Diverse pollinator communities enhance plant reproductive success

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1748, 2012, Pages 4845-4852

  Albrecht, Matthias ^a,b   Schmid, Bernhard ^a   Hautier, Yann ^a   Müller, Christine B ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b AGROSCOPE RECKENHOLZ TÄNIKON RESEARCH STATION ART   (Switzerland)

Author keywords

Biodiversity ecosystem function relationship; Complementary resource use; Ecosystem services; Plant pollinator interactions; Positive selection effect; Social bees

Indexed keywords

EID: 84868130490     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.1621     Document Type: Article

References (59)

1. Hooper, D. U. et al. 2005 Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3-35. (doi:10.1890/04-0922)
2. Balvanera, P., Pfisterer, A. B., Buchmann, N., He, J.-S., Nakashizuka, T., Raffaelli, D. & Schmid, B. 2006 Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol. Lett. 9, 1146-1156. (doi:10.1111/j.1461-0248.2006.00963.x)
3. Cardinale, B. J., Srivastava, D. S., Duffy, J. E., Wright, J. P., Downing, A. L., Sankaran, M. & Jouseau, C. 2006 Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443, 989-992. (doi:10. 1038/nature05202)
4. Ashman, T.-L. et al. 2004Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85, 2408-2421. (doi:10.1890/03-8024)
5. Kearns, C. A., Inouye, D. W. & Waser, N. M. 1998 Endangered mutualisms: the conservation of plant-pollinator interactions. Annu. Rev. Ecol. Syst. 29, 83-112. (doi:10.1146/annurev.ecolsys.29.1.83)
6. Klein, A. M., Vaissiere, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C. & Tscharntke, T. 2007 Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274, 303-313. (doi:10.1098/rspb.2006.3721)
7. Biesmeijer, J. C. et al. 2006 Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351-354. (doi:10.1126/ science.1127863)
8. Winfree, R., Aguilar, R., Vázquez, D. P., LeBuhn, G. & Aizen, M. A. 2009 A meta-analysis of bees' responses to anthropogenic disturbance. Ecology 90, 2068-2076. (doi:10.1890/08-1245.1)
9. Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O. & Kunin, W. E. 2010 Global pollinator declines: trends, impacts and drivers. TREE 25, 345-353. (doi:10.1016/j.tree.2010.01.007)
10. Kremen, C., Williams, N. M. & Thorp, R. W. 2002 Crop pollination from native bees at risk from agricultural intensification. Proc. Natl Acad. Sci. USA. 99, 16 812-16 816. (doi: 10.1073/pnas.262413599)
11. Steffan-Dewenter, I., Münzenberg, U., Bürger, C., Thies, C. & Tscharntke, T. 2002 Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83, 1421-1432. (doi:10.1890/0012-9658(2002)083 [1421:SDEOLC]2.0.CO;2)
12. Klein, A. M., Steffan-Dewenter, I. & Tscharntke, T. 2003 Fruit set of highland coffee increases with the diversity of pollinating bees. Proc. R. Soc. Lond. B 270, 955-961. (doi: 10.1098/rspb.2002.2306)
13. Albrecht, M., Duelli, P., Muller, C., Kleijn, D. & Schmid, B. 2007The Swiss agri-environment scheme enhancespollinator diversity and plant reproductive success in nearby intensively managed farmland. J. Appl. Ecol. 44, 813-822. (doi:10.1111/j.1365-2664.2007.01306.x)
14. Kremen, C. et al. 2007 Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol. Lett. 10, 299-314. (doi:10.1111/j.1461-0248.2007.01018.x)
15. Winfree, R., Williams, N. M., Dushoff, J. & Kremen, C. 2007 Native bees provide insurance against ongoing honey bee losses. Ecol. Lett. 10, 1105-1113. (doi:10. 1111/j.1461-0248.2007.01110.x)
16. Hoehn, P., Tscharntke, T., Tylianakis, J. M. & Steffan-Dewenter, I. 2008 Functional group diversity of bee pollinators increases crop yield. Proc. R. Soc. B 275, 2283-2291. (doi:10.1098/rspb.2008.0405)
17. Ricketts, T. H. et al. 2008 Landscape effects on crop pollination services: Are there general patterns? Ecol. Lett. 11, 499-515. (doi:10.1111/j.1461-0248.2008.01157.x)
18. 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. (doi:10.1098/rspb.2008.0709)
19. Fontaine, C., Dajoz, I., Meriguet, J. & Loreau, M. 2006 Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities. PloS Biol. 4, 129-135. (doi:10.1371/journal.pbio.0040001)
20. Klein, A. M., Müller, C. B., Hoehn, P. & Kremen, C. 2009 Understanding the role of species richness for crop pollination services. In Biodiversity, ecosystem functioning, and human wellbeing (eds S. Naeem, D. E. Bunker, A. Hector, M. Loreau & C. Perrings), pp. 195-208. New York, NY: Oxford University Press.
21. Blüthgen, N. & Klein, A. M. 2011 Functional complementarity and specialisation: the role of biodiversity in plant-pollinator interactions. Basic Appl. Ecol. 12, 282-291. (doi: 10.1016/j.baae.2010.1011.1001)
22. Paschke, M., Abs, C. & Schmid, B. 2002 Effects of population size and pollen diversity on reproductive success and offspring size in the narrow endemic Cochlearia bavarica (Brassicaceae). Am. J. Bot. 89, 1250-1259. (doi:10.3732/ajb.89.8.1250)
23. Huston, M. A. 1997Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110, 449-460. (doi:10.1007/s004420050180)
24. Tilman, D., Lehman, C. L. & Thomson, K. T. 1997 Plant diversity and ecosystemproductivity: theoretical considerations. Proc. Natl Acad. Sci. USA 94, 1857-1861. (doi:10.1073/pnas.94.5.1857)
25. Loreau, M. & Hector, A. 2001 Partitioning selection and complementarity in biodiversity experiments. Nature 412, 72-76. (doi:10.1038/35083573)
26. Sahli, H. F. & Conner, J. K. 2007 Visitation, effectiveness, and efficiency of 15 genera of visitiors to wild radish, Raphanus raphanistrum (Brassicaceae). Am. J. Bot. 94, 203-209. (doi:10.3732/ajb.94.2.203)
27. Cardinale, B. J., Palmer, M. A. & Collins, S. L. 2002 Species diversity increases ecosystem functioning through interspecific facilitation. Nature 415, 426-429. (doi:10. 1038/415426a)
28. Greenleaf, S. S. & Kremen, C. 2006 Wild bees enhance honey bees' pollination of hybrid sunflower. Proc. Natl Acad. Sci. USA 103, 13 890-13 895. (doi:10.1073/ pnas.0600929103)
29. Loreau, M. 1998 Biodiversity and ecosystem functioning: a mechanistic model. Proc. Natl Acad. Sci. USA 95, 5632-5636. (doi:10.1073/pnas.95.10.5632)
30. Perfectti, F., Gómez, J. M. & Bosch, J. 2009 The functional consequences of diversity in plant-pollinator interactions. Oikos 118, 1430-1440. (doi:10.1111/j. 1600-0706.2009.17491.x)
31. Stone, G. N., 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, 208-221. (doi:10.1046/j.1365-2311.1999.00181.x)
32. Stanton, M., Young, H. J., Ellstrand, N. C. & Clegg, J. M. 1991 Consequences of floral variation for male and female reproduction in experimental populations of wild radish (Raphanus sativus L.). Evolution 45, 268-280. (doi:10.2307/2409662)
33. Karron, J. D., Marshall, D. L. & Oliveras, D. M. 1990 Numbers of sporophytic self-incompatibility alleles in populations of wild radish. Theor. Appl. Genet. 79, 457-460. (doi:10.1007/BF00226152)
34. Conner, J. K. & Rush, S. 1996 Effects of flower size and number on pollinator visitation to wild radish, Raphanus raphanistrum. Oecologia 105, 509-516. (doi:10.1007/ BF00330014)
35. Westrich, P. 1990 Die Wildbienen Baden-Württembergs: Volume 2. Stuttgart, Germany: Ulmer Verlag.
36. Kormann, K. 1988 Schwebfliegen Mitteleuropas. München, Germany: Landsberg.
37. Ashman, T.-L., Galloway, L. F. & Stanton, Ms. L. 1993 Apparent versus effective mating in an experimental population of Raphanus sativus. Oecologia 96, 102-107. (doi:10.1007/BF00318036)
38. R Development Core Team 2009 R: A language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
39. Burnham, K. P. & Anderson, D. R. 2002 Model selection and multimodel inference, 2nd edn. New York, NY: Springer.
40. Grömping, U. 2006 Relative importance for linear regression in R: the package relaimpo. J. Stat. Softw. 17, 1-27.
41. Albrecht, M., Schmid, B., Hautier, Y. & Müller, C. B. Data from: Diverse pollinator communities enhance plant reproductive success. Dryad Digital Repository. See http://dx.doi.org/10.5061/dryad.8gj1c.
42. Gómez, J. M., Bosch, J., Perfectti, F., Fernández, J. & Abdelaziz, M. 2007 Pollinator diversity affects plant reproduction and recruitment: the tradeoffs of generalization. Oecologia 153, 597-605. (doi:10.1007/s00442-007-0758-3)
43. Finke, D. L. & Snyder, W. E. 2008 Niche partitioning increases resource exploitation by diverse communities. Science 321, 1488-1490. (doi:10.1126/science.1160854)
44. Schmid, B., Joshi, J. & Schläpfer, F. 2002 Empirical evidence for biodiversity-ecosystem functioning relationships. In Functional consequences of biodiversity: experimental progress and theoretical extensions (eds A. Kinzig, D. Tilman & P. Pacala), pp. 120-150. Princeton, NJ: Princeton University Press.
45. Srinivasan, U. T., Dunne, J. A., Harte, J. & Martinez, N. D. 2007 Response of complex food webs to realistic extinction sequences. Ecology 88, 671-682. (doi:10. 1890/06-0971)
46. Schmid, B., Balvaneara, P., Cardinale, B. J., Godbold, J., Pfisterer, A. B., Raffaelli, D., Solan, M. & Srivastava, D. S. 2009 Consequences of species loss for ecosystem functioning: meta-analyses of data from biodiversity experiments. In Biodiversity, ecosystem functioning and human wellbeing: an ecological and economic perspective (eds S. Naeem, D. E. Bunker, A. Hector, M. Loreau & C. Perrings), pp. 14-29. New York, NY: Oxford University Press.
47. Jousset, A., Schmid, B., Scheu, S. & Eisenhauer, N. 2011 Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol. Lett. 14, 537-545. (doi:10. 1111/j.1461-0248.2011.01613.x)
48. Dimitrakopoulos, P. G. & Schmid, B. 2004 Positive biodiversity effects increase linearly with biotope space. Ecol. Lett. 7, 574-583. (doi:10.1111/j.1461-0248. 2004.00607.x)
49. Irwin, R. E., Bronstein, J. L., Manson, J. S. & Richardson, L. 2010 Nectar robbing: ecological and evolutionary perspectives. Annu. Rev. Ecol. Evol. Syst. 41, 271-292. (doi:10.1146/annurev.ecolsys.110308.120330)
50. Becker, J., Eisenhauer, N., Scheu, S. & Jousset, A. 2012 Increasing antagonistic interactions cause bacterial communities to collapse at high diversity. Eocl. Lett. 15, 468-474. (doi:101111/j.1461-0248.2012.01759.x)
51. Herrera, C. M. 1990 Daily patterns of pollinator activity, differential pollinating effectiveness, and floral resource availability, in a summer-flowering Mediterranean shrub. Oikos 58, 277-288. (doi:10.2307/3545218)
52. Cardinale, B. J., Ives, A. R. & Inchausti, P. 2004 Effects of species diversity on the primary productivity of ecosystems: extending our spatial and temporal scales of inference. Oikos 104, 437-450. (doi:10.1111/j.0030-1299.2004.13254.x)
53. Tylianakis, J. M., Rand, T. A., Ansgar, K., Klein, A. M., Buchmann, N., Perner, J. & Tscharntke, T. 2008 Resource heterogeneity moderates the biodiversity-function relationship in real world ecosystems. PLoS Biol. 6, e122. (doi:10.1371/journal.pbio.0060122)
54. Stone, G. N. 1994 Activity patterns of females of the solitary bee Anthophora plumipes in relation to temperature, nectar supplies and body-size. Ecol. Entomol. 19, 177-189. (doi:10.1111/j.1365-2311.1994.tb00408.x)
55. Willmer, P. G. & Corbet, S. A. 1981 Temporal and microclimatic partitioning of the floral resources of Justicia aurea amongst a concourse of pollen vectors and nectar robbers. Oecologia 51, 67-78. (doi:10.1007/ BF00344655)
56. Vicens, V. & 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. (doi:10.1603/0046-222X-29.3.413)
57. Free, J. B. 1968 Foraging behaviour of honeybees (Apis mellifera), and bumblebees (Bombus spp) on blackcurrant (Ribes nigrum), raspberry (Rubus idaeus) and strawberry (Fragaria x Ananassa) flowers. J. Appl. Ecol. 5, 157-168. (doi:10.2307/2401280)
58. Gilbert, F. 1985 Diurnal activity patterns in hoverflies (Diptera, Syrphidae). Ecol. Entomol. 10, 385-392. (doi:10.1111/j.1365-2311.1985.tb00736.x)
59. Motten, A. F., Campbell, D. R., Alexander, D. E. & Miller, H. L. 1981 Pollination effectiveness of specialist and generalist visitors of a North-Carolina population of Claytonia virginica. Ecology 62, 1278-1287. (doi:10. 2307/1937292)