Beyond biomass: Measuring the effects of community-level nitrogen enrichment on floral traits, pollinator visitation and plant reproduction

Journal of Ecology

Volumn 98, Issue 3, 2010, Pages 705-717

  Burkle, Laura A ^a,b,c   Irwin, Rebecca E ^a,b  

^a Lamont Doherty Earth Observatory   (United States)

^b ROCKY MOUNTAIN BIOLOGICAL LABORATORY   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Indirect effects; Ipomopsis aggregata; Mutualism; Nutrient limitation; Potentilla pulcherrima; Species interactions

Indexed keywords

BIOMASS; BOTTOM-UP CONTROL; COMMUNITY RESPONSE; COMMUNITY STRUCTURE; DEVELOPMENTAL BIOLOGY; DICOTYLEDON; ENVIRONMENTAL CHANGE; FLORAL TRAIT; FLOWER VISITING; MUTUALISM; NITROGEN; NUTRIENT ENRICHMENT; NUTRIENT LIMITATION; PLANT-HERBIVORE INTERACTION; PLANT-POLLINATOR INTERACTION; POLLINATION; PRIMARY PRODUCTION; SPECIES DIVERSITY;

COLORADO; UNITED STATES;

IPOMOPSIS AGGREGATA; POACEAE; POTENTILLA; POTENTILLA PULCHERRIMA;

EID: 77952924852     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/j.1365-2745.2010.01648.x     Document Type: Article

References (68)

1. Agrawal AA, Strauss SY, Stout MJ. Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution 1999, 53:1093-1104.
2. Ashman TL. Is relative pollen production or removal a good predictor of relative male fitness? An experimental exploration with a wild strawberry (Fragaria virginiana, Rosaceae). American Journal of Botany 1998, 85:1166-1171.
3. Ashman T, Knight T, Steets J, Amarasekare P, Burd M, Campbell D, Dudash M, Johnston M, Mazer S, Mitchell R, Morgan M, Wilson W. Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 2004, 85:2408-2421.
4. Asikainen E, Mutikainen P. Pollen and resource limitation in a gynodioecious species. American Journal of Botany 2005, 92:487-494.
5. Baron JS, Rueth HM, Wolfe AM, Nydick KR, Allstott EJ, Minear JT, Moraska B. Ecosystem responses to nitrogen deposition in the Colorado Front Range. Ecosystems 2000, 3:352-368.
6. Biernaskie JM, Cartar RV. Variation in rate of nectar production depends on floral display size: a pollinator manipulation hypothesis. Functional Ecology 2004, 18:125-129.
7. Binkley D. Ion-exchange resin bags - factors affecting estimates of nitrogen availability. Soil Science Society of America Journal 1984, 48:1181-1184.
8. Bowman WD, Fisk MC. Primary production. Structure and Function of an Alpine Ecosystem: Niwot Ridge, CO 2001, 177-197. Bowman WD, Seastedt TR. eds, pp, Oxford University Press, Oxford
9. Bowman WD, Theodose TA, Schardt JC, Conant RT. Constraints of nutrient availability on primary production in two alpine tundra communities. Ecology 1993, 74:2085-2097.
10. Brancaleoni L, Gualmini M, Tomaselli M, Gerdol R. Responses of subalpine dwarf-shrub heath to irrigation and fertilization. Journal of Vegetation Science 2007, 18:337-344.
11. Brewer JS. The relationship between soil fertility and fire-stimulated floral induction in 2 populations of grass-leaved golden aster, Pityopsis graminifolia. Oikos 1995, 74:45-54.
12. Bronstein JL. Conditional outcomes in mutualistic interactions. Trends in Ecology and Evolution 1994, 9:214-217.
13. Brys R, Jacquemyn H, Endels P, De Blust G, Hermy M. Effect of habitat deterioration on population dynamics and extinction risks in a previously common perennial. Conservation Biology 2005, 19:1633-1643.
14. Campbell DR. Evolution of floral traits in a hermaphroditic plant: field measurements of heritabilities and genetic correlations. Evolution 1996, 50:1442-1453.
15. Campbell DR, Halama KJ. Resource and pollen limitations to lifetime seed production in a natural plant population. Ecology 1993, 74:1043-1051.
16. Campbell DR, Waser NM, Price MV, Lynch EA, Michell RJ. Components of phenotypic selection: pollen export and flower corolla width in Ipomopsis aggregata. Evolution 1991, 45:1458-1467.
17. Cross MS, Harte J. Compensatory responses to loss of warming-sensitive plant species. Ecology 2007, 88:740-748.
18. Dalgleish HJ, Kula AR, Hartnett DC, Sandercock BK. Responses of two bunchgrasses to nitrogen addition in tallgrass prairie: the role of bud bank demography. American Journal of Botany 2008, 95:672-680.
19. Dreisig H. Ideal free distributions of nectar foraging bumblebees. Oikos 1995, 72:161-172.
20. Dunne JA. Effects of climate change and variability on plant biomass and soil nitrogen cycling in subalpine meadows 2000, Dissertation, University of California, Berkeley
21. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine, and terrestrial systems. Ecology Letters 2007, 10:1135-1142.
22. Engel EC, Irwin RE. Linking pollinator visitation rate and pollen receipt. American Journal of Botany 2003, 90:1612-1618.
23. Eviner VT, Chapin FS, Vaughn CE. Nutrient manipulations in terrestrial systems. Methods in Ecosystem Science 2000, 289-307. Sala OE, Jackson RB, Mooney HAHowarth RW. eds, pp, Springer-Verlag, New York
24. Feinsinger P. Effects of plants species on each other's pollination: is community structure influenced? Trends in Ecology and Evolution 1987, 2:123-126.
25. Fenn ME, Haeuber R, Tonnesen GS, Baron JS, Grossman-Clarke S, Hope D, Jaffe DA, Copeland S, Geiser L, Rueth HM, Sickman JO. Nitrogen emissions, deposition, and monitoring in the western United States. BioScience 2003, 53:391-403.
26. Galen C. Why do flowers vary? BioScience 1999, 49:631-640.
27. Gotelli NJ, Entsminger GL. EcoSim: Null Models Software for Ecology, Version 7 2009, http://garyentsminger.com/ecosim/index.htm, Acquired Intelligence and Kesey-Bear, Jerico, VT, Available at:
28. Goulson D. Why do pollinators visit proportionally fewer flowers in large patches? Oikos 2000, 91:485-492.
29. Gurevitch J, Hedges L. Meta-analysis: combining the results of independent experiments. Design and Analysis of Ecological Experiments 2001, 347-369. Scheiner S, Gurevitch J. eds, pp, Oxford University Press, New York
30. Hainsworth F, Wolf L, Mercier T. Pollen limitation in a monocarpic species, Ipomopsis aggregata. Journal of Ecology 1985, 71:263-270.
31. Hedges LV, Gurevitch J, Curtis P. The meta-analysis of response ratios in experimental ecology. Ecology 1999, 80:1150-1156.
32. Irwin RE. The consequences of direct versus indirect species interactions to selection on traits: pollination and nectar robbing in Ipomopsis aggregata. American Naturalist 2006, 167:315-328.
33. Ishihama F, Washitani I. Behavior of queen bumblebee pollinators on Primula sieboldii (Primulaceae) in response to different patch sizes and spacing. Plant Species Biology 2007, 22:167-174.
34. Jongejans E, de Kroon H, Berendse F. The interplay between shifts in biomass allocation and costs of reproduction in four grassland perennials under simulated successional change. Oecologia 2006, 147:369-378.
35. Klinkhamer PG, Jong TJd, Linnebank LA. Small-scale spatial patterns determine ecological relationships: an experimental example using nectar production rates. Ecology Letters 2001, 4:559-567.
36. Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley R. Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecology Letters 2007, 10:299-314.
37. Lau TC, Stephenson AG. Effects of soil-nitrogen on pollen production, pollen grain-size, and pollen performance in Cucurbita pepo (Cucurbitaceae). American Journal of Botany 1993, 80:763-768.
38. Mattila E, Kuitunen MT. Nutrient versus pollination limitation in Platanthera bifolia and Dactylorhiza incarnata (Orchidaceae). Oikos 2000, 89:360-366.
39. Mitchell RJ. Effects of floral traits, pollinator visitation, and plant size on Ipomopsis aggregata fruit production. American Naturalist 1994, 143:870-889.
40. Monaco TA, Johnson DA, Norton JM, Jones TA, Connors KJ, Norton JB, Redinbaugh MB. Contrasting responses of intermountain west grasses to soil nitrogen. Journal of Range Management 2003, 56:282-290.
41. Munoz A, Celedon-Neghme C, Cavieres L, Arroyo M. Bottom-up effects of nutrient availability on flower production, pollinator visitation, and seed output in a high-Andean shrub. Oecologia 2005, 143:126-135.
42. National Acid Deposition Program 2006, http://nadp.sws.uiuc.edu/, Available at:
43. Ne'eman G, Ne'eman R, Ellison AM. Limits to reproductive success of Sarracenia purpurea (Sarraceniaceae). American Journal of Botany 2006, 93:1660-1666.
44. Neytcheva MS, Aarssen LW. More plant biomass results in more offspring production in annuals, or does it? Oikos 2008, 117:1298-1307.
45. Pleasants J. Bumblebee response to variation in nectar availability. Ecology 1981, 62:1648-1661.
46. Pleasants JM. Nectar production patterns in Ipomopsis aggregata (Polemoniaceae). American Journal of Botany 1983, 70:1468-1475.
47. Potts S, Vulliamy B, Dafni A, Ne'eman G, Willmer P. Linking bees and flowers: how do floral communities structure pollinator communities? Ecology 2003, 84:2628-2642.
48. Poveda K, Steffan-Dewenter I, Scheu S, Tscharntke T. Floral trait expression and plant fitness in response to below- and aboveground plant-animal interactions. Perspectives in Plant Ecology Evolution and Systematics 2005, 7:77-83.
49. Price MV, Waser NM, Irwin RE, Campbell DR, Brody AK. Temporal and spatial variation in pollination of a montane herb: a seven-year study. Ecology 2005, 86:2106-2116.
50. Price MV, Campbell DR, Waser NM, Brody AK. Bridging the generation gap in plants: pollination, parental fecundity, and offspring demography. Ecology 2008, 89:1596-1604.
51. Quinn GP, Keough MJ. Experimental Design and Data Analysis for Biologists 2002, University Press, Cambridge
52. Reekie E, Bazzaz FA. Reproductive Allocation in Plants 2005, Elsevier Academic Press, Burlington, MA
53. Robertson AW, Macnair MR. The effects of floral display size on pollinator service to individual flowers of Myosotis and Mimulus. Oikos 1995, 72:106-114.
54. Rosenberg MS, Adams DC, Gurevitch J. MetaWin: Statistical Software for Meta-Analysis, Version 2 2000, Sinauer Associates, Sunderland, MA
55. Shaver GR, Chapin FS. Effect of fertilizer on production and biomass of tussock tundra, Alaska, USA. Arctic and Alpine Research 1986, 18:261-268.
56. Siemann E. Experimental tests of effects of plant productivity and diversity on grassland arthropod diversity. Ecology 1998, 79:2057-2069.
57. Sievering H, Rusch D, Marquez L. Nitric acid, particulate nitrate and ammonium in the continental free troposphere: nitrogen deposition to an alpine tundra ecosystem. Atmospheric Environment 1996, 30:2527-2537.
58. Snow AA, Lewis PO. Reproductive traits and male-fertility in plants - empirical approaches. Annual Review of Ecology and Systematics 1993, 24:331-351.
59. Strauss SY, Conner JK, Rush SL. Foliar herbivory affects floral characters and plant attractiveness to pollinators: implications for male and female plant fitness. American Naturalist 1996, 147:1098-1107.
60. Suding KN, Collins SL, Gough L, Clark C, Cleland EE, Gross KL, Milchunas DG, Pennings S. Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:4387-4392.
61. Tilman D. Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecological Monographs 1987, 57:189-214.
62. de Valpine P, Harte J. Plant responses to experimental warming in a montane meadow. Ecology 2001, 82:637-648.
63. Wallace JB, Eggert SL, Meyer JL, Webster JR. Multiple trophic levels of a forest stream linked to terrestrial litter inputs. Science 1997, 277:102-104.
64. Wolfe BE, Husband BC, Klironomos JN. Effects of a belowground mutualism on an aboveground mutualism. Ecology Letters 2005, 8:218-223.
65. Wootton J. Indirect effects and habitat use in an intertidal community: interaction chains and interaction modifications. American Naturalist 1993, 141:71-89.
66. Wootton JT. The nature and consequences of indirect effects in ecological communities. Annual Review of Ecology and Systematics 1994, 25:443-466.
67. Zimmerman M. Plant reproduction and optimal foraging: experimental nectar manipulations in Delphinium nelsonii. Oikos 1983, 41:57-63.
68. Zimmerman M, Pyke G. Reproduction in Polemonium: assessing the factors limiting seed set. American Naturalist 1988, 131:723-738.