, Volume 161, Issue 4, pp 813–823 | Cite as

Reproduction of Amorpha canescens (Fabaceae) and diversity of its bee community in a fragmented landscape

  • Malinda W. Slagle
  • Stephen D. Hendrix
Community Ecology - Original Paper


Loss of insect pollinators due to habitat fragmentation often results in negative effects on plant reproduction, but few studies have simultaneously examined variation in the bee community, site characteristics and plant community characteristics to evaluate their relative effects on plant reproduction in a fragmented habitat. We examined the reproduction of a common tallgrass prairie forb, Amorpha canescens (Fabaceae), in large (>40 ha) and small (<2 ha) prairie remnants in Iowa and Minnesota in relation to the diversity and abundance of its bee visitors, plant population size, and species density of the forb flowering community. We found significant positive effects of the diversity of bees visiting A. canescens on percent fruit set at a site in both years of the study and in 2002 an additional significant positive effect of plant species density. Abundance of bees visiting A. canescens had a significant positive effect on percent fruit set in 2002, but was only marginally significant in 2003. In 2003 but not 2002, the plant species density at the sites had a significant negative effect on the diversity and abundance of bees visiting A. canescens, indicating community-level characteristics can influence the bee community visiting any one species. Site size, a common predictor of plant reproduction in fragmented habitats did not contribute to any models of fruit set and was only marginally related to bee diversity one year. Andrena quintilis, one of the three oligolectic bee species associated with A. canescens, was abundant at all sites, suggesting it has not been significantly affected by fragmentation. Our results show that the diversity of bees visiting A. canescens is important for maintaining fruit set and that bee visitation is still sufficient for at least some fruit set in all populations, suggesting these small remnants act as floral resource oases for bees in landscapes often dominated by agriculture.


Fruit set Bee visitors Habitat fragmentation Prairie Oligolectic bees 



We thank H. Snowgren, K. Gaddis, A. Hill, M. Wendel, and C. Slagle for field and laboratory assistance, K. Cowles for statistical assistance, the Snow Entomological Museum, C. Gienapp, and C. Michener for bee identification assistance, K. Copp for figure preparation, and the Avis Cone Foundation, Center for Global and Regional Environmental Research, the American Museum of Natural History and the Explorer’s Club for financial assistance. These studies comply with current laws in the country in which they were conducted.

Supplementary material

442_2009_1429_MOESM1_ESM.docx (73 kb)
Supplementary material 1 (DOCX 73 kb)


  1. Ågren J (1996) Population size, pollinator limitation, and seed set in the self-incompatible herb Lythrum salicaria. Ecology 77:1779–1790CrossRefGoogle Scholar
  2. Aizen MA, Feinsinger P (1994) Habitat fragmentation, native insect pollinators, and feral honeybees in Argentine chaco serrano. Ecol Appl 4:378–392CrossRefGoogle Scholar
  3. Alexandersson R, Ågren J (1996) Population size, pollinator visitation and fruit production in the deceptive orchid Calypso bulbosa. Oecologia 107:533–540CrossRefGoogle Scholar
  4. Ashman T, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudach MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan M, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421CrossRefGoogle Scholar
  5. Banaszak J (1992) Strategy for conservation of wild bees in an agricultural landscape. Agric Ecosyst Environ 40:179–192CrossRefGoogle Scholar
  6. Banaszak J (1996) Ecological bases of conservation of wild bees. In: Matheson A, Buchmann SL, O’Toole C, Westrich P, Williams IH (eds) The conservation of bees. Academic Press, London, pp 55–62Google Scholar
  7. Becker P, Moure JS, Peralta FJA (1991) More about euglossine bees in Amazonian forest fragments. Biotropica 23:586–591CrossRefGoogle Scholar
  8. Bell JJ (2007) Contrasting patterns of species and functional composition of coral reef sponge assemblages. Mar Ecol Prog Ser 339:73–81CrossRefGoogle Scholar
  9. Bock CE, Jones ZF, Bock JH (2008) The oasis effect: response of birds to exurban development in a southwestern savanna. Ecol Appl 18:1093–1106CrossRefPubMedGoogle Scholar
  10. Brys R, Jacquemyn H, Endels P, van Rossum F, Hermy M, Triest L, De Bruyn L, Blust GDE (2004) Reduced reproductive success in small populations of the self-incompatible Primula vulgaris. J Ecol 92:5–14CrossRefGoogle Scholar
  11. Buchmann SL, Nabhan GP (1996) The forgotten pollinators. Island Press, Washington, DCGoogle Scholar
  12. Cane JH (2001) Habitat fragmentation and native bees: a premature verdict? Conserv Ecol 5:3. [online] URL:
  13. Cane JH (2006) An evaluation of pollination mechanisms for purple prairie-clover, Dalea purpurea (Fabaceae: Amorpheae). Am Midl Nat 156:193–197CrossRefGoogle Scholar
  14. Cane JH, Sipes S (2006) Floral specialization by bees: analytical methods and a revised lexicon for oligolecty. In: Waser NM, Ollerton J (eds) Plant–pollinator interactions: from specialization to generalization. Chicago Press, Chicago, pp 99–122Google Scholar
  15. Cane JH, Minckley RL, Kervin LJ, Roulston TH, Williams NM (2006) Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation. Ecol Appl 16:632–644CrossRefPubMedGoogle Scholar
  16. Cruden RW (1977) Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31:32–46CrossRefGoogle Scholar
  17. Daniel WW (1995) Biostatistics: a foundation for analysis in the health sciences, 6th edn. Wiley, New YorkGoogle Scholar
  18. Davis JD, Debinski DM, Danielson BJ (2007) Local and landscape effects on the butterfly community in fragmented Midwest USA prairie habitats. Landsc Ecol 22:1341–1354CrossRefGoogle Scholar
  19. Davis JD, Hendrix SD, Debinski DM, Hemsley CJ (2008) Butterfly, bee, and forb community composition and cross-taxon incongruence in tallgras prairie fragments. J Insect Conserv 12:69–79CrossRefGoogle Scholar
  20. Draper NR (1998) Applied regression analysis. Wiley, New YorkGoogle Scholar
  21. Dyer JG, Shinn AF (1978) Pollen collected by Calliopsis andreniformis Smith in North America (Hymenoptera: Andrenidae). J Kans Entomol Soc 51:787–795Google Scholar
  22. Freund R, Littell RC (1986) SAS system for regression. SAS Institute, CaryGoogle Scholar
  23. Gamfeldt L, Hillebrand H, Jonsson PR (2008) Multiple functions increase the importance of biodiversity for overall ecosystem functioning. Ecology 89:1223–1231CrossRefPubMedGoogle Scholar
  24. Glass WD (1981) The importance of refuge size in preserving species of prairie legumes, goldenrods, and milkweeds. M.Sc. thesis. University of Illinois at Chicago Circle, ChicagoGoogle Scholar
  25. Goulson D, Darvill B (2004) Niche overlap and diet breadth in bumblebees; are rare species more specialized in their choice of flowers? Apidologie 35:55–63CrossRefGoogle Scholar
  26. Greenleaf SS, Kremen C (2006) Wild bee species increase tomato production and respond differently to surrounding land use in northern California. Biol Conserv 133:81–87CrossRefGoogle Scholar
  27. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596CrossRefPubMedGoogle Scholar
  28. Gross CL, Bartier FV, Mulligan DR (2003) Floral structure, breeding system and fruit-set in the threatened sub-shrub Tetratheca juncea Smith (Tremandraceae). Ann Bot 92:771–777CrossRefPubMedGoogle Scholar
  29. Hayes J (2007) Florida workshop discusses colony collapse disorder. Am Bee J 147:295–303Google Scholar
  30. Heithaus (1974) The role of plant–pollinator interactions in determining community structure. Ann Mo Bot Gard 61:675–691CrossRefGoogle Scholar
  31. Hendrix SD (1994) Effects of population size on fertilization, seed production, and seed predation in two prairie legumes. In: Wickett RG, Lewis PD, Woodliffe A, Pratt P (eds) Proceedings of the 13th North American Prairie Conference, Department of Parks and Recreation, Windsor, pp 115–121Google Scholar
  32. Hendrix SD, Kyhl JF (2000) Population size and reproduction in Phlox pilosa. Conserv Biol 14:304–313CrossRefGoogle Scholar
  33. Heschel MS, Paige KN (1995) Inbreeding depression, environmental stress, and population size variation in scarlet gilia (Ipomopsis aggregata). Conserv Biol 9:126–133CrossRefGoogle Scholar
  34. Hill AF (2005) Diversity, abundance, and similarity of floral resources for pollinators in tallgrass prairie fragments. M.Sc. thesis. University of Iowa, Iowa CityGoogle Scholar
  35. Hurd PD Jr (1979) Superfamily Apoidea. In: Krombein KV, Hurd PDJ, Smith DR, Burks BD (eds) Catalog of Hymenoptera in North America north of Mexico, 1st edn. Smithsonian Institute Press, Washington, DCGoogle Scholar
  36. Institute SAS (2001) SAS software: changes and enhancements through release 8.2. SAS Institute, CaryGoogle Scholar
  37. Jennersten O (1988) Pollination in Dianthus deltoides (Caryophyllaceae)—effects of habitat fragmentation on visitation and seed set. Conserv Biol 2:359–366CrossRefGoogle Scholar
  38. Klein AM, Steffan-Dewenter I, Tscharntke T (2003) Fruit set of highland coffee increases with the diversity of pollinating bees. Proc R Soc Lond B Biol Sci 270:955–961CrossRefGoogle Scholar
  39. Klein AM, Cunningham SA, Bos M, Steffan-Dewenter I (2008) Advances in pollination ecology from tropical plantation crops. Ecology 89:935–943CrossRefPubMedGoogle Scholar
  40. Kremen C, Williams NM, Bugg RL, Fay JP, Thorp RW (2004) The area requirements of an ecosystem service: crop pollination by native bee communities in California. Ecol Lett 7:1109–1119CrossRefGoogle Scholar
  41. Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley R, Packer L, Potts SG, Roulston T, Steffan-Dewenter I, Vazquez DP, Winfree R, Adams L, Crone EE, Greenleaf SS, Keitt TH, Klein AM, 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 10:299–314CrossRefPubMedGoogle Scholar
  42. LaBerge W (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
  43. Larsen TH, Williams NM, Kremen C (2005) Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecol Lett 8:538–547CrossRefGoogle Scholar
  44. Leach MK, Givnish TJ (1996) Ecological determinants of species loss in remnant prairies. Science 273:1555–1558CrossRefGoogle Scholar
  45. Lewis CK (1999) The effects of habitat fragmentation on Amorpha canescens, a prairie forb, and its associated herbivores. M.Sc. thesis. University of Iowa, Iowa CityGoogle Scholar
  46. Magurran AE (2004) Measuring biological diversity. Blackwell Scientific, MaldenGoogle Scholar
  47. Matsumura C, Washitani I (2000) Effects of population size and pollinator limitation on seed-set of Primula sieboldii populations in a fragmented landscape. Ecol Res 15:307–322CrossRefGoogle Scholar
  48. McGregor RL, Barkley TM, Brooks RE, Schofield EK (1986) Flora of the great plains. University of Kansas Press, LawrenceGoogle Scholar
  49. Michener CD (2000) The bees of the world. Johns Hopkins University Press, BaltimoreGoogle Scholar
  50. Michener CD, McGinley RJ, Danforth BN (1994) The bee genera of North and Central America (Hymenoptera: Apoidea). Smithsonian Institution Press, Washington, DCGoogle Scholar
  51. Minckley RL, Roulston TH (2006) Incidental mutualisms and pollen specialization among bees. Oligolecty. In: Waser NM, Ollerton J (eds) Plant–pollinator interactions: from specialization to generalization. Chicago Press, Chicago, pp 69–98Google Scholar
  52. Mitchell TB (1960) Bees of the eastern United States, vol I. The North Carolina Agricultural Experimental Station, RaleighGoogle Scholar
  53. Mitchell TB (1962) Bees of the eastern United States, vol II. The North Carolina Agricultural Experiment Station, RaleighGoogle Scholar
  54. Molano-Flores B, Hendrix SD (1999) The effects of population size and density on the reproductive output of Anemone canadensis L. (Ranunculaceae). Int J Plant Sci 160:759–766CrossRefGoogle Scholar
  55. Morgan JW (1999) Effects of population size on seed production and germinability in an endangered, fragmented grassland plant. Conserv Biol 13:266–273CrossRefGoogle Scholar
  56. Norton C (2007) Colony collapse disorder investigated by US bee researchers. Am Bee J 147:199–202Google Scholar
  57. Packer L, Zayed A, Grixti JC, Ruz L, Owen RE, Vivallo F, Toro H (2005) Conservation genetics of potentially endangered mutualisms: reduced levels of genetic variation in specialist versus generalist bees. Conserv Biol 19:195–202CrossRefGoogle Scholar
  58. Parrish JAD, Bazzaz FA (1979) Difference in pollination niche relationships in early and late successional communities. Ecology 60:597–610CrossRefGoogle Scholar
  59. Potts SG, Vulliamy B, Dafni A, Ne’eman G, Willmer P (2003) Linking bees and flowers: how do floral communities structure pollinator communities? Ecology 84:2628–2642CrossRefGoogle Scholar
  60. Powell AH, Powell GVN (1987) Population dynamics of male euglossine bees in Amazonian forest fragments. Biotropica 19:176–179CrossRefGoogle Scholar
  61. Reed C (1995) Species richness of insects on prairie flowers in southeastern Minnesota. In: Hartnett DC (ed) Proceedings of the 14th North America Prairie Conference: Prairie Biodiversity. Kansas State University, Manhattan, pp 103–115Google Scholar
  62. Resetarits WJ, Chalcraft DR (2007) Functional diversity within a morphologically conservative genus of predators: implications for functional equivalence and redundancy in ecological communities. Funct Ecol 21:793–804CrossRefGoogle Scholar
  63. Richards CM, Church S, McCauley DE (1999) The influence of population size and isolation on gene flow by pollen in Silene alba. Evolution 53:63–73CrossRefGoogle Scholar
  64. Robertson C (1928) Flowers and insects. Lists of visitors to four hundred and fifty-three flowers. Science Press, LancasterGoogle Scholar
  65. Roubik DW (2001) Ups and downs of pollinator populations: when is there a decline? Conserv Ecol 5:2 [online] URL:
  66. Steffan-Dewenter I, Tscharntke T (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121:432–440CrossRefGoogle Scholar
  67. Steinauer EM, Collins SL (1996) Prairie ecology: the tallgrass prairie. In: Samson FB, Knopf FL (eds) Prairie conservation: preserving North America’s most endangered ecosystem. Island Press, Washington, DC, pp 39–52Google Scholar
  68. Stephen WP (1954) A revision of the bee genus Colletes in America north of Mexico. Univ Kans Bull 36:149–527Google Scholar
  69. Stone GN, Gilbert F, Willmer P, Potts S, Semida F, Zalat S (1999) Windows of opportunity and the temporal structuring of foraging activity in a desert solitary bee. Ecol Entomol 24:208–221CrossRefGoogle Scholar
  70. Swink F, Wilhelm G (1994) Plants of the Chicago region. Indiana Academy of Science, IndianapolisGoogle Scholar
  71. Tepedino V, Stanton N (1981) Diversity and competition in bee–plant communities on short-grass prairie. Oikos 36:35–44CrossRefGoogle Scholar
  72. Towne EG, Knapp AK (1996) Biomass and density responses in tallgrass prairie legumes to annual fire and topographic position. Am J Bot 83:175–179CrossRefGoogle Scholar
  73. Tscharntke T, Gathmann A, Steffan-Dewenter I (1998) Bioindication using trap-nesting bees and wasps and their natural enemies: community structure and interactions. J Appl Ecol 35:708–719Google Scholar
  74. Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060CrossRefGoogle Scholar
  75. Weaver J (1954) North American prairie. Johnsen, LincolnGoogle Scholar
  76. Weaver JE, Fitzpatrick TJ (1934) The prairie. Ecol Monogr 4:109–295CrossRefGoogle Scholar
  77. Williams NM, Minckley RL, Silveira FA (2001) Variation in native bee faunas and its implications for detecting community changes. Conserv Ecol 5:7. [online] URL: Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of BiologyUniversity of IowaIowa CityUSA
  2. 2.Litzsinger Road Ecology CenterMissouri Botanical GardenSaint LouisUSA

Personalised recommendations