Advertisement

Woodland and floral richness boost bumble bee density in cranberry resource pulse landscapes

  • Vera PfeifferEmail author
  • Janet Silbernagel
  • Christelle Guédot
  • Juan Zalapa
Research Article

Abstract

Context

Native pollinators provide an important ecosystem service for many pollination-dependent fruit crops, but require nesting and foraging resources in proximity to target crop plants. Landscape context and fluctuation in floral resources may influence the distribution of pollination services.

Objectives

This study investigates how landscape context influences bumble bee density on cranberry marshes across a resource pulse created by the target crop bloom.

Methods

We sampled bumble bees at fourteen cranberry marshes before, during, and after the cranberry bloom in central Wisconsin. We quantified floral richness and surrounding land cover and assessed their effects on bumble bee density and colony representation using OLS regression. We measured colony representation as a colony detection rate—where low colony detection means more colonies were represented by single individual foragers.

Results

The amount of forest surrounding marshes explained the most variation in colony density, but not colony representation on site. Sites with high meadow interspersion in the surrounding landscape had lower colony representation (i.e., detection rate), suggesting some dilution effect. Colony density and detection did not change between the pre- and post-bloom period and resource pulse, even after statistically controlling for important landscape-scale effects. Yet, relative increase in colony density, was best explained by increased floral richness and decreased open-shrub bog. Landscapes with less clumpy forest experienced increased colony representation during the crop bloom.

Conclusions

We suggest maintaining forest within cultivated landscapes to promote local bumble bee colony density, and increasing floral richness on site to attract foraging bees.

Keywords

Bombus Resource pulse Mass-flowering Floral resources Landscape genetics Microsatellites 

Notes

Acknowledgements

We thank Tyler Yanisch, Perla Lozoya, Robin Sandner, Anne Vandenburg, and Aidee Guzman for their help with bee field surveys and DNA extractions and all the cranberry growers who provided access to their marshes for the study. We also thank two anonymous reviewers and the editor for their thoughtful feedback that helped to improve the manuscript. Juan Zalapa was supported by USDA-ARS Project No. 5090-21220-004-00-D. Christelle Guedot was partially funded by the Wisconsin Cranberry Board.

Supplementary material

10980_2019_810_MOESM1_ESM.docx (23 kb)
Supplementary material 1 (DOCX 23 kb)

References

  1. Aizen MA, Harder LD (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19:915–918CrossRefGoogle Scholar
  2. Barton K (2017) MuMIn: multi-model inference. R package version 1(40):4Google Scholar
  3. Bivand R (2018) spdep: Spatial Dependence: weighting schemes, statistics and models. R package version 0.8-1Google Scholar
  4. Blaauw BR, Isaacs R (2014) Flower plantings increase wild bee abundance and the pollination services provided to a pollinator dependent crop. J Appl Ecol 51:890–898CrossRefGoogle Scholar
  5. Bommarco R, Kleijn D, Potts SG (2013) Ecological intensification: Harnessing ecosystem services for food security. Trends Ecol Evol 28:230–238CrossRefGoogle Scholar
  6. Brosi BJ, Armsworth PR, Daily GC (2008) Optimal design of agricultural landscapes for pollination services. Conserv Lett 1:27–36CrossRefGoogle Scholar
  7. Broussard M, Rao S, Stephen WP (2011) Native bees, honeybees, and pollination in Oregon cranberries. HortScience 46:885–888CrossRefGoogle Scholar
  8. Cade B (2015) Model averaging and muddled multimodel inferences. Ecology 96(9):2370–2382CrossRefGoogle Scholar
  9. Cane JH, Schiffhauer D (2003) Dose-response relationships between pollination and fruiting refine pollinator comparisons for cranberry (Vaccinium macrocarpon [Ericaceae]). Am J Bot 90:1425–1432CrossRefGoogle Scholar
  10. Carvell C, Jordan W, Bourke A, Pickles R, Redhead J, Heard M (2012) Molecular and spatial analyses reveal links between colony-specific foraging distance and landscape-level resource availability in two bumblebee species. Oikos 121:734–742CrossRefGoogle Scholar
  11. Carvell C, Osborne JL, Bourke AFG, Freeman SN, Pywell RF, Heard MS (2011) Bumble bee species’ responses to a targeted conservation measure depend on landscape context and habitat quality. Ecol Appl 21:1760–1771CrossRefGoogle Scholar
  12. Darvill B, Knight M, Goulson D (2004) Use of genetic markers to quantify bumblebee foraging range and nest density. Oikos 107:471–478CrossRefGoogle Scholar
  13. Diekotter T, Kadoya T, Franziska P, Wolters V, Jauker F (2010) Oilseed rape crops distort plant-pollinator interactions. J Appl Ecol 47:209–214CrossRefGoogle Scholar
  14. Diekotter T, Peter F, Jauker B, Wolters V, Jauker F (2013) Mass-flowering crops increase richness of cavity-nesting bees and wasps in modern agro-ecosystems. Bioenergy 6(3):219–226Google Scholar
  15. Dramstad WE (1996) Do bumble bees (Hymenoptera: Apidae) really forage close to their nests? J Insect Behav 9:163–182CrossRefGoogle Scholar
  16. ESRI (2011) ArcGIS desktop: release 10. Environmental Systems Research Institute, Redlands, CAGoogle Scholar
  17. Estoup A, Scholl A, Pouvreau A, Solignac M (1995) Monoandry and polyandry in bumble bees (Hymenoptera; Bombinae) as evidenced by highly variable microsatellites. Mol Ecol 4:89–93CrossRefGoogle Scholar
  18. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515CrossRefGoogle Scholar
  19. Fahrig L (2017) Ecological responses to habitat fragmentation per se. Annu Rev Ecol Evol Syst 48:1–23CrossRefGoogle Scholar
  20. Funk R, Schmid-Hempel R, Schmid-Hempel P (2006) Microsatellite loci for Bombus spp. Mol Ecol Notes 6:83–86CrossRefGoogle Scholar
  21. Gaines-Day HR, Gratton C (2015) Biotic and abiotic factors contribute to cranberry pollination. J Pollinat Ecol 15:15–22Google Scholar
  22. Gaines-Day HR, Gratton C (2016) Crop yield is correlated with honey bee hive density but not in high woodland landscapes. Agr Ecosyst Environ 218:53–57CrossRefGoogle Scholar
  23. Galpern P, Johnson SA, Retzlaff JL, Chang D, Swann J (2017) Reduced abundance and earlier collection of bumble bee workers under intensive cultivation of a mass-flowering prairie crop. Ecol Evol 7:2414–2422CrossRefGoogle Scholar
  24. Garibaldi LA, Aizen MA, Klein AM, Cunningham SA, Harder LD (2011) Global growth and stability of agricultural yield decrease with pollinator dependence. Proc Natl Acad Sci USA 108:5909–5914CrossRefGoogle Scholar
  25. Garibaldi LA, Carvalheiro LG, Leonhardt SD, Aizen MA, Blaauw BR, Isaacs R, Kuhlmann M, Kleijn D, Klein AM, Kremen C, Morandin L, Scheper J, Winfree R (2014) From research to action: enhancing crop yield through wild pollinators. Front Ecol Environ 12:439–447CrossRefGoogle Scholar
  26. Garnett T, Appleby MC, Balmford A, Bateman IJ, Benton TG, Bloomer P, Burlingame B, Dawkins M, Dolan L, Fraser D, Herrero M, Hoffmann I, Smith P, Thornnton PK, Toulmin C, Vermeulen SJ, Godfray HCJ (2013) Sustainable intensification in agriculture: premises and policies. Science 341:33–34CrossRefGoogle Scholar
  27. Goulson D, Hughes W, Derwent L, Ltout J (2002) Colony growth of bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats. Oecologia 130:267–273CrossRefGoogle Scholar
  28. Goulson D, Lepais O, O’Connor S, Osborne JL, Sanderson RA, Cussans J, Goffe L, Darvill B (2010) Effects of land use at the landscape scale on bumblebee nest density and survival. J Appl Ecol 47:1207–1215CrossRefGoogle Scholar
  29. Grab H, Blitzer EJ, Danforth B, Loeb G, Poveda K (2017) Temporally dependent pollinator competition and facilitation with mass flowering crops affects yield in co-blooming crops. Sci Rep 7:45296CrossRefGoogle Scholar
  30. Hadley AS, Betts MG (2012) The effects of landscape fragmentation on pollination dynamics: absence of evidence not evidence of absence. Biol Rev 87:526–544CrossRefGoogle Scholar
  31. Hanley ME, Franco M, Dean CE, Franklin EL, Harris HR, Haynes AG, Rapson SR, Rowse G, Thomas KC, Waterhouse BR, Knight ME (2011) Increased bumblebee abundance along the margins of a mass flowering crop: evidence for pollinator spill-over. Oikos 120:1618–1624CrossRefGoogle Scholar
  32. Heard MS, Carvell C, Carreck NL, Rothery P, Osborne JL, Bourke AFG (2007) Landscape context not patch size determines bumble-bee density on flower mixtures sown for agri-environment schemes. Biol Lett 3:638–641CrossRefGoogle Scholar
  33. Hemberger J, Gratton C (2018) Floral resource pulse decreases bumble bee foraging trip duration in central Wisconsin agroecosystem. Ecol Entomol 43:447–457CrossRefGoogle Scholar
  34. Hoehn P, Tscharntke T, Tylianakis M, Steffan-Dewenter I (2008) Functional group diversity of bee pollinators increases crop yield. Proc R Soc B 275:2283–2291CrossRefGoogle Scholar
  35. Holzschuh A, Dainese M, Gonzalez-Varo JP, Mudri-Stojnic S, Riedinger V, Rundlof M, Scheper J, Wickens JB, Wickens VJ, Bommarco R, Kleijn D, Potts SG, Roberts SPM, Smith HG, Vila M, Vujic A, Steffan-Dewenter I (2016) Mass-flowering crops dilute pollinator abundance in agricultural landscapes across Europe. Ecol Lett 19:1228–1236CrossRefGoogle Scholar
  36. Iverson AL, Marín LE, Ennis KK, Gonthier DJ, Connor-Barrie BT, Remfert JL, Cardinale BJ, Perfecto I (2014) Do polycultures promote win-wins or trade-offs in agricultural ecosystem services? A meta-analysis. J Appl Ecol 51:1593–1602CrossRefGoogle Scholar
  37. Jha S (2013) Bumble bee pollen use and preference across spatial scales in human-altered landscapes. Ecol Entomol 38:570–579CrossRefGoogle Scholar
  38. Jha S, Kremen C (2012) Resource diversity and landscape-level homogeneity drive native bee foraging. Proc Natl Acad Sci 8:555–558Google Scholar
  39. Jha S, Kremen C (2013) Urban land use limits regional bumble bee gene flow. Mol Ecol 22:2483–2495CrossRefGoogle Scholar
  40. Jones O, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resourc 10:551–555CrossRefGoogle Scholar
  41. Kallioniemi E, Åström J, Rusch G, Dahle S, Åström S, Gjershaug J (2017) Local resources, linear elements and mass-flowering crops determine bumble bee occurrences in moderately intensified farmlands. Agr Ecosyst Environ 239:90–100CrossRefGoogle Scholar
  42. Kashian R, Peterson J (2013) Cranberries of Wisconsin—analyzing the economic impact. J Bus Case Stud 9:185–192CrossRefGoogle Scholar
  43. King MJ, Buchmann SL (2003) Floral sonication by bees: Mesosomal vibration by Bombus and Xylocopa, but not Apis (Hymenoptera:Apidae), ejects pollen from poricidal anthers. J Kansas Entomol Soc 76:295–305Google Scholar
  44. Klein AM, Vaissiére B, Cane J, Steffan-Dewenter I, Cunningham S, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc Biol Sci 274:303–313CrossRefGoogle Scholar
  45. Kovacs-Hostyanszki A, Haenke S, Batary P, Jauker B, Baldi A, Tscharntke T, Holzschuh A (2013) Contrasting effects of mass-flowering crops on bee pollination of hedge plants at different spatial and temporal scales. Ecol Appl 23:1938–1946CrossRefGoogle Scholar
  46. Li H, Reynolds JF (1993) A new contagion index to quantify patterns of landscapes. Landscape Ecol 8:155–162CrossRefGoogle Scholar
  47. Lozier JD, Strange JP, Stewart IJ, Cameron SA (2011) Patterns of range-wide genetic variation in six North American bumble bee (Apidae: Bombus) species. Mol Ecol 20:4870–4888CrossRefGoogle Scholar
  48. McGarigal K, Cushman SA, and Ene E (2012) FRAGSTATS v4: spatial pattern analysis program for categorical and continuous maps. University of Massachusetts, Amherst. http://www.umass.edu/landeco/research/fragstats/fragstats.html. Accessed 31 Aug 2017
  49. Nicolson SW, Wright GA (2017) Plant-pollinator interactions and threats to pollination: perspectives from the flower to the landscape. Funct Ecol 31:22–25CrossRefGoogle Scholar
  50. O’Connor S, Park K, Goulson D (2012) Humans versus dogs; a comparison of methods for the detection of bumble bee nests. J Apic Res 51:204–211CrossRefGoogle Scholar
  51. Pebesma E (2018) sp: classes and methods for spatial data. R package version 1.3-1Google Scholar
  52. Pennell MW, CR Miller (2012) capwire: estimates population size from non-invasive sampling. R package version 1.1.4Google Scholar
  53. Pywell RF, Heard MS, Woodcock BA, Hinsley S, Ridding L, Nowakowski M, Bullock JM (2015) Wildlife-friendly farming increases crop yield: evidence for ecological intensification. Proc R Soc B Biol Sci.  https://doi.org/10.1098/rspb.2015.1740 Google Scholar
  54. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  55. Rao S, Strange J (2012) Bumble bee foraging distance and colony density associated with a late season mass flowering crop. Environ Entomol 41:905–915CrossRefGoogle Scholar
  56. Redhead JW, Dreier S, Bourke A, Heard MS, Jordan W, Sumner S, Wang J, Carvell C (2016) Effects of habitat composition and landscape structure on worker foraging distances of five bumble bee species. Ecol Appl 26:726–739CrossRefGoogle Scholar
  57. Riedinger V, Renner M, Rundlöf M, Steffan-Dewenter I, Holzschuh A (2014) Early mass-flowering crops mitigate pollinator dilution in late-flowering crops. Landscape Ecol 29:425–435CrossRefGoogle Scholar
  58. Rundlöf M, Persson AS, Smith HG, Bommarco R (2014) Late-season mass-flowering red clover increases bumble bee queen and male densities. Biol Conserv 172:138–145CrossRefGoogle Scholar
  59. Sardinas H, Kremen C (2015) Pollination services from field-scale agricultural diversification may be context-dependent. Agr Ecosyst Environ 207:17–25CrossRefGoogle Scholar
  60. Spiesman B, Bennett A, Isaacs R, Gratton C (2017) Bumble bee colony growth and reproduction depend on local flower dominance and natural habitat area in the surrounding landscape. Biol Conserv 206:217–223CrossRefGoogle Scholar
  61. Stanley D, Stout J (2014) Pollinator sharing between mass-flowering oilseed rape and co-flowering wild plants: implications for wild plant pollination. Plant Ecol 215:315–325CrossRefGoogle Scholar
  62. Stolle E, Rohde M, Vautrin D, Solignac M, Schmid-Hempel P, Schmid-Hempel R, Moritz RFA (2009) Novel microsatellite DNA loci for Bombus terrestris (Linnaeus, 1758). Mol Ecol Resour 9:1345–1352CrossRefGoogle Scholar
  63. Symonds M, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21CrossRefGoogle Scholar
  64. Tasei JN, Aupinel P (2008) Nutritive value of 15 single pollens and pollen mixes tested on larvae produced by bumblebee workers (Bombus terrestris, Hymenoptera: Apidae). Apidologie (Celle) 39:397–409CrossRefGoogle Scholar
  65. United Nations Food and Agriculture Organization (UNFAO) (2017) Cranberry production in 2016, Crops/Regions/World list/Production Quantity. Corporate Statistical Database (FAOSTAT). Retrieved 18 Oct 2018Google Scholar
  66. United States Department of Agriculture—Farm Service Agency (2013) National Agricultural Imagery Program (NAIP) Digital aerial photography. https://datagateway.nrcs.usda.gov/. Accessed through http://www.wisconsinview.org
  67. Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513Google Scholar
  68. Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979CrossRefGoogle Scholar
  69. Westphal C, Steffan-Dewenter I, Tscharntke T (2006) Foraging trip duration of bumblebees in relation to landscape-wide resource availability. Ecol Entomol 31:389–394CrossRefGoogle Scholar
  70. Williams NM, Regetz J, Kremen C (2012) Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. Ecology 93:1049–1058CrossRefGoogle Scholar
  71. Williams PH, Thorp RW, Richardson LL, Colla SR (2014) An Identification guide: bumble bees of North America. Princeton University Press, PrincetonGoogle Scholar
  72. Wisconsin Department of Natural Resources (2012) Ecological landscapes of Wisconsin. http://dnr.wi.gov/topic/landscapes/. Accessed: April 2014

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Nelson Institute for Environmental StudiesUniversity of WisconsinMadisonUSA
  2. 2.Department of EntomologyUniversity of WisconsinMadisonUSA
  3. 3.USDA-ARS Vegetable Crops Research Unit, Department of HorticultureUniversity of WisconsinMadisonUSA

Personalised recommendations