Landscape Ecology

, Volume 34, Issue 5, pp 967–978 | Cite as

Anthropogenic landscapes support fewer rare bee species

  • Tina HarrisonEmail author
  • Jason Gibbs
  • Rachael Winfree
Research Article



The response of rare species to human land use is poorly known because rarity is difficult to study; however, it is also important because rare species compose most of biodiversity, and are disproportionately vulnerable. Regional bee pollinator faunas have not been assessed for rarity outside of Europe. Therefore, we do not know to what extent anthropogenic landscapes support rare North American bee biodiversity.


We ask how richness and abundance of bee species respond to land use, within quartiles of species defined by their numerical, phenological, and geographical rarity.


We conducted a field study to sample bee communities in forested, agricultural, and urban landscapes replicated across a large spatial extent of the northeastern United States. We used large independent data sets to classify observed bee species according to three forms of rarity: their numerical rarity (low regional frequency in a museum-based data set), phenological rarity (short flight season length) and geographical rarity (small range size).


For all three forms of rarity, we found half as many rare bee species in agricultural landscapes compared to forest. We found half as many phenologically rare species in urban landscapes. Bees that had both shorter flight seasons and smaller range sizes were between one-third and one-half as rich in both types of anthropogenic landscapes, regardless of regional frequency.


Although a minority of rare bee species were found in anthropogenic landscapes, our overall conclusion is that the native vegetation of our region, forest, is critical for supporting rare bee biodiversity.


Rarity Commonness Pollinator Land use Urban Phenology Apoidea 



We thank Sam Droege at the USGS Patuxent Wildlife Research Center in Beltsville, Maryland for identifying 1338 bee specimens of Nomada, and for sharing his data (3500 of the 42,552 specimen records used for defining bee species’ phenology). We also thank members of the Winfree lab for invaluable comments and support throughout this study’s planning, analysis and writing, and helpful comments from the associate editor and two anonymous peer reviewers that improved the final manuscript. This work was supported by a federal Graduate Assistance in Areas of National Need (GAANN) fellowship awarded to TH through the Rutgers University Ecology & Evolution Graduate Program.

Supplementary material

10980_2017_592_MOESM1_ESM.docx (3.1 mb)
Supplementary material 1 (DOCX 3127 kb)


  1. Arduser M (2016) Key to Osmia females known from eastern North America (east of the Great Plains). Accessed 1 Oct 2016
  2. Ascher JS (2006–2017) AMNH BEES species occurrence database. Accessed 1 Nov 2017
  3. Baldock KCR, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Osgathorpe LM, Pott SG, Robertson KM, Scott AV, Stone GN, Vaughan IP, Memmott J (2015) Where is the UK’s pollinator biodiversity? The importance of urban areas for flower-visiting insects. Proc R Soc B 282:20142849Google Scholar
  4. Bartomeus I, Ascher JS, Gibbs J, Danforth BN, Wagner DL, Hedtke SM, Winfree R (2013) Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc Natl Acad Sci 110:4656–4660CrossRefGoogle Scholar
  5. Bates D, Maechler M, Bolker BM, Walker S (2015) lme4: linear mixed-effects models using Eigen and S4. R Packag. version 1.7Google Scholar
  6. Blair RB (2001) Birds and butterflies along urban gradients in two ecoregions of the United States: is urbanization creating a homogeneous fauna? In: Lockwood JL, Mckinney ML (eds) Biotic homogenization. Springer, New York, pp 33–56CrossRefGoogle Scholar
  7. Bouseman JK, LaBerge WE (1979) A revision of the bees of the genus Andrena of the Western Hemisphere. Part IX. Subgenus Melandrena. Trans Am Entomol Soc 104:275–389Google Scholar
  8. Cardillo M, Mace GM, Gittleman JL, Mace GM, Purvis A (2008) The predictability of extinction: biological and external correlates of decline in mammals. Proc R Soc B 275:1441–1448CrossRefGoogle Scholar
  9. Cardoso P, Erwin TL, Borges PAV, New TR (2011) The seven impediments in invertebrate conservation and how to overcome them. Biol Conserv 144:2647–2655CrossRefGoogle Scholar
  10. Cariveau DP, Winfree R (2015) Causes of variation in wild bee responses to anthropogenic drivers. Curr Opin Insect Sci 10:1–6CrossRefGoogle Scholar
  11. Coddington JA, Agnarsson I, Miller JA, Kuntner M, Hormiga G (2009) Undersampling bias: the null hypothesis for singleton species in tropical arthropod surveys. J Anim Ecol 78:573–584CrossRefGoogle Scholar
  12. Coelho BWT (2004) A review of the bee genus Augochlorella (Hymenoptera: Halictidae: Augochlorini). Syst Entomol 29:282–323CrossRefGoogle Scholar
  13. Collen B, Dulvy NK, Gaston KJ, Gärdenfors U, Keith DA, Punt AE, Regan HM, Böhm M, Hedges S, Seddon M, Butchart SHM, Hilton-Taylor C, Hoffmann M, Bachman SP, Akçakaya HR (2016) Clarifying misconceptions of extinction risk assessment with the IUCN Red List. Biol Lett 12:1424–1442CrossRefGoogle Scholar
  14. Davies KF, Margules CR, Lawrence JF (2004) A synergistic effect puts rare, specialized species at greater risk of extinction. Ecology 85:265–271CrossRefGoogle Scholar
  15. Dray S, Legendre P (2008) Testing the species traits-environment relationships: the fourth-corner problem revisited. Ecology 89:3400–3412CrossRefGoogle Scholar
  16. Fowler J (2016) Specialist bees of the northeast: host plants and habitat conservation. Northeast Nat 23:305–320CrossRefGoogle Scholar
  17. Gaston KJ (1996) Species-range-size distributions: patterns, mechanisms and implications. Trends Ecol Evol 11:197–201CrossRefGoogle Scholar
  18. Gibbs J (2011) Revision of the metallic Lasioglossum (Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini). Zootaxa 1–216Google Scholar
  19. Gibbs J, Packer L, Dumesh S, Danforth BN (2013) Revision and reclassification of Lasioglossum (Evylaeus), L. (Hemihalictus) and L. (Sphecodogastra) in eastern North America (Hymenoptera: Apoidea: Halictidae). Zootaxa 3672:1–117CrossRefGoogle Scholar
  20. Godet L, Gaüzere P, Jiguet F, Devictor V (2015) Dissociating several forms of commonness in birds sheds new light on biotic homogenization. Glob Ecol Biogeogr 24:416–426CrossRefGoogle Scholar
  21. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391CrossRefGoogle Scholar
  22. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596CrossRefGoogle Scholar
  23. Hall DM, Camilo GR, Tonietto RK, Ollerton J, Ahrné K, Arduser M, Ascher JS, Baldock KCR, Fowler R, Frankie G, Goulson D, Gunnarsson B, Hanley ME, Jackson JI, Langellotto G, Lowenstein D, Minor ES, Philpott SM, Potts SG, Sirohi MH, Spevak EM, Stone GN, Threlfall CG (2016) The city as a refuge for insect pollinators. Conserv Biol 1:24–29Google Scholar
  24. Harnik PG, Simpson C, Payne JL (2012) Long-term differences in extinction risk among the seven forms of rarity. Proc R Soc B 279:4969–4976CrossRefGoogle Scholar
  25. Horner-Devine MC, Daily GC, Ehrlich PR, Boggs CL (2003) Countryside biogeography of tropical butterflies. Conserv Biol 17:168–177CrossRefGoogle Scholar
  26. Hull PM, Darroch SAF, Erwin DH (2015) Rarity in mass extinctions and the future of ecosystems. Nature 528:345–351CrossRefGoogle Scholar
  27. Knapp S, Kühn I, Bakker JP, Kleyer M, Klotz S, Ozinga WA, Poschold P, Thompson K, Thuiller W, Römermann C (2009) How species traits and affinity to urban land use control large-scale species frequency. Divers Distrib 15:533–546CrossRefGoogle Scholar
  28. Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley R, Packer L, Potts SG, Roulston T, Steffan-Dewenter I, Vázquez DP, Winfree R, Adams L, Crone EE, Greenleaf SS, Keitt TH, Klein A-M, Regetz J, Ricketts TH (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10:299–314CrossRefGoogle Scholar
  29. LaBerge WE (1961) A revision of the bees of the genus Melissodes in North and Central America. Part III (Hymenoptera, Apidae). Univ Kansas Sci Bull 42:283–663CrossRefGoogle Scholar
  30. LaBerge WE (1967) A revision of the bees of the genus Andrena of the Western Hemisphere. Part I. Callandrena (Hymenoptera: Andrenidae). Bull Univ Nebraska State Museum 7:1–316Google Scholar
  31. LaBerge WE (1971) A revision of the bees of the genus Andrena of the Western Hemisphere. Part IV. Scrapteropsis, Xiphandrena and Raphandrena. Trans Am Entomol Soc 97:441–520Google Scholar
  32. LaBerge WE (1973) A revision of the bees of the genus Andrena of the Western Hemisphere. Part VI. Subgenus Trachandrena. Trans Am Entomol Soc 99:235–371Google Scholar
  33. LaBerge WE (1977) A revision of the bees of the genus Andrena of the Western Hemisphere. Part VIII. Subgenera Thysandrena, Dasyandrena, Psammandrena, Rhacandrena, Euandrena, Oxyandrena. Trans Am Entomol Soc 103:1–143Google Scholar
  34. LaBerge WE (1980) A revision of the bees of the genus Andrena of the western hemisphere. Part X. Subgenus Andrena. Trans Am Entomol Soc 106:395–525Google Scholar
  35. LaBerge WE (1986) A revision of the bees of the genus Andrena of the Western Hemisphere. Part XI. Minor subgenera and subgeneric key. Trans Am Entomol Soc 111:440–567Google Scholar
  36. LaBerge WE (1987) A revision of the bees of the genus Andrena of the Western Hemisphere. Part XII. Subgenera Leucandrena, Ptilandrena, Scoliandrena, and Melandrena. Trans Am Entomol Soc 112:191–248Google Scholar
  37. LaBerge WE (1989) A revision of the bees of the genus Andrena of the Western Hemisphere. Part XIII. Subgenera Simandrena and Taeniandrena. Trans Am Entomol Soc 115:1–56Google Scholar
  38. LaBerge WE, Ribble DW (1975) A revision of the bees of the genus Andrena of the Western Hemisphere. Part VII. Subgenus Euandrena. Trans Am Entomol Soc 101:371–446Google Scholar
  39. Larkin LL, Andrus R, Droege S (2016) Andrena. In: Discover life. Accessed 10 Nov 2016
  40. Laverty TM, Harder LD (1988) The bumble bees of eastern Canada. Can Entomol 120:965–967CrossRefGoogle Scholar
  41. Lockwood JLF, Hoopes MF, Marchetti MP (2006) Invasion ecology. Wiley-Blackwell, HobokenGoogle Scholar
  42. Matteson K, Ascher J, Langellotto G (2008) Bee richness and abundance in New York city urban gardens. Ann Entomol Soc Am 101:140–150CrossRefGoogle Scholar
  43. Mayfield MM, Daily GC (2005) Countryside biogeography of neotropical herbaceous and shrubby plants. Ecol Appl 15:423–439CrossRefGoogle Scholar
  44. McGinley RJ (1986) Studies of Halictinae (Apoidea: Halictidae), I: Revision of New World Lasioglossum Curtis. Smithson Contrib Zool 429:1–294CrossRefGoogle Scholar
  45. McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–452CrossRefGoogle Scholar
  46. Mitchell TB (1960) Bees of the Eastern United States: volume I. N C Agric Exp Stn Tech Bull 141:1–538Google Scholar
  47. Mitchell TB (1962) Bees of the Eastern United States: volume II. N C Agric Exp Stn Tech Bull 152:1–557Google Scholar
  48. Motten A (1986) Pollination ecology of the spring wildflower community of a temperate deciduous forest. Ecol Monogr 56:21–42CrossRefGoogle Scholar
  49. Newbold T, Hudson LN, Hill SLL, Contu S, Lysenko I, Senior RA, Börger L, Bennett DJ, Choimes A, Collen B, Day J, De Palma A, Díaz S, Echeverria-Londoño S, Edgar MJ, Feldman A, Garon M, Harrison MLK, Alhusseini T, Ingram DJ, Itescu Y, Kattge J, Kemp V, Kirkpatrick L, Kleyer M, Laginha Pinto Correia D, Martin CD, Meiri S, Novosolov M, Pan Y, Phillips HRP, Purves DW, Robinson A, Simpson J, Tuck SL, Weiher E, White HJ, Ewers RM, Mace GM, Scharlemann JPW, Purvis A (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45–50CrossRefGoogle Scholar
  50. Nickerson C, Ebel R, Borchers A, Carriazo F (2011) Major uses of land in the United States, 2007. United States Dep Agric Econ Inf BullGoogle Scholar
  51. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326CrossRefGoogle Scholar
  52. Omernik JM (1987) Ecoregions of the conterminous United States. Ann Assoc Am Geogr 77:118–125CrossRefGoogle Scholar
  53. Pereira HM, Leadley PW, Proença V, Alkemade R, Scharlemann JPW, Fernandez-Manjarrés JF, Araújo MB, Balvanera P, Biggs R, Cheung WWL, Chini L, Cooper HD, Gilman EL, Guénette S, Hurtt GC, Huntington HP, Mace GM, Oberdorff T, Revenga C, Rodrigues P, Scholes RJ, Sumaila UR, Walpole M (2010) Scenarios for global biodiversity in the 21st century. Science 330:1496–1501CrossRefGoogle Scholar
  54. Pimm SL, Jenkins CN, Abell R, Brooks TM, Gittleman JL, Joppa LN, Raven PH, Roberts CM, Sexton JO (2014) The biodiversity of species and their rates of extinction, distribution, and protection. Science 344:1246752CrossRefGoogle Scholar
  55. Preston FW (1948) The commonness, and rarity, of species. Ecology 29:254–283CrossRefGoogle Scholar
  56. Rabinowitz D (1981) Seven forms of rarity. In: Synge H (ed) The biological aspects of rare plant conservation. Wiley, Chichester, pp 205–217Google Scholar
  57. Rehan SM, Sheffield CS (2011) Morphological and molecular delineation of a new species in the Ceratina dupla species-group (Hymenoptera: Apidae: Xylocopinae) of eastern North America. Zootaxa 2873:35–50CrossRefGoogle Scholar
  58. Ribble DW (1968) Revisions of two subgenera of Andrena: Micrandrena Ashmead and Derandrena, new subgenus (Hymenoptera: Apoidea). Bull Univ Nebraska State Museum 8:237–394Google Scholar
  59. Rudel TK, Coomes OT, Moran E, Achard F, Angelsen A, Xu J, Lambin E (2005) Forest transitions: towards a global understanding of land use change. Glob Environ Chang 15:23–31CrossRefGoogle Scholar
  60. Scheper J, Bommarco R, Holzschuh A, Potts SG, Riedinger V, Roberts SPM, Rundlöf M, Smith HG, Steffan-Dewenter I, Wickens JB, Wickens VJ, Kleijn D (2015) Local and landscape-level floral resources explain effects of wildflower strips on wild bees across four European countries. J Appl Ecol 52:1165–1175CrossRefGoogle Scholar
  61. Schoener TW (1974) The compression hypothesis and temporal resource partitioning. Proc Natl Acad Sci 71:4169–4172CrossRefGoogle Scholar
  62. Scott MC (2006) Winners and losers among stream fishes in relation to land use legacies and urban development in the southeastern US. Biol Conserv 127:301–309CrossRefGoogle Scholar
  63. Stephen WP, Rao S (2005) Unscented Color Traps for Non-Apis Bees (Hymenoptera: Apiformes). Sour J Kansas Entomol Soc 78:373–380CrossRefGoogle Scholar
  64. ter Braak CJF, Cormont A, Dray SP (2012) Improved testing of species traits-environment relationships in the fourth-corner problem. Ecology 93:1525–1526CrossRefGoogle Scholar
  65. Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batáry P, Bengtsson J, Clough Y, Crist TO, Dormann CF, Ewers RM, Fründ J, Holt RD, Holzschuh A, Klein AM, Kleijn D, Kremen C, Landis DA, Laurance W, Lindenmayer D, Scherber C, Sodhi N, Steffan-Dewenter I, Thies C, van der Putten WH, Westphal C (2012) Landscape moderation of biodiversity patterns and processes—eight hypotheses. Biol Rev Camb Philos Soc 87:661–685CrossRefGoogle Scholar
  66. Umaña MN, Zhang C, Cao M, Lin L, Swenson NG (2015) Commonness, rarity, and intraspecific variation in traits and performance in tropical tree seedlings. Ecol Lett 18:1329–1337CrossRefGoogle Scholar
  67. Venables WN, Ripley BD (2002) Modern applied statistics with S. Issues Accuracy Scale, 868Google Scholar
  68. Villéger S, Blanchet S, Beauchard O, Oberdorff T, Brosse S (2011) Homogenization patterns of the world’s freshwater fish faunas. Proc Natl Acad Sci 108:18003–18008CrossRefGoogle Scholar
  69. Westrich P (1996) Habitat requirements of central European bees and the problems of parital habitats. Linn Soc Symp Ser 18:1–6Google Scholar
  70. Winfree R, Bartomeus I, Cariveau DP (2011) Native pollinators in anthropogenic habitats. Annu Rev Ecol Evol Syst 42:1–22CrossRefGoogle Scholar
  71. Winfree R, Griswold T, Kremen C (2007) Effect of human disturbance on bee communities in a forested ecosystem. Conserv Biol 21:213–223CrossRefGoogle Scholar
  72. Zeileis A (2006) Object-oriented computation of sandwich estimators. J Stat Softw 16:1–16CrossRefGoogle Scholar
  73. 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 143:669–676CrossRefGoogle Scholar

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© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Ecology, Evolution, & Natural ResourcesRutgers UniversityNew BrunswickUSA
  2. 2.Department of EntomologyUniversity of ManitobaWinnipegCanada

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