Warming, CO2, and nitrogen deposition interactively affect a plant-pollinator mutualism

Ecology Letters

Volumn 15, Issue 3, 2012, Pages 227-234

  Hoover, Shelley E R ^a   Ladley, Jenny J ^a   Shchepetkina, Anastasia A ^a   Tisch, Maggie ^a   Gieseg, Steven P ^a   Tylianakis, Jason M ^a  

^a UNIVERSITY OF CANTERBURY   (New Zealand)

Author keywords

Bombus; Bottom up; Carbon dioxide; Cucurbita; Ecosystem service; Global change; Global warming; Higher order effects; Pollination; Species interactions; Temperature

Indexed keywords

APOIDEA; BOMBUS (GENUS); CUCURBITA;

AMINO ACID; CARBON DIOXIDE; NITROGEN;

ANIMAL; ARTICLE; BEE; CHEMISTRY; ECOSYSTEM; FLOWER; GREENHOUSE EFFECT; GROWTH, DEVELOPMENT AND AGING; NECTAR; PHYSIOLOGY; PLANT PHYSIOLOGY; POLLINATION; SQUASH; SURVIVAL RATE;

AMINO ACIDS; ANIMALS; BEES; CARBON DIOXIDE; CUCURBITA; ECOSYSTEM; FLOWERS; GLOBAL WARMING; NITROGEN; PLANT NECTAR; PLANT PHYSIOLOGICAL PROCESSES; POLLINATION; SURVIVAL RATE;

EID: 84856676899     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/j.1461-0248.2011.01729.x     Document Type: Article

References (50)

1. Aguilar, R., Ashworth, L., Galetto, L. & Aizen, M.A. (2006). Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol. Lett., 9, 968-980.
2. Aizen, M., Morales, C. & Morales, J. (2008). Invasive mutualists erode native pollination webs. PLoS Biol., 6, e31.
3. Baayen, R. (2010). languageR: data sets and functions with "Analyzing Linguistic Data: a practical introduction to statistics". R package version 1.0.
4. Baker, H.G. & Baker, I. (1977). Intraspecific constancy of floral nectar amino-acid complements. Bot. Gaz., 138, 183-191.
5. Baker, H. & Baker, I. (1983). Floral nectar sugar constituents in relation to pollinator type. In: Handbook of Experimental Pollination Biology (eds Jones, C. & Little, R.). Van Nostrand Reinhold New York, USA, pp. 117-141.
6. Baker, H.G. & Baker, I. (1986). The occurrence and significance of amino-acids in floral nectar. Plant Syst. Evol., 151, 175-186.
7. Barker, R.J. & Lehner, Y. (1974). Acceptance and sustenance value of naturally occurring sugars fed to newly emerged adult workers of honey bees (Apis mellifera L). J. Exp. Zool., 187, 277-285.
8. Bates, D. & Maechler, M. (2009). lme4: linear mixed-effects models using S4 classes. R package version 0.999375-32.
9. Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemuller, R., Edwards, M., Peeters, T. et al. (2006). Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science, 313, 351-354.
10. Brittain, C.A., Vighi, M., Bommarco, R., Settele, J. & Potts, S.G. (2010). Impacts of a pesticide on pollinator species richness at different spatial scales. Basic Appl. Ecol., 11, 106-115.
11. Burkle, L.A. & Irwin, R.E. (2009a). The effects of nutrient addition on floral characters and pollination in two subalpine plants, Ipomopsis aggregata and Linum lewisii. Plant Ecol., 203, 83-98.
12. Burkle, L.A. & Irwin, R. (2009b). The importance of interannual variation and bottom-up nitrogen enrichment for plant-pollinator networks. Oikos, 118, 1816-1829.
13. Dag, A. & Eisikowitch, D. (2000). The effect of carbon dioxide enrichment on nectar production in melons under greenhouse conditions. J. Apic. Res., 39, 88-89.
14. Dray, S. & Dufour, A. (2007). The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw., 22, 1-20.
15. Erhardt, A. & Rusterholz, H.P. (1998). Do Peacock butterflies (Inachis io L.) detect and prefer nectar amino acids and other nitrogenous compounds? Oecologia, 117, 536-542.
16. Gallai, N., Salles, J.-M., Settele, J. & Vaissière, B.E. (2009). Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ., 68, 810-821.
17. Gardener, M.C. & Gillman, M.P. (2001). The effects of soil fertilizer on amino acids in the floral nectar of corncockle, Agrostemma githago (Caryophyllaceae). Oikos, 92, 101-106.
18. Gardener, M.C. & Gillman, M.P. (2002). The taste of nectar - a neglected area of pollination ecology. Oikos, 98, 552-557.
19. Goulson, D. (2003). Bumblebees: Their Behaviour and Ecology. Oxford University Press, Oxford, UK.
20. Goulson, D., Lye, G.C. & Darvill, B. (2008). Decline and conservation of bumble bees. Annu. Rev. Entomol., 53, 191-208.
21. Hegland, S.J., Nielsen, A., Lazaro, A., Bjerknes, A.L. & Totland, O. (2009). How does climate warming affect plant-pollinator interactions? Ecol. Lett., 12, 184-195.
22. Hoehn, P., Tscharntke, T., Tylianakis, J.M. & Steffan-Dewenter, I. (2008). Functional group diversity of bee pollinators increases crop yield. Proc. R. Soc. B-Biol. Sci., 275, 2283-2291.
23. Inouye, D.W. & Waller, G.D. (1984). Responses of honeybees (Apis mellifera) to amino acid solutions mimicking nectars. Ecology, 65, 618-625.
24. Jablonski, L.M., Wang, X.Z. & Curtis, P.S. (2002). Plant reproduction under elevated CO2 conditions: a meta-analysis of reports on 79 crop and wild species. New Phytol., 156, 9-26.
25. Klein, A.M., Vaissiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C. et al. (2007). Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B-Biol. Sci., 274, 303-313.
26. Lopezaraiza-Mikel, M., Hayes, R., Whalley, M. & Memmott, J. (2007). The impact of an alien plant on a native plant-pollinator network: an experimental approach. Ecol. Lett., 10, 539-550.
27. MEA (Millennium Ecosystem Assessent) (2005). Ecosystems and human well-being: Synthesis. Island Press, Washington D.C.
28. Memmott, J., Craze, P.G., Waser, N.M. & Price, M.V. (2007). Global warming and the disruption of plant-pollinator interactions. Ecol. Lett., 10, 710-717.
29. Mevi-Schutz, J. & Erhardt, A. (2005). Amino acids in nectar enhance butterfly fecundity: a long-awaited link. Am. Nat., 165, 411-419.
30. Molet, M., Chittka, L., Stelzer, R.J., Streit, S. & Raine, N.E. (2008). Colony nutritional status modulates worker responses to foraging recruitment pheremone in the bumblebee Bombus terrestris. Behav. Ecol. Sociobiol., 62, 1919-1926.
31. Mullan, B., Wratt, D., Dean, S. & Hollis, M. (2008). Climate change effects and impacts assessment. a guidance manual for local government in New Zealand. In: NIWA Client Report p. 156.
32. Ollerton, J., Winfree, R. & Tarrant, S. (2011). How many flowering plants are pollinated by animals? Oikos, 120, 321-326.
33. Pacini, E., Nepi, M. & Vesprini, J.L. (2003). Nectar biodiversity: a short review. Plant Syst. Evol., 238, 7-21.
34. Petanidou, T. (2005). Sugars in Mediterranean floral nectars: an ecological and evolutionary approach. J. Chem. Ecol., 31, 1065-1088.
35. Petanidou, T., Van Laere, A., Ellis, W.N. & Smets, E. (2006). What shapes amino acid and sugar composition in Mediterranean floral nectars? Oikos, 115, 155-169.
36. Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O. & Kunin, W.E. (2010). Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol., 25, 345-353.
37. R Development Core Team (2006). R 2.3.1 - a language and environment.
38. Rafferty, N.E. & Ives, A.R. (2011). Effects of experimental shifts in flowering phenology on plant-pollinator interactions. Ecol. Lett., 14, 69-74.
39. Reich, P.B., Hobbie, S.E., Lee, T., Ellsworth, D.S., West, J.B., Tilman, D. et al. (2006). Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature, 440, 922-925.
40. 2 on flowering phenology and nectar production of nectar plants important for butterflies of calcareous grasslands. Oecologia, 113, 341-349.
41. Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R. et al. (2000). Global biodiversity scenarios for the year 2100. Science, 287, 1770-1774.
42. Schweiger, O., Biesmeijer, J.C., Bommarco, R., Hickler, T., Hulme, P.E., Klotz, S. et al. (2010). Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biol. Rev., 85, 777-795.
43. Smeets, P. & Duchateau, M.J. (2003). Longevity of Bombus terrestris workers (Hymenoptera: Apidae) in relation to pollen availability, in the absence of foraging. Apidologie, 34, 333-337.
44. Springer, C.J. & Ward, J.K. (2007). Flowering time and elevated atmospheric CO2. New Phytol., 176, 243-255.
45. Springer, C.J., Orozco, R.A., Kelly, J.K. & Ward, J.K. (2008). Elevated CO2 influences the expression of floral-initiation genes in Arabidopsis thaliana. New Phytol., 178, 63-67.
46. Tylianakis, J.M., Didham, R.K., Bascompte, J. & Wardle, D.A. (2008). Global change and species interactions in terrestrial ecosystems. Ecol. Lett., 11, 1351-1363.
47. Velthuis, H.H.W. & van Doorn, A. (2006). A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie, 37, 421-451.
48. Vitousek, P.M., Aber, J.D., Howarth, R.W., Likens, G.E., Matson, P.A., Schindler, W. et al. (1997). Human alteration of the global nitrogen cycle- sources and consequences. Ecol. Appl., 7, 737-750.
49. Winfree, R., Cariveau, D. & Bartomeus, I. (2011). Native pollinators in anthropogenic habitats. Ann. Rev. Ecol. Evol. Syst., 42, 1-22.
50. Zvereva, E.L. & Kozlov, M.V. (2006). Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a metaanalysis. Glob. Change Biol., 12, 27-41.