. Analysis of wildlife radio-tracking data. Elsevier.Google Scholar
  127. Wikelski, M., R. W. Kays, N. J. Kasdin, K. Thorup, J. A. Smith, and G. W. Swenson. 2007. Going wild: what a global small-animal tracking system could do for experimental biologists. J. Exp. Biol. 210:181–186.CrossRefPubMedGoogle Scholar
  128. Wikelski, M., J. Moxley, A. Eaton-Mordas, M. M. Lopez-Uribe, R. Holland, D. Moskowitz, D. W. Roubik, and R. Kays. 2010. Large-range movements of neotropical orchid bees observed via radio telemetry. PLoS One 5:e10738.CrossRefPubMedPubMedCentralGoogle Scholar
  129. Williams, N. M., E. E. Crone, T. H. Roulston, R. L. Minckley, L. Packer, and S. G. Potts. 2010. Ecological and life-history traits predict bee species responses to environmental disturbances. Biol. Conserv. 143:2280–2291.CrossRefGoogle Scholar
  130. Williams, N. M., J. Regetz, and C. Kremen. 2011. Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. Ecology 93:1049–1058.CrossRefGoogle Scholar
  131. Williams, P. H., and J. L. Osborne. 2009. Bumblebee vulnerability and conservation world-wide. Apidologie 40:367–387.CrossRefGoogle Scholar
  132. Wolf, S., D. P. McMahon, K. S. Lim, C. D. Pull, S. J. Clark, R. J. Paxton, and J. L. Osborne. 2014. So Near and Yet So Far: Harmonic Radar Reveals Reduced Homing Ability of Nosema Infected Honeybees. PLoS One 9:e103989.CrossRefPubMedPubMedCentralGoogle Scholar
  133. Woodard, S. H., and S. Jha. 2017. Wild bee nutritional ecology: predicting pollinator population dynamics, movement, and services from floral resources. Curr. Opin. Insect Sci. 21:83–90.CrossRefPubMedGoogle Scholar
  134. Woodgate, J. L., J. C. Makinson, K. S. Lim, A. M. Reynolds, and L. Chittka. 2016. Life-Long Radar Tracking of Bumblebees. PLoS One 11:e0160333.CrossRefPubMedPubMedCentralGoogle Scholar
  135. Woodgate, J. L., J. C. Makinson, K. S. Lim, A. M. Reynolds, and L. Chittka. 2017. Continuous Radar Tracking Illustrates the Development of Multi-destination Routes of Bumblebees. Sci. Rep. 7:17323CrossRefPubMedPubMedCentralGoogle Scholar
  136. Zurbuchen, A., S. Cheesman, J. Klaiber, A. Müller, S. Hein, and S. Dorn. 2010a. Long foraging distances impose high costs on offspring production in solitary bees. J. Anim. Ecol. 79:674–681.CrossRefPubMedGoogle Scholar
  137. Zurbuchen, A., L. Landert, J. Klaiber, A. Müller, S. Hein, and S. Dorn. 2010b. Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol. Conserv. 143:669–676.CrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Graduate Group in Ecology & Department of EntomologyUniversity of California DavisDavisUSA

Personalised recommendations