Skip to main content

Advertisement

Log in

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

  • Research Article
  • Published:
Landscape Ecology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aizen MA, Harder LD (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19:915–918

    Article  CAS  PubMed  Google Scholar 

  • Barton K (2017) MuMIn: multi-model inference. R package version 1(40):4

    Google Scholar 

  • Bivand R (2018) spdep: Spatial Dependence: weighting schemes, statistics and models. R package version 0.8-1

  • Blaauw BR, Isaacs R (2014) Flower plantings increase wild bee abundance and the pollination services provided to a pollinator dependent crop. J Appl Ecol 51:890–898

    Article  Google Scholar 

  • Bommarco R, Kleijn D, Potts SG (2013) Ecological intensification: Harnessing ecosystem services for food security. Trends Ecol Evol 28:230–238

    Article  PubMed  Google Scholar 

  • Brosi BJ, Armsworth PR, Daily GC (2008) Optimal design of agricultural landscapes for pollination services. Conserv Lett 1:27–36

    Article  Google Scholar 

  • Broussard M, Rao S, Stephen WP (2011) Native bees, honeybees, and pollination in Oregon cranberries. HortScience 46:885–888

    Article  Google Scholar 

  • Cade B (2015) Model averaging and muddled multimodel inferences. Ecology 96(9):2370–2382

    Article  PubMed  Google Scholar 

  • Cane JH, Schiffhauer D (2003) Dose-response relationships between pollination and fruiting refine pollinator comparisons for cranberry (Vaccinium macrocarpon [Ericaceae]). Am J Bot 90:1425–1432

    Article  PubMed  Google Scholar 

  • 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 121:734–742

    Article  Google Scholar 

  • 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 21:1760–1771

    Article  CAS  PubMed  Google Scholar 

  • Darvill B, Knight M, Goulson D (2004) Use of genetic markers to quantify bumblebee foraging range and nest density. Oikos 107:471–478

    Article  Google Scholar 

  • Diekotter T, Kadoya T, Franziska P, Wolters V, Jauker F (2010) Oilseed rape crops distort plant-pollinator interactions. J Appl Ecol 47:209–214

    Article  Google Scholar 

  • 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):219–226

    Google Scholar 

  • Dramstad WE (1996) Do bumble bees (Hymenoptera: Apidae) really forage close to their nests? J Insect Behav 9:163–182

    Article  Google Scholar 

  • ESRI (2011) ArcGIS desktop: release 10. Environmental Systems Research Institute, Redlands, CA

    Google Scholar 

  • 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 4:89–93

    Article  CAS  PubMed  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • Fahrig L (2017) Ecological responses to habitat fragmentation per se. Annu Rev Ecol Evol Syst 48:1–23

    Article  Google Scholar 

  • Funk R, Schmid-Hempel R, Schmid-Hempel P (2006) Microsatellite loci for Bombus spp. Mol Ecol Notes 6:83–86

    Article  CAS  Google Scholar 

  • Gaines-Day HR, Gratton C (2015) Biotic and abiotic factors contribute to cranberry pollination. J Pollinat Ecol 15:15–22

    Google Scholar 

  • Gaines-Day HR, Gratton C (2016) Crop yield is correlated with honey bee hive density but not in high woodland landscapes. Agr Ecosyst Environ 218:53–57

    Article  Google Scholar 

  • 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 7:2414–2422

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 108:5909–5914

    Article  PubMed  Google Scholar 

  • 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 12:439–447

    Article  Google Scholar 

  • 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 341:33–34

    Article  CAS  PubMed  Google Scholar 

  • Goulson D, Hughes W, Derwent L, Ltout J (2002) Colony growth of bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats. Oecologia 130:267–273

    Article  CAS  PubMed  Google Scholar 

  • 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 47:1207–1215

    Article  Google Scholar 

  • 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 7:45296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hadley AS, Betts MG (2012) The effects of landscape fragmentation on pollination dynamics: absence of evidence not evidence of absence. Biol Rev 87:526–544

    Article  PubMed  Google Scholar 

  • 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 120:1618–1624

    Article  Google Scholar 

  • 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 3:638–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hemberger J, Gratton C (2018) Floral resource pulse decreases bumble bee foraging trip duration in central Wisconsin agroecosystem. Ecol Entomol 43:447–457

    Article  Google Scholar 

  • Hoehn P, Tscharntke T, Tylianakis M, Steffan-Dewenter I (2008) Functional group diversity of bee pollinators increases crop yield. Proc R Soc B 275:2283–2291

    Article  PubMed  Google Scholar 

  • 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 19:1228–1236

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 51:1593–1602

    Article  Google Scholar 

  • Jha S (2013) Bumble bee pollen use and preference across spatial scales in human-altered landscapes. Ecol Entomol 38:570–579

    Article  Google Scholar 

  • Jha S, Kremen C (2012) Resource diversity and landscape-level homogeneity drive native bee foraging. Proc Natl Acad Sci 8:555–558

    Google Scholar 

  • Jha S, Kremen C (2013) Urban land use limits regional bumble bee gene flow. Mol Ecol 22:2483–2495

    Article  PubMed  Google Scholar 

  • Jones O, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resourc 10:551–555

    Article  Google Scholar 

  • 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 239:90–100

    Article  Google Scholar 

  • Kashian R, Peterson J (2013) Cranberries of Wisconsin—analyzing the economic impact. J Bus Case Stud 9:185–192

    Article  Google Scholar 

  • 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 76:295–305

    Google Scholar 

  • 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 274:303–313

    Article  PubMed  Google Scholar 

  • 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 23:1938–1946

    Article  PubMed  Google Scholar 

  • Li H, Reynolds JF (1993) A new contagion index to quantify patterns of landscapes. Landscape Ecol 8:155–162

    Article  Google Scholar 

  • 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 20:4870–4888

    Article  PubMed  Google Scholar 

  • 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

  • Nicolson SW, Wright GA (2017) Plant-pollinator interactions and threats to pollination: perspectives from the flower to the landscape. Funct Ecol 31:22–25

    Article  Google Scholar 

  • 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 51:204–211

    Article  Google Scholar 

  • Pebesma E (2018) sp: classes and methods for spatial data. R package version 1.3-1

  • Pennell MW, CR Miller (2012) capwire: estimates population size from non-invasive sampling. R package version 1.1.4

  • 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

    Article  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Rao S, Strange J (2012) Bumble bee foraging distance and colony density associated with a late season mass flowering crop. Environ Entomol 41:905–915

    Article  Google Scholar 

  • 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 26:726–739

    Article  PubMed  Google Scholar 

  • 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 29:425–435

    Article  Google Scholar 

  • Rundlöf M, Persson AS, Smith HG, Bommarco R (2014) Late-season mass-flowering red clover increases bumble bee queen and male densities. Biol Conserv 172:138–145

    Article  Google Scholar 

  • Sardinas H, Kremen C (2015) Pollination services from field-scale agricultural diversification may be context-dependent. Agr Ecosyst Environ 207:17–25

    Article  Google Scholar 

  • 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 206:217–223

    Article  Google Scholar 

  • Stanley D, Stout J (2014) Pollinator sharing between mass-flowering oilseed rape and co-flowering wild plants: implications for wild plant pollination. Plant Ecol 215:315–325

    Article  Google Scholar 

  • 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 9:1345–1352

    Article  CAS  PubMed  Google Scholar 

  • 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 65:13–21

    Article  Google Scholar 

  • 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) 39:397–409

    Article  CAS  Google Scholar 

  • 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 2018

  • 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

  • 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 10:506–513

    CAS  PubMed  Google Scholar 

  • Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979

    Article  PubMed  PubMed Central  Google Scholar 

  • Westphal C, Steffan-Dewenter I, Tscharntke T (2006) Foraging trip duration of bumblebees in relation to landscape-wide resource availability. Ecol Entomol 31:389–394

    Article  Google Scholar 

  • Williams NM, Regetz J, Kremen C (2012) Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. Ecology 93:1049–1058

    Article  PubMed  Google Scholar 

  • Williams PH, Thorp RW, Richardson LL, Colla SR (2014) An Identification guide: bumble bees of North America. Princeton University Press, Princeton

    Google Scholar 

  • Wisconsin Department of Natural Resources (2012) Ecological landscapes of Wisconsin. http://dnr.wi.gov/topic/landscapes/. Accessed: April 2014

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vera Pfeiffer.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pfeiffer, V., Silbernagel, J., Guédot, C. et al. Woodland and floral richness boost bumble bee density in cranberry resource pulse landscapes. Landscape Ecol 34, 979–996 (2019). https://doi.org/10.1007/s10980-019-00810-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-019-00810-1

Keywords

Navigation