Landscape Ecology

, Volume 31, Issue 10, pp 2459–2469 | Cite as

Modeling local spatial patterns of wild bee diversity in Pennsylvania apple orchards

  • Melanie A. Kammerer
  • David J. Biddinger
  • Neelendra K. Joshi
  • Edwin G. Rajotte
  • David A. Mortensen
Research Article



The positive correlation between landscape area of semi-natural habitat and wild pollinator richness and abundance in agroecosystems has been well studied. However, we lack a deep understanding of local scale floral resource and nest provisioning for wild bees necessary to optimize implementation of pollinator conservation practices.


The primary objective of this study was to use a spatially interactive landscape pollination model (hereafter, the Lonsdorf model) to represent field scale spatial patterns of wild bee abundance and richness within a heterogeneous landscape in the mid-Atlantic USA.


We parameterized the Lonsdorf model with high resolution aerial imagery and insight from a previously published floristic study. To test the Lonsdorf model predictions, field studies were conducted to measure wild bee abundance and species richness in apple orchards as a function of distance from a forest edge.


Field measurements indicated apple pollinator abundance and species richness significantly decreased with increasing distance from the forest edge. The Lonsdorf model pollination service score was highly sensitive to changes in resource provisioning in orchard and non-crop areas, and including resource rich forest and forest edge habitats in the model significantly improved pollination service estimates.


We demonstrated a novel application of the Lonsdorf model at a field scale to predict trends in pollination service provisioning as a factor of local habitat features. With sufficiently detailed inputs, the Lonsdorf model is a promising tool to quantify field scale pollination service deficits, guiding more cost effective habitat supplementation and other conservation efforts.


Forest edge Lonsdorf model Malus domestica Pollination Spatial modeling Wild bees 



We would like to thank Amanda Ritz, Dr. Katie Ellis, Kathy Wholaver, Lot Miller, and Edwin Winzeler at the Penn State University Fruit Research and Extension Center for field and lab work; David & Steve Slaybaugh, Scott Slaybaugh, Eddie Diveley Jr., and Brian Knouse the participating growers in the study; Leo R. Donovall, Sam Droege, and Dr. Jason Gibbs for bee identification; Dr. Ottar Bjornstad for statistical assistance, and Dr. Eric Lonsdorf for suggestions on model implementation, and two anonymous reviewers for very helpful manuscript feedback. This research was funded by the United States Department of Agriculture Specialty Crops Research Initiative (USDA-SCRI) grant PEN04398, USDA-SCRI Coordinated Agricultural Project grant MICL05063, and the State Horticultural Association of Pennsylvania.

Supplementary material

10980_2016_416_MOESM1_ESM.docx (23.1 mb)
Supplementary material 1 (DOCX 23676 kb)


  1. Ascher JS, Pickering J (2013) Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila).
  2. Bartomeus I, Ascher JS, Gibbs J, Danforth BN, Wagner DL, Hedtke SM, Winfree R (2013a) Data from: historical changes in northeastern US bee pollinators related to shared ecological traits. Dryad Digit Repos. doi: 10.5061/dryad.0nj49 Google Scholar
  3. Bartomeus I, Ascher JS, Gibbs J, Danforth BN, Wagner DL, Hedtke SM, Winfree R (2013b) Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc Natl Acad Sci 110:4656–4660CrossRefPubMedPubMedCentralGoogle Scholar
  4. Batáry P, Báldi A, Kleijn D, Tscharntke T (2011) Landscape-moderated biodiversity effects of agri-environmental management: a meta-analysis. Proc R Soc B 278:1894–1902CrossRefPubMedGoogle Scholar
  5. Batáry P, Dicks LV, Kleijn D, Sutherland WJ (2015) The role of agri-environment schemes in conservation and environmental management. Conserv Biol 29:1006–1016CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw. doi: 10.18637/jss.v067.i01 Google Scholar
  7. Blaauw BR, Isaacs R (2014) Flower plantings increase wild bee abundance and the pollination services provided to a pollination-dependent crop. J Appl Ecol 51:890–898CrossRefGoogle Scholar
  8. Blitzer EJ, Gibbs J, Park MG, Danforth BN (2016) Pollination services for apple are dependent on diverse wild bee communities. Agric Ecosyst Environ 221:1–7CrossRefGoogle Scholar
  9. Brosi BJ, Armsworth PR, Daily GC (2008) Optimal design of agricultural landscapes for pollination services. Conserv Lett 1:27–36CrossRefGoogle Scholar
  10. Core Team R (2016) R: A Language and Environment for Statistical Computing. Austria, ViennaGoogle Scholar
  11. Crassweller R (ed) (2012) Pennsylvania Tree Fruit Production Guide. Pennsylvania State University. AGRS-045, 357 p.
  12. Egan JF, Mortensen DA (2012) A comparison of land-sharing and land-sparing strategies for plant richness conservation in agricultural landscapes. Ecol Appl 22:459–471CrossRefPubMedGoogle Scholar
  13. ESRI (2013) ArcMap 10.1. Environmental Systems Resource Institute, Redlands, CAGoogle Scholar
  14. Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder MN, Nielsen A, Sibert J (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249CrossRefGoogle Scholar
  15. Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG, Harder LD, Afik O, Bartomeus I, Benjamin F, Boreux V, Cariveau D, Chacoff NP, Dudenhöffer JH, Freitas BM, Ghazoul J, Greenleaf S, Hipólito J, Holzschuh A, Howlett B, Isaacs R, Javorek SK, Kennedy CM, Krewenka KM, Krishnan S, Mandelik Y, Mayfield MM, Motzke I, Munyuli T, Nault BA, Otieno M, Petersen J, Pisanty G, Potts SG, Rader R, Ricketts TH, Rundlöf M, Seymour CL, Schüepp C, Szentgyörgyi H, Taki H, Tscharntke T, Vergara CH, Viana BF, Wanger TC, Westphal C, Williams N, Klein AM (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611Google Scholar
  16. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596CrossRefPubMedGoogle Scholar
  17. Groff SC, Loftin CS, Drummond F, Bushmann S, McGill B (2016) Parameterization of the InVEST Crop Pollination Model to spatially predict abundance of wild blueberry (Vaccinium angustifolium Aiton) native bee pollinators in Maine, USA. Environ Model Softw 79:1–9CrossRefGoogle Scholar
  18. Joshi NK, Leslie T, Rajotte EG, Kammerer MA, Otieno M, Biddinger DJ (2015) Comparative trapping efficiency to characterize bee abundance, diversity, and community composition in apple orchards. Ann Entomol Soc Am. doi: 10.1093/aesa/sav057 Google Scholar
  19. Joshi NK, Biddinger DJ, Rajotte EG (2011) A survey of apple pollination practices, knowledge and attitudes of fruit growers in Pennsylvania. 10th International Pollination Symposium, Puebla, MexicoGoogle Scholar
  20. Kammerer MA, Biddinger DJ, Rajotte EG, Mortensen DA (2016) Local plant diversity across multiple habitats supports a diverse wild bee community in Pennsylvania apple orchards. Environ Entomol 45:32–38CrossRefPubMedGoogle Scholar
  21. Kleijn D, Baquero RA, Clough Y, Díaz M, De Esteban J, Fernández F, Gabriel D, Herzog F, Holzschuh A, Jöhl R, Knop E, Kruess A, Marshall EJP, Steffan-Dewenter I, Tscharntke T, Verhulst J, West TM, Yela JL (2006) Mixed biodiversity benefits of agri-environment schemes in five European countries. Ecol Lett 9:243–257CrossRefPubMedGoogle Scholar
  22. Klein A-M, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B Biol Sci 274:303–313. doi:  10.1098/rspb.2006.3721 CrossRefGoogle Scholar
  23. Kremen C, M’Gonigle LK (2015) EDITOR’S CHOICE: small-scale restoration in intensive agricultural landscapes supports more specialized and less mobile pollinator species. J Appl Ecol 52:602–610CrossRefGoogle Scholar
  24. Kremen C, Williams NM (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci 99:16812–16816CrossRefPubMedPubMedCentralGoogle Scholar
  25. LaBerge WE (1989) A Revision of the Bees of the Genus Andrena of the Western Hemisphere. Part XIII. Subgenera Simandrena and Taeniandrena. Transactions of the American Entomological Society (1890-) 115:1–56. doi:  10.2307/25078446
  26. Lonsdorf E, Kremen C, Ricketts T, Winfree R, Williams N, Greenleaf S (2009) Modelling pollination services across agricultural landscapes. Ann Bot 103:1589CrossRefPubMedPubMedCentralGoogle Scholar
  27. Mallinger RE, Gratton C (2015) Species richness of wild bees, but not the use of managed honeybees, increases fruit set of a pollinator-dependent crop. J Appl Ecol 52:323–330CrossRefGoogle Scholar
  28. Mandelik Y, Winfree R, Neeson T, Kremen C (2012) Complementary habitat use by wild bees in agro-natural landscapes. Ecol Appl 22:1535–1546CrossRefPubMedGoogle Scholar
  29. Michener CD (2007) The Bees of the World, 2nd edn. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  30. Michener CD, McGinley RJ, Danforth BN (1994) The bee genera of North and Central America (Hymenoptera: Apoidea). Smithsonian Inst Pr, WashingtonGoogle Scholar
  31. Morandin LA, Kremen C (2013) Hedgerow restoration promotes pollinator populations and exports native bees to adjacent fields. Ecol Appl 23:829–839CrossRefPubMedGoogle Scholar
  32. Mortensen DA, Egan JF, Maxwell BD, Ryan MR, Smith RG (2012) Navigating a Critical Juncture for Sustainable Weed Management. Bioscience 62:75–84CrossRefGoogle Scholar
  33. Natural Capital Project (2014) InVEST: Crop Pollination Model. Version 3.1.0.
  34. Olsson O, Bolin A, Smith HG, Lonsdorf EV (2015) Modeling pollinating bee visitation rates in heterogeneous landscapes from foraging theory. Ecol Model 316:133–143CrossRefGoogle Scholar
  35. PAMAP Program, Pennsylvania Department of Conservation and Natural Resources, Bureau of Topographic and Geologic Survey (2007) PAMAP Program- County Mosaics 2007Google Scholar
  36. Park M, Danforth B, Losey J, Biddinger D, Vaughan M, Dollar J, Rajotte E, Agnello A (2015) Wild Pollinators of Eastern Apple Orchards and How to Conserve Them. 2nd edition. Cornell University, Penn State University, and The Xerces Society.
  37. Rands SA, Whitney HM (2010) Effects of pollinator density-dependent preferences on field margin visitations in the midst of agricultural monocultures: a modelling approach. Ecol Model 221:1310–1316CrossRefGoogle Scholar
  38. Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng’ A, Potts SG, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515CrossRefPubMedGoogle Scholar
  39. Roulston TH, Goodell K (2011) The role of resources and risks in regulating wild bee populations. Annu Rev Entomol 56:293–312CrossRefPubMedGoogle Scholar
  40. Sidhu CS (2013) Farm and landscape-level effects on cucurbit pollinators on small farms in a diversified agroecosystem. PhD Thesis. Pennsylvania State UniversityGoogle Scholar
  41. Skaug H, Fournier D, Bolker B, Magnusson A, Nielsen A (2014) glmmADMB: generalized linear mixed models using AD Model BuilderGoogle Scholar
  42. Steffan-Dewenter I, Münzenberg U, Bürger C, Thies C, Tscharntke T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432CrossRefGoogle Scholar
  43. The Pennsylvania State Climatologist (2013) National Weather Service Cooperative Observer (COOP) Program. Accessed 12 Jun 2013
  44. Tuell JK, Isaacs R (2009) Elevated pan traps to monitor bees in flowering crop canopies. Entomol Exp Appl 131:93–98CrossRefGoogle Scholar
  45. Vaughan M, Skinner M (2008) Using Farm Bill Programs for Pollinator Conservation. NRCS National Plant Data Center, The Xerces Society for Invertebrate Conservation, and San Francisco State UniversityGoogle Scholar
  46. Winfree R, Williams NM, Dushoff J, Kremen C (2007) Native bees provide insurance against ongoing honey bee losses. Ecol Lett 10:1105–1113CrossRefPubMedGoogle Scholar
  47. Winfree R, Williams NM, Gaines H, Ascher J, Kremen C (2008) Wild bee pollinators provide the majority of crop visitation across land-use gradients in New Jersey and Pennsylvania, USA. J Appl Ecol 45:793–802CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Melanie A. Kammerer
    • 1
    • 2
  • David J. Biddinger
    • 3
    • 4
  • Neelendra K. Joshi
    • 5
  • Edwin G. Rajotte
    • 4
  • David A. Mortensen
    • 1
    • 2
  1. 1.Intercollege Graduate Degree Program in EcologyThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of Plant ScienceThe Pennsylvania State UniversityUniversity ParkUSA
  3. 3.Fruit Research and Extension CenterThe Pennsylvania State UniversityBiglervilleUSA
  4. 4.Department of EntomologyThe Pennsylvania State UniversityUniversity ParkUSA
  5. 5.Department of EntomologyUniversity of ArkansasFayettevilleUSA

Personalised recommendations