Accounting for imperfect detection in species with sessile life cycle stages: a case study of bumble bee nests

Abstract

For bumble bees and other social organisms, colonies are the functional unit of the population rather than the individual workers. Estimates of bumble bee nest density are thus critical for understanding population distribution and trends of this important pollinator group. Yet, surveys of bumble bee nests and other taxa with sessile life stages rarely account for imperfect detection. Here, we demonstrate the use of mark-recapture methods to estimate the density of bumble bee nests at multiple sites using standardized survey protocols. We detected ~ 30% of nests in a 2-h survey of each 3000 m2 plot. We determined that 4–5 visits were sufficient to estimate the total number of nests at our site with reasonable precision, equating to one-third the effort previously assumed necessary to reliably estimate nest density. Mark-recapture approaches can be used to generate unbiased estimates of density with reduced search effort, while simultaneously increasing the rate at which nests are discovered.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Data availability

All data and code associated with these analyses will be archived in Dryad Digital Repository upon acceptance of this manuscript.

References

  1. Berberich GM, Dormann CF, Klimetzek D, Berberich MB, Sanders NJ, Ellison AM (2016) Detection probabilities for sessile organisms. Ecosphere 7:e01546. https://doi.org/10.1002/ecs2.1546

    Article  Google Scholar 

  2. Brown LM, Breed GA, Severns PM, Crone EE (2017) Losing a battle but winning the war: moving past preference–performance to understand native herbivore–novel host plant interactions. Oecologia 183:441–453. https://doi.org/10.1007/s00442-016-3787-y

    Article  PubMed  Google Scholar 

  3. Couvillon MJ, Fitzpatrick G, Dornhaus A (2010) Ambient air temperature does not predict whether small or large workers forage in bumble bees (Bombus impatiens). Psyche 2010:536430. https://doi.org/10.1155/2010/536430

    Article  PubMed  Google Scholar 

  4. Crone EE, Williams NM (2016) Bumble bee colony dynamics: quantifying the importance of land use and floral resources for colony growth and queen production. Ecol Lett 19:460–468. https://doi.org/10.1111/ele.12581

    Article  PubMed  Google Scholar 

  5. Cumber R (1953) Some aspects of the biology and ecology of humble-bees bearing upon the yields of red-clover seed in New Zealand. N Z J Sci Technol 34:227–240

    Google Scholar 

  6. Darvill B, Knight ME, Goulson D (2004) Use of genetic markers to quantify bumblebee foraging range and nest density. Oikos 107:471–478. https://doi.org/10.1111/j.0030-1299.2004.13510.x

    Article  Google Scholar 

  7. Fussell M, Corbet SA (1992) The nesting places of some British bumble bees. J Apic Res 31:32–41. https://doi.org/10.1080/00218839.1992.11101258

    Article  Google Scholar 

  8. Goulson D (2010) Bumblebees: behaviour, ecology, and conservation, 2nd edn. Oxford University Press, New York, p 317

    Google Scholar 

  9. 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 47:1207–1215. https://doi.org/10.1111/j.1365-2664.2010.01872.x

    Article  Google Scholar 

  10. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153(3):589–596.

    Article  Google Scholar 

  11. Gu W, Swihart RK (2004) Absent or undetected? Effects of non-detection of species occurrence on wildlife–habitat models. Biol Conserv 116:195–203. https://doi.org/10.1016/S0006-3207(03)00190-3

    Article  Google Scholar 

  12. Harder LD (1986) Influences on the density and dispersion of bumble bee nests (Hymenoptera: Apidae). Ecography 9:99–103. https://doi.org/10.1111/j.1600-0587.1986.tb01196.x

    Article  Google Scholar 

  13. Heard M, Carvell C, Carreck N, Rothery P, Osborne J, Bourke A (2007) Landscape context not patch size determines bumble-bee density on flower mixtures sown for agri-environment schemes. Biol Lett 3:638–641. https://doi.org/10.1098/rsbl.2007.0425

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Herrmann F, Westphal C, Moritz RF, Steffan-Dewenter I (2007) Genetic diversity and mass resources promote colony size and forager densities of a social bee (Bombus pascuorum) in agricultural landscapes. Mol Ecol 16:1167–1178. https://doi.org/10.1111/j.1365-294X.2007.03226.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Hobbs GA (1964) Ecology of species of Bombus Latr. (Hymenoptera: Apidae) in Southern Alberta. I. Subgenus Alpinobombus Skor. Can Entomol 96:1465–1470. https://doi.org/10.4039/Ent961465-11

    Article  Google Scholar 

  16. Hobbs GA (1965) Ecology of species of Bombus Latr. (Hymenoptera: Apidae) in Southern Alberta. III. Subgenus Cullumanobombus Vogt. Can Entomol 97:1293–1302. https://doi.org/10.4039/Ent971293-12

    Article  Google Scholar 

  17. Jolly GM (1965) Explicit estimates from capture-recapture data with both death and immigration-stochastic model. Biometrika 52:225–247. https://doi.org/10.2307/2333826

    CAS  Article  PubMed  Google Scholar 

  18. Kellner KF (2018) jagsUI: a wrapper around ‘rjags’ to streamline ‘JAGS’ analyses. R package version 1.5.0. https://CRAN.R-project.org/package=jagsUI

  19. Kellner KF, Swihart RK (2014) Accounting for imperfect detection in ecology: a quantitative review. PLoS ONE 9:e111436. https://doi.org/10.1371/journal.pone.0111436

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Kells AR, Goulson D (2003) Preferred nesting sites of bumblebee queens (Hymenoptera: Apidae) in agroecosystems in the UK. Biol Conserv 109:165–174. https://doi.org/10.1016/S0006-3207(02)00131-3

    Article  Google Scholar 

  21. Kéry M, Schaub M (2012) Bayesian population analysis using WinBUGS: a hierarchical perspective. Academic Press, Cambridge

    Google Scholar 

  22. Kéry M, Schmidt B (2008) Imperfect detection and its consequences for monitoring for conservation. Community Ecol 9:207–216. https://doi.org/10.1556/ComEc.9.2008.2.10

    Article  Google Scholar 

  23. Kwon YJ, Saeed S (2003) Effect of temperature on the foraging activity of Bombus terrestris L. (Hymenoptera: Apidae) on greenhouse hot pepper (Capsicum annuum L.). Appl Entomol Zool 38:275–280. https://doi.org/10.1303/aez.2003.275

    Article  Google Scholar 

  24. Laverty TM, Harder LD (1988) The bumble bees of Eastern Canada. Can Entomol 120:965–987. https://doi.org/10.4039/Ent120965-11

    Article  Google Scholar 

  25. Link WA, Nichols JD (1994) On the importance of sampling variance to investigations of temporal variation in animal population size. Oikos 69:539–544. https://doi.org/10.2307/3545869

    Article  Google Scholar 

  26. Lye GC, Osborne JL, Park KJ, Goulson D (2012) Using citizen science to monitor Bombus populations in the UK: nesting ecology and relative abundance in the urban environment. J Insect Conserv 16:697–707. https://doi.org/10.1007/s10841-011-9450-3

    Article  Google Scholar 

  27. O’Connor S, Park KJ, Goulson D (2012) Humans versus dogs; a comparison of methods for the detection of bumble bee nests. J Apic Res 51:204–211. https://doi.org/10.3896/IBRA.1.51.2.09

    Article  Google Scholar 

  28. O’Connor S, Park KJ, Goulson D (2017) Location of bumblebee nests is predicted by counts of nest-searching queens. Ecol Entomol 42:731–736. https://doi.org/10.1111/een.12440

    Article  Google Scholar 

  29. Osborne JL, Martin AP, Shortall CR, Todd AD, Goulson D, Knight ME, Hale RJ, Sanderson RA (2008) Quantifying and comparing bumblebee nest densities in gardens and countryside habitats. J Appl Ecol 45:784–792. https://doi.org/10.1111/j.1365-2664.2007.01359.x

    Article  Google Scholar 

  30. Otis DL, Burnham KP, White GC, Anderson DR (1978) Statistical inference from capture data on closed animal populations. Wildl Monogr 62:3–135

    Google Scholar 

  31. Plath O (1922) Notes on the nesting habits of several North American bumblebees. Psyche 5–6:189–202. https://doi.org/10.1155/1922/34572

    Article  Google Scholar 

  32. Pollock KH (1982) A capture-recapture design robust to unequal probability of capture. J Wildl Manag 46:752–757. https://doi.org/10.2307/3808568

    Article  Google Scholar 

  33. Pope NS, Jha S (2017) Inferring the foraging ranges of social bees from sibling genotypes sampled across discrete locations. Conserv Gen 18:645–658. https://doi.org/10.1007/s10592-017-0941-y

    Article  Google Scholar 

  34. Pope NS, Jha S (2018) Seasonal food scarcity prompts long-distance foraging by a wild social bee. Am Nat 191:45–57. https://doi.org/10.1086/694843

    Article  PubMed  Google Scholar 

  35. Rao S, Skyrm KM (2013) Nest density of the native bumble bee, Bombus nevadensis Cresson (Hymenoptera: Apoidea), in an agricultural landscape. J Kans Entomol Soc 86:93–97. https://doi.org/10.2317/JKES120708.1

    Article  Google Scholar 

  36. Rao S, Strange JP (2012) Bumble bee (Hymenoptera: Apidae) foraging distance and colony density associated with a late-season mass flowering crop. Environ Entomol 41:905–915. https://doi.org/10.1603/EN11316

    Article  Google Scholar 

  37. Richards KW (1978) Nest site selection by bumble bees (Hymenoptera: Apidae) in southern alberta. Can Entomol 110:301–318. https://doi.org/10.4039/Ent110301-3

    Article  Google Scholar 

  38. Royle JA, Dorazio RM (2008) Hierarchical modeling and inference in ecology. The analysis of data from populations, metapopulations and communities. Academic Press, London

    Google Scholar 

  39. Schwarz CJ, Arnason AN (1996) A general methodology for the analysis of capture–recapture experiments in open populations. Biometrics 52:860–873. https://doi.org/10.2307/2533048

    Article  Google Scholar 

  40. Seber GF (1965) A note on the multiple-recapture census. Biometrika 52:249–259. https://doi.org/10.2307/2333827

    CAS  Article  PubMed  Google Scholar 

  41. Slade NA, Alexander HM, Dean Kettle W (2003) Estimation of population size and probabilities of survival and detection in Mead’s milkweed. Ecology 84:791–797. https://doi.org/10.1890/0012-9658(2003)084%5b0791:EOPSAP%5d2.0.CO;2

    Article  Google Scholar 

  42. Svensson B, Lagerlöf J, Svensson BG (2000) Habitat preferences of nest-seeking bumble bees (Hymenoptera: Apidae) in an agricultural landscape. Agric Ecosyst Environ 77:247–255. https://doi.org/10.1016/S0167-8809(99)00106-1

    Article  Google Scholar 

  43. Waters J, O’Connor S, Park KJ, Goulson D (2010) Testing a detection dog to locate bumblebee colonies and estimate nest density. Apidologie 42:200–205. https://doi.org/10.1051/apido/2010056

    Article  Google Scholar 

  44. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139. https://doi.org/10.1080/00063659909477239

    Article  Google Scholar 

  45. Williams NM, Minckley RL, Silveira FA (2001) Variation in native bee faunas and its implications for detecting community changes. Conserv Ecol 5:7. https://doi.org/10.5751/ES-00259-050107

    Article  Google Scholar 

  46. Williams BK, Nichols JD, Conroy MJ (2002) Analysis and management of animal populations. Academic Press, New York

    Google Scholar 

  47. Williams NM, Regetz J, Kremen C (2012) Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. Ecology 93:1049–1058. https://doi.org/10.1890/11-1006.1

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Trustees of Reservations and Appleton Farms for providing access to their properties where this study was conducted. We thank Russ Hopping for invaluable assistance in locating study sites. We also thank Annika Greenleaf, Max McCarthy, Moshe Steyn, Erin Wampole, and our sniffer-dogs-in-training, Indy and Molly, for assistance with field work. This work was supported by the US National Science Foundation (DEB1354022) and the US Strategic Environmental Research and Development Program (SERDP, RC-2119).

Author information

Affiliations

Authors

Contributions

All authors conceived of research ideas, designed methodology, and collected field data. DI and EC led statistical analysis and writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Corresponding author

Correspondence to Genevieve Pugesek.

Ethics declarations

Conflict of interest

The authors declare they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Iles, D.T., Pugesek, G., Kerr, N.Z. et al. Accounting for imperfect detection in species with sessile life cycle stages: a case study of bumble bee nests. J Insect Conserv 23, 945–955 (2019). https://doi.org/10.1007/s10841-019-00179-1

Download citation

Keywords

  • Bombus
  • Closed population model
  • Mark-recapture
  • Monitoring
  • Nesting habitat
  • Survey design