Conservation Genetics

, Volume 18, Issue 3, pp 645–658 | Cite as

Inferring the foraging ranges of social bees from sibling genotypes sampled across discrete locations

Research Article


A knowledge of the distances regularly travelled by foraging bees is essential to understanding the movement of pollen across landscapes, and has implications for the conservation of both pollinators and plants. Unfortunately, the movements of bees are difficult to measure directly at ecologically relevant scales. A common strategy for quantifying the foraging ranges of social bees is to sample the genotypes of foragers across a landscape. Individual foragers can be assigned to colonies with polymorphic genetic markers, and the dispersion of siblings in space can be used to make inference about colony locations and foraging movements. Several previous studies have sampled sibling genotypes at discrete locations (for example, at regular points along a transect), rather than in continuous space. Restricting the collection of bees to discrete locations presents a number of considerations for sampling design and data analysis. In this paper, we develop a spatially-explicit, model-based framework for the simulation and estimation of foraging ranges. Using these tools, we simulated experiments to characterise the efficacy of different sampling strategies, and provide an example with actual data that demonstrates the advantages of our method over an approach based on regression.


Social bees Foraging range estimation Sibship reconstruction Sampling design Spatial analysis 



We would like to thank members of the Jha lab at the University of Texas at Austin, attendees of the 2015 Ecological Society of America symposium “Conservation genetics of bee pollinators”, and three anonymous referees for useful comments and criticisms. We acknowledge the Texas Advanced Computing Center (TACC, at the University of Texas at Austin for providing HPC resources that have contributed to the research results reported within this paper. This work was supported by the University of Texas at Austin, the National Science Foundation (NSF DEB 1148679), and the Army Research Office. NP is supported in part by an NSF predoctoral fellowship (NSF DEB 1110007).

Supplementary material

10592_2017_941_MOESM1_ESM.pdf (326 kb)
Supplementary material 1 (PDF 326 kb)


  1. Biernaskie JM, Walker SC, Gegear RJ (2009) Bumblebees learn to forage like Bayesians. Am Nat 174(3):413–423CrossRefPubMedGoogle Scholar
  2. Bohart G (1972) Management of wild bees for the pollination of crops. Annu Rev Entomol 17(1):287–312CrossRefGoogle Scholar
  3. Bond W (1994) Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Philos Trans R Soc Lond B: Biol Sci 344(1307):83–90CrossRefGoogle Scholar
  4. Bondrup-Nielsen S (1983) Density estimation as a function of live-trapping grid and home range size. Can J Zool 61(10):2361–2365CrossRefGoogle Scholar
  5. Carpenter B, Gelman A, Hoffman M, Lee D, Goodrich B, Betancourt M, Brubaker MA, Guo J, Li P, Riddell A (2016) Stan: a probabilistic programming language. J Stat SoftwGoogle Scholar
  6. Chapman R, Wang J, Bourke A (2003) Genetic analysis of spatial foraging patterns and resource sharing in bumble bee pollinators. Mol Ecol 12(10):2801–2808CrossRefPubMedGoogle Scholar
  7. Darvill B, Knight ME, Goulson D (2004) Use of genetic markers to quantify bumblebee foraging range and nest density. Oikos 107(3):471–478CrossRefGoogle Scholar
  8. Dreier S, Redhead JW, Warren IA, Bourke AFG, Heard MS, Jordan WC, Sumner S, Wang J, Carvell C (2014) Fine-scale spatial genetic structure of common and declining bumble bees across an agricultural landscape. Mol Ecol 23(14):3384–3395CrossRefPubMedPubMedCentralGoogle Scholar
  9. Efford M (2004) Density estimation in live-trapping studies. Oikos 106(3):598–610CrossRefGoogle Scholar
  10. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evolut Syst 35:375–403CrossRefGoogle Scholar
  11. Foster RJ, Harmsen BJ (2012) A critique of density estimation from camera-trap data. J Wildl Manag 76(2):224–236CrossRefGoogle Scholar
  12. Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7(4):457–472CrossRefGoogle Scholar
  13. Goulson D, Lepais O, O'Connor S, Osborne JL, Sanderson RA, Cussans J, Goffe L, Darvill B (2010) Effects of land use at a landscape scale on bumblebee nest density and survival. J Appl Ecol 47(6):1207–1215CrossRefGoogle Scholar
  14. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153(3):589–596CrossRefPubMedGoogle Scholar
  15. Hagen M, Wikelski M, Kissling WD (2011) Space use of bumblebees (Bombus spp.) revealed by radio-tracking. PloS ONE 6(5):e19997CrossRefPubMedPubMedCentralGoogle Scholar
  16. Heinrich B (2004) Bumblebee economics. Harvard University Press, LondonGoogle Scholar
  17. Jha S, Dick CW (2010) Native bees mediate long-distance pollen dispersal in a shade coffee landscape mosaic. Proc Natl Acad Sci 107(31):13760–13764CrossRefPubMedPubMedCentralGoogle Scholar
  18. Jha S, Kremen C (2013) Resource diversity and landscape-level homogeneity drive native bee foraging. Proc Natl Acad Sci 110(2):555–558CrossRefPubMedGoogle Scholar
  19. Keitt TH (2009) Habitat conversion, extinction thresholds, and pollination services in agroecosystems. Ecol Appl 19(6):1561–1573CrossRefPubMedGoogle Scholar
  20. Knight ME, Martin AP, Bishop S, Osborne JL, Hale RJ, Sanderson RA, Goulson D (2005) An interspecific comparison of foraging range and nest density of four bumblebee (Bombus) species. Mol Ecol 14(6):1811–1820CrossRefPubMedGoogle Scholar
  21. Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci 99(26):16812–16816CrossRefPubMedPubMedCentralGoogle Scholar
  22. Lihoreau M, Raine NE, Reynolds AM, Stelzer RJ, Lim KS, Smith AD, Osborne JL, Chittka L (2012) Radar tracking and motion-sensitive cameras on flowers reveal the development of pollinator multi-destination routes over large spatial scales. PLoS Biol 10(9):e1001392CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lonsdorf E, Kremen C, Ricketts T, Winfree R, Williams N, Greenleaf S (2009) Modelling pollination services across agricultural landscapes. Ann Bot 103(9):1589–1600CrossRefPubMedPubMedCentralGoogle Scholar
  24. Osborne J, Clark S, Morris R, Williams I, Riley J, Smith A, Reynolds D, Edwards A (1999) A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar. J Appl Ecol 36(4):519–533CrossRefGoogle Scholar
  25. Osborne JL, Martin AP, Carreck NL, Swain JL, Knight ME, Goulson D, Hale RJ, Sanderson RA (2008) Bumblebee flight distances in relation to the forage landscape. J Anim Ecol 77(2):406–415CrossRefPubMedGoogle Scholar
  26. Parmenter RR, Yates TL, Anderson DR, Burnham KP, Dunnum JL, Franklin AB, Friggens MT, Lubow BC, Miller M, Olson GS et al (2003) Small-mammal density estimation: a field comparison of grid-based vs. web-based density estimators. Ecol Monogr 73(1):1–26CrossRefGoogle Scholar
  27. Pearson DE, Ruggiero LF (2003) Transect versus grid trapping arrangements for sampling small-mammal communities. Wildl Soc Bull 31(2):454–459Google Scholar
  28. Robertson AW, Mountjoy C, Faulkner BE, Roberts MV, Macnair MR (1999) Bumble bee selection of Mimulus guttatus flowers: the effects of pollen quality and reward depletion. Ecology 80(8):2594–2606CrossRefGoogle Scholar
  29. Royle JA, Chandler RB, Gazenski KD, Graves TA (2013) Spatial capture-recapture models for jointly estimating population density and landscape connectivity. Ecology 94(2):287–294CrossRefPubMedGoogle Scholar
  30. Royle JA, Chandler RB, Sollmann R, Gardner B (2013) Spatial capture-recapture. Academic Press, CambridgeGoogle Scholar
  31. Schlather M, Malinowski A, Menck PJ, Oesting M, Strokorb K (2015) Analysis, simulation and prediction of multivariate random fields with package random fields. J Stat Softw 63(8):1–25CrossRefGoogle Scholar
  32. Sun CC, Fuller AK, Royle JA (2014) Trap configuration and spacing influences parameter estimates in spatial capture-recapture models. PloS ONE 9(2):e88025CrossRefPubMedPubMedCentralGoogle Scholar
  33. Visscher PK, Seeley TD (1982) Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology 63(6):1790–1801CrossRefGoogle Scholar
  34. Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166(4):1963–1979CrossRefPubMedPubMedCentralGoogle Scholar
  35. Williams NM, Regetz J, Kremen C (2012) Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. Ecology 93(5):1049–1058CrossRefPubMedGoogle Scholar
  36. Worton B (1987) A review of models of home range for animal movement. Ecol Model 38(3):277–298CrossRefGoogle Scholar
  37. Zurbuchen A, Landert L, Klaiber J, Müller A, Hein S, Dorn S (2010) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol Conserv 143(3):669–676CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.Department of Integrative BiologyUniversity of TexasAustinUSA

Personalised recommendations