Bee species diversity enhances productivity and stability in a perennial crop

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Rogers, Shelley R ^a   Tarpy, David R ^a   Burrack, Hannah J ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APIS MELLIFERA; ARTICLE; BEE; CROP PRODUCTION; FRUIT; HABROPODA LABORIOSA; NONHUMAN; PERENNIAL PLANT; PLANT SEED; POLLINATION; POLLINATOR; POPULATION ABUNDANCE; SPECIES DIVERSITY; SPECIES RICHNESS; UNITED STATES; WILD ANIMAL; ANIMAL; BIODIVERSITY; BLUEBERRY; ENVIRONMENT; GENETICS; PHYSIOLOGY; SPECIES DIFFERENCE; STATISTICAL MODEL;

ANIMALS; BEES; BIODIVERSITY; BLUEBERRY PLANT; ENVIRONMENT; LINEAR MODELS; NORTH CAROLINA; POLLINATION; SPECIES SPECIFICITY;

EID: 84901218224     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097307     Document Type: Article

References (62)

1. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, et al. (2001) Diversity and productivity in a long-term grassland experiment. Science 294: 843-845. (Pubitemid 33032100)
2. Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, et al. (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443: 989-992. (Pubitemid 44646175)
3. Duffy JE, Cardinale BJ, France KE, McIntyre PB, Thebault E, et al. (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol Lett 10: 522-538. (Pubitemid 46718935)
4. Ebeling A, Klein A, Tscharntke T (2011) Plant-flower visitor interaction webs: temporal stability and pollinator specialization increases along an experimental plant diversity gradient. Basic Appl Ecol 12: 300-309.
5. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, et al. (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75: 3-35. (Pubitemid 40301269)
6. Balvanera P, Pfisterer AB, Buchmann N, He J, Nakashizuka T, et al. (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9: 1146-1156. (Pubitemid 44403808)
7. Haddad NM, Crutsinger GM, Gross K, Haarstad J, Tilman D (2011) Plant diversity and the stability of foodwebs. Ecol Lett 14: 42-46.
8. Klein A, Steffan-Dewenter I, Tscharntke T (2003) Fruit set of highland coffee increases with the diversity of pollinating bees. Proc R Soc B 270: 955-961. (Pubitemid 36561032)
9. Hoehn P, Tscharntke T, Tylianakis JM, Steffan-Dewenter I (2008) Functional group diversity of bee pollinators increases crop yield. Proc R Soc B 275: 2283-2291.
10. Allen-Wardell G, Bernhardt P, Bitner R, Burquez A, Buchmann S, et al. (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conserv Biol 12: 8-17. (Pubitemid 28153802)
11. Winfree R, Williams NM, Dushoff J, Kremen C (2007) Native bees provide insurance against ongoing honey bee losses. Ecol Lett 10: 1105-1113. (Pubitemid 47512357)
12. Britain C, Williams N, Kremen C, Klein AM (2013) Synergistic effects of non-Apis bees and honey bees for pollination services. Proc R Soc B 280: 20122767.
13. Greenleaf SS, Kremen C (2006) Wild bees enhance honey bees' pollination of hybrid sunflower. Proc Natl Acad Sci USA 103: 13890-13895. (Pubitemid 44414003)
14. Blüthgen N, Klein A (2011) Functional complementarity and specialisation: the role of biodiversity in plant-pollinator interactions. Basic Appl Ecol 12: 282-291.
15. Chagnon M, Gingras J, DeOliveira D (1993) Complementary aspects of strawberry pollination by honey and indigenous bees (Hymenoptera). J Econ Entomol 86: 416-420.
16. Rogers SR, Tarpy DR, Burrack HJ (2013) Multiple criteria for evaluating pollinator performance in highbush blueberry agroecosystems. Environ Entomol 42: 1201-1209.
17. Naeem S (1998) Species redundancy and ecosystem reliability. Conserv Biol 12: 39-45.
18. Elmqvist T, Folke C, Nystrom M, Peterson G, Bengtsson J, et al. (2003) Response diversity, ecosystem change, and resilience. Front Ecol Environ 1: 488-494.
19. Michener CD (1974) The social behavior of the bees: A comparative study. Cambridge, MA: Belknap Press. 404 p.
20. Tuell JK, Isaacs R (2010) Weather during bloom affects pollination and yield of highbush blueberry. J Econ Entomol 103: 557-562.
21. Williams NM, Crone EE, Roulston TH, Minckley RL, Packer L, et al. (2010) Ecological and life-history traits predict bee species responses to environmental disturbances. Biol Conserv 143: 2280-2291.
22. Winfree R, Kremen C (2009) Are ecosystem services stabilized by differences among species? A test using crop pollination. Proc R Soc B 276: 229-237.
23. Cariveau DP, Williams NM, Benjamin FE, Winfree R (2013) Response diversity to land use occurs but does not consistently stabilize ecosystem services provided by native pollinators. Ecol Lett 16: 903-911.
24. Inouye D (1978) Resource partitioning in bumblebees - experimental studies of foraging behavior. Ecology 59: 672-678.
25. Lichtenberg EM, Imperatriz-Fonseca VL, Nieh JC (2010) Behavioral suites mediate group-level foraging dynamics in communities of tropical stingless bees. Insectes Sociaux 57: 105-113.
26. Makino T, Sakai S (2005) Does interaction between bumblebees (Bombus ignitus) reduce their foraging area?: bee-removal experiments in a net cage. Behav Ecol Sociobiol 57: 617-622. (Pubitemid 40554658)
27. Morse D (1982) Foraging relationships within a guild of bumble bees. Insectes Sociaux 29: 445-454.
28. Pinkus-Rendon M, Parra-Tabla V, Melendez-Ramirez V (2005) Floral resource use and interactions between Apis mellifera and native bees in cucurbit crops in Yucatan, Mexico. Can Entomol 137: 441-449. (Pubitemid 41617296)
29. Rogers SR, Cajamarca P, Tarpy DR, Burrack HJ (2013) Honey bees and bumble bees respond differently to inter- and intra-specific encounters. Apidologie 44: 621-629.
30. Adamson NL (2011) An assessment of non-Apis bees as fruit and vegetable crop pollinators in southwest Virginia. PhD thesis, Virginia Polytechnic Institute and State University, Blacksburg, VA.
31. Cane J, Payne J (1993) Regional, annual, and seasonal-variation in pollinator guilds- intrinsic traits of bees (Hymenoptera, Apoidea) underlie their patterns of abundance at Vaccinium ashei (Ericaceae). Ann Entomol Soc Am 86: 577-588.
32. MacKenzie K, Eickwort G (1996) Diversity and abundance of bees (Hymenoptera: Apoidea) foraging on highbush blueberry (Vaccinium corymbosum L) in central New York. J Kans Entomol Soc 69: 185-194. (Pubitemid 28149121)
33. MacKenzie K, Winston M (1984) Diversity and abundance of native bee pollinators on berry crops and natural vegetation in the Lower Fraser Valley, British Columbia. Can Entomol 116: 965-974.
34. Ratti CM, Higo HA, Griswold TL, Winston ML (2008) Bumble bees influence berry size in commercial Vaccinium spp. cultivation in British Columbia. Can Entomol 140: 348-363. (Pubitemid 351968078)
35. Tuell JK, Ascher JS, Isaacs R (2009) Wild bees (Hymenoptera: Apoidea: Anthophila) of the Michigan highbush blueberry agroecosystem. Ann Entomol Soc Am 102: 275-287.
36. Dogterom MH, Winston ML, Mukai A (2000) Effect of pollen load size and source (self, outcross) on seed and fruit production in highbush blueberry cv. 'Bluecrop' (Vaccinium corymbosum; Ericaceae). Am J Bot 87: 1584-1591.
37. Huang YH, Lang GA, Johnson CE, Sundberg MD (1997) Influences of crossand self-pollination on peroxidase activities, isozymes, and histological localization during 'Sharpblue' blueberry fruit development. J Am Soc Hortic Sci 122: 616-624. (Pubitemid 27383821)
38. Delaplane KS, Mayer DF (2000) Crop pollination by bees. Wallingford: CABI. 344 p.
39. Inouye DW (1980) The terminology of floral larceny. Ecology 61: 1251-1253.
40. Droege S (2010) The very handy manual: how to catch and identify bees and manage a collection. USGS Native Bee Inventory and Monitoring Lab, Beltsville, MD.
41. Tuell JK, Isaacs R (2009) Elevated pan traps to monitor bees in flowering crop canopies. Entomol Exp Appl 131: 93-98.
42. Droege S, Tepedino VJ, Lebuhn G, Link W, Minckley RL, et al. (2010) Spatial patterns of bee captures in North American bowl trapping surveys. Insect Conserv Divers 3: 15-23.
43. Michener CD, McGinley RJ, Danforth BN (1994) The bee genera of North and Central America (Hymenoptera: Apoidea). Washington, DC: Smithsonian Institution Press. 209 p.
44. Mitchell TB (1960) Bees of the eastern United States, I. North Carolina Agricultural Experiment Station Technical bulletin 141: 1-538.
45. Mitchell TB (1962) Bees of the eastern United States, II. North Carolina Agricultural Experiment Station Technical bulletin 152: 1-557.
46. Bursac Z, Gauss CH, Williams DK, Hosmer D (2008) Purposeful selection of variables in logistic regression. Source Code Biol Med 3: 17-25.
47. US Department of Agriculture Economic Research Service (2012) U.S. Blueberry Industry. Available: http://usda.mannlib.cornell.edu/MannUsda/ viewDocumentInfo.do?documentID=1765. Accessed 2013 April 10.
48. Mainland CM (2012) Berry evaluations in 2011. Proc NC Blueberry Counc 46: 26-40.
49. Lonsdorf E, Kremen C, Ricketts T, Winfree R, Williams N, et al. (2009) Modelling pollination services across agricultural landscapes. Ann Bot 103: 1589-1600.
50. Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, et al. (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14: 1062-1072.
51. Cane J, Payne J (1988) Foraging ecology of the bee Habropoda laboriosa (Hymenoptera, Anthophoridae), an oligolege of blueberries (Ericaceae, Vaccinium) in the southeastern United States. Ann Entomol Soc Am 81: 419-427.
52. Cane JH (1997) Lifetime monetary value of individual pollinators: the bee Habropoda laboriosa at rabbiteye blueberry (Vaccinium ashei Reade). Proc Sixth Int Symp Vaccinium Cult 446: 67-70.
53. Pascarella JB (2007) Foraging patterns of the southeastern blueberry bee Habropoda laboriosa (Apidae, Hymenoptera): implications for understanding oligolecty. J Apic Res 46: 19-27.
54. Loose JL, Drummond FA, Stubbs C, Woods S, Hoffmann S (2005) Conservation and management of native bees in cranberry. Maine Agricultural and Forest Experiment Station Technical bulletin 191: 1-27.
55. Stubbs CS, Jacobson HA, Osgood EA, Drummond FA (1992) Alternative forage plants for native (wild) bees associated with lowbush blueberry, Vaccinium spp., in Maine. Maine Agricultural Experiment Station Technical Bulletin 148: 1-54.
56. Sheffield C, Kevan P, Smith R, Rigby S, Rogers R (2003) Bee species of Nova Scotia, Canada, with new records and notes on bionomics and floral relations (Hymenoptera: Apoidea). J Kans Entomol Soc 76: 357-384. (Pubitemid 36599914)
57. Westphal C, Bommarco R, Carre G, Lamborn E, Morison N, et al. (2008) Measuring bee diversity in different European habitats and biogeographical regions. Ecol Monogr 78: 653-671.
58. Cane J, Minckley R, Kervin L (2000) Sampling bees (Hymenoptera: Apiformes) for pollinator community studies: pitfalls of pan-trapping. J Kans Entomol Soc 73: 225-231. (Pubitemid 32679924)
59. Roulston TH, Smith SA, Brewster AL (2007) A comparison of pan trap and intensive net sampling techniques for documenting a bee (Hymenoptera: Apiformes) fauna. J Kans Entomol Soc 80: 179-181. (Pubitemid 46851501)
60. Vicens N, Bosch J (2000) Weather-dependent pollinator activity in an apple orchard, with special reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae). Environ Entomol 29: 413-420. (Pubitemid 30608974)
61. Sanchez-Lafuente AM, Rodriguez-Girones MA, Parra R (2012) Interaction frequency and per-interaction effects as predictors of total effects in plant-pollinator mutualisms: a case study with the self-incompatible herb Linaria lilacina. Oecologia 168: 153-165.
62. Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, et al. (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundanace. Science 339: 1608-1611.