Testing the effect-response framework: Key response and effect traits determining above-ground biomass of salt marshes

Journal of Vegetation Science

Volumn 22, Issue 3, 2011, Pages 387-401

  Minden, Vanessa ^a   Kleyer, Michael ^a  

^a UNIVERSITY OF OLDENBURG   (Germany)

Author keywords

Allometric relationships; Effect trait; Path analysis; Response trait; Structural equation modelling; Trade off

Indexed keywords

ABOVEGROUND BIOMASS; ALLOMETRY; BIOMASS ALLOCATION; COHORT ANALYSIS; ECOSYSTEM FUNCTION; KEYSTONE SPECIES; LIFE HISTORY TRAIT; NUTRIENT AVAILABILITY; PATH ANALYSIS; PHYTOMASS; SALINITY; SALTMARSH; TRADE-OFF;

GERMANY;

EID: 79954997526     PISSN: 11009233     EISSN: 16541103     Source Type: Journal    
DOI: 10.1111/j.1654-1103.2011.01272.x     Document Type: Article

References (78)

1. Ad-Hoc-AG Boden 2005. Bodenkundliche Kartieranleitung. E. Schweitzerbart'sche Verlagsbuchhandlung, Hannover, DE.
2. Aerts, R. & Chapin, F.S.I. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances of Ecological Research 30: 1-67.
3. Allen, S.E. 1989. Chemical analysis of ecological materials. Blackwell Scientific, Oxford, UK.
4. Backhaus, K., Erichson, B., Plinke, W. & Weiber, R. 2003. Multivariate analyse methoden. Springer-Verlag, Berlin, DE.
5. Bakker, J.P., De Leeuw, J., Dijkema, K.S., Leendertse, P.C., Prins, H.H.T. & Rozema, J. 1993. Salt marshes along the coast of The Netherlands. Hydrobiologia 265: 73-95.
6. Bakker, J.P., Bos, D., Stahl, J., De Vries, Y. & Jensen, A. 2003. Biodiversität und Landnutzung in Salzwiesen. Nova Acta Leopoldina NF 87 328: 163-194.
7. Bakker, J.P., Bunje, J., Dijkema, K.S., Frikke, J., Hecker, N., Kers, B., Körber, P., Kohlus, J. & Stock, M. 2005. Salt marshes. In: Essink, K., Dettman, C., Farke, H., Laursen, K., Lüerßen, G., Marencic, H. & Wiersinga, W. (eds.) Wadden Sea quality status report 2004, Wadden Sea ecosystem No. 19 - 2005. Common Wadden Sea Secretariat (CWSS), Wilhelmshaven, DE.
8. Bazzaz, F.A. 1997. Allocation of resources in plants: state of the science and critical questions. In: Bazzaz, F.A. & Grace, J. (eds.) Plant resource allocation. pp. 1-37. Academic Press, San Diego, CA, US.
9. Blew, J., Günther, K., Laursen, K., van Roomen, M., Südbeck, P., Eskildsen, K., Potel, P. & Rösner, H.-U. 2005. Overview on trend and numbers of migratory waterbirds in the Wadden Sea 1980-2000. In: Blew, J. & Südbeck, P. (eds.) Migratory water birds in the Wadden Sea 1980-2000. Common Wadden Sea Secretariat (CWSS), Wilhelmshaven, DE.
10. Browne, M. & Cudeck, R. 1993. Alternative ways of assessing equation model fit. In: Boollen, K.A. & Long, J.S. (eds.) Testing structural equation models. pp. 136-162. Sage Publications, Newbury Park, CA, US.
11. Cavalieri, A.J. 1983. Proline and glycine betaine accumulation by Spartina alterniflora Loisel. in response to NaCl and nitrogen in a controlled environment. Oecologia 57: 20-24.
12. Cunningham, S., Summerhayes, B. & Westoby, M. 1999. Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecological Monographs 69: 569-588.
13. de Bello, F., Lavorel, S., Diaz, S., Harrington, R., Cornelissen, J.H.C., Bardgett, R.D., Berg, M.P., Cipriotti, P., Feld, C.K., Hering, D., da Silva, P.M., Potts, S.G., Sandin, L., Sousa, J.P., Storkey, J., Wardle, D.A. & Harrison, P.A. 2010. Towards an assessment of multiple ecosystem processes and services via functional traits. Biodiversity and Conservation 19: 2873-2893.
14. De Deyn, G.B., Cornelissen, J.H.C. & Bardgett, R.D. 2008. Plant functional traits and soil carbon sequestration in contrasting biomes. Ecology Letters 11: 516-531.
15. De Leeuw, J., Olff, H. & Bakker, J.P. 1990. Year-to-year variation in peak above-ground biomass of six salt-marsh angiosperm communities as related to rainfall deficit and inundation frequency. Aquatic Botany 36: 139-151.
16. Deutscher Wetterdienst 2009. Mean climate values for the period 1961 to 1990. Available at (accessed 6 April 2009).
17. Díaz, S. & Cabido, M. 2001. Vive la difference: plant functional diversity matters to ecosystem processes. Trends in Ecology & Evolution 16: 646-655.
18. Dormann, C.F., Van der Wal, R. & Bakker, J.P. 2000. Competition and herbivory during salt marsh succession: the importance of forb growth strategy. Journal of Ecology 88: 571-583.
19. Egan, T.P. & Ungar, I.A. 2001. Competition between Salicornia europaea and Atriplex prostrata (Chenopodiaceae) along an experimental salinity gradient. Wetlands Ecology and Management 9: 457-461.
20. Egnér, H., Riehm, H. & Domingo, W.R. 1960. Untersuchungen über die Bodenanalyse als Grundlage für die Beurteilung des Nährstoffzustandes des Bodens II. Chemische Extraktionsmethoden zur Phosphor- und Kaliumbestimmung. Kungl. Lantbrukshögskolans Annualer 26: 199-215.
21. Enquist, B.J. & Niklas, K.J. 2002. Global allocation rules for patterns of biomass partitioning in seed plants. Science 295: 1517-1520.
22. Garnier, E., Shipley, B., Roumet, C. & Laurent, G. 2001. A standardized protocol for the determination of specific leaf area and leaf dry matter content. Functional Ecology 15: 688-695.
23. Garnier, E., Cortez, J., Billès, G., Navas, M.-L., Roumet, C., Debussche, M., Laurent, G., Blanchard, A., Aubry, D., Bellmann, A., Neill, C. & Toussaint, J.-P. 2004. Plant functional markers capture ecosystem properties during secondary succession. Ecology 85: 2630-2637.
24. Garnier, E., Lavorel, S., Ansquer, P., Castro, H., Cruz, P., Dolezal, J., Eriksson, O., Fortunel, C., Freitas, H., Golodets, C., Grugulis, K., Jouany, C., Kazakou, E., Kigel, J., Kleyer, M., Lehsten, V., Lepš, J., Meier, T., Pakeman, R., Papadimitriou, M., Papanastasis, V.P., Quested, H., Quétier, F., Robson, M., Roumet, C., Rusch, G., Skarpe, C., Sternberg, M., Theau, J.-P., Thébault, A., Vile, D. & Zarovali, M. 2007. Assessing the effects of land-use change on plant traits, communities and ecosystem functioning in grasslands: a standardized methodology and lessons from an application to 11 European sites. Annals of Botany 99: 967-985.
25. Gitay, H. & Noble, I.R. 1997. What are functional types and how should we seek them? In: Smith, T.M., Shugart, H.H. & Woodward, F.I. (eds.) Plant functional types: their relevance to ecosystem properties. pp. 3-19. Cambridge University Press, Cambridge, UK.
26. Grace, J.B. 2006. Structural equation modeling and natural systems. Cambridge University Press, Cambridge, UK.
27. Grace, J.B. & Pugesek, B.H. 1997. A structural equation model of plant species richness and its application to a coastal wetland. The American Naturalist 149: 436-460.
28. Grace, J.B. & Pugesek, B.H. 1998. On the use of path analysis and related procedures for the investigation of ecological problems. The American Naturalist 152: 151-159.
29. Grime, J.P. 1998. Benefits of plant diversity to ecosystems: immediate, filter and founder effects. Journal of Ecology 86: 902-910.
30. Groenendijk, A.M. 1985. Ecological consequences of tidal management for the salt-marsh vegetation. Vegetatio 62: 415-424.
31. Hammer, Ø., Harper, D.A.T. & Ryan, P.D. 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4 (1): 9. Available at .
32. Harrison, S.P., Prentice, I.C., Barboni, D., Kohfeld, K.E., Ni, J. & Sutra, J.P. 2010. Ecophysiological and bioclimatic foundations for a global plant functional classification. Journal of Vegetation Science 21: 300-317.
33. Hooper, D.U., Chapin, F.S., Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H., Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setälä, H., Symstad, A.J., Vandermeer, J. & Ward, D.A. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge and needs for further research. Ecological Monographs 75: 3-35.
34. Janiesch, P. 1991. Oberirdische Biomasseproduktion und Mineralstoffhaushalt von Salzwiesen der niedersächsischen Küste. Drosera 1/2: 127-138.
35. Kazakou, E., Vile, D., Shipley, B., Gallet, C. & Garnier, E. 2006. Co-variations in litter decomposition, leaf traits and plant growth in species from a Mediterranean old-field succession. Functional Ecology 20: 21-30.
36. Kiehl, K., Esselink, P. & Bakker, J.P. 1997. Nutrient limitation and plant species composition in temperate salt marshes. Oecologia 111: 325-330.
37. Kingsolver, J.G. & Schemske, D.W. 1991. Path analyses of selection. Trends in Ecology & Evolution 6: 276-280.
38. Kinzel, H. 1982. Pflanzenökologie und Mineralstoffwechsel. Ulmer Verlag, Stuttgart, DE.
39. Knevel, I.C., Bekker, R.M., Kunzmann, D., Stadler, M. & Thompson, K. 2005. The LEDA Traitbase - Collecting and measuring standards of life-history traits of the northwest European flora. University of Groningen, Community and Conservation Ecology group, Groningen, NL.
40. Kuijper, D.P.J., Dubbeld, J. & Bakker, J.P. 2005. Competition between two grass species with and without grazing over a productivity gradient. Plant Ecology 179: 237-246.
41. Lavorel, S. & Garnier, E. 2002. Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Functional Ecology 16: 545-556.
42. Lavorel, S., Díaz, S., Cornelissen, J.H.C., Garnier, E., Harrison, S.P., McIntyre, S., Pausas, J.G., Pérez-Harguindeguy, N., Roumet, C. & Urcelay, C. 2007. Plant functional types: Are we getting any closer to the holy grail? Series: global change - the IGBP series. Springer Verlag, Berlin, DE.
43. Leeuw, J.D., Olff, H. & Bakker, J.P. 1990. Year-to-year variation in peak above-ground biomass of six salt-marsh angiosperm communities as related to rainfall deficit and inundation frequency. Aquatic Botany 36: 139-151.
44. 4 (Spartina anglica) salt marsh species. Vegetatio 104/105: 379-388.
45. Lenssen, G.M., van Duin, W.E., Jak, P. & Rozema, J. 1995. The response of Aster tripolium and Puccinellia maritima to atmospheric carbon dioxide enrichment and their interactions with flooding and salinity. Aquatic Botany 50: 181-192.
46. Mardia, K.V. 1970. Measures of multivariate skewness and kurtosis with applications. Biometrika 57: 519-530.
47. Mardia, K.V. 1974. Applications of some measures of multivariate skewness and kurtosis in testing normality and robustness studies. Sankhyā - The Indian Journal of Statistics Series B 36: 115-128.
48. McCarthy, M.C. & Enquist, B.J. 2007. Consistency between an allometric approach and optimal partitioning theory in global patterns of plant biomass allocation. Functional Ecology 21: 713-720.
49. McCune, B. & Grace, J.B. 2002. Structural equation modeling. In: McCune, B. & Grace, J.B. (eds.) Analysis of ecological communities. pp. 233-256. MjM Software Design, Gleneden Beach, OR, US.
50. Mitchell, R.J. 1992. Testing evolutionary and ecological hypotheses using path analysis and structural equation modeling. Functional Ecology 6: 123-129.
51. Moles, A.T. & Westoby, M. 2006. Seed size and plant strategy across the whole life cycle. Oikos 133: 91-105.
52. Müller, I., Schmid, B. & Weiner, J. 2000. The effect of nutrient availability on biomass allocation patterns in 27 species of herbaceous plants. Perspectives in Plant Ecology, Evolution and Systematics 3/2: 115-127.
53. Murphy, J. & Riley, J.P. 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27: 31-36.
54. Naeem, S. & Wright, E.J. 2003. Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecology Letters 6: 567-579.
55. Niklas, K.J. 1994. Plant allometry. The scaling of form and process. The University of Chicago Press, Chicago, IL, US.
56. Niklas, K.J. 2006. Plant allometry, leaf nitrogen and phosphorus stoichiometry, and interspecific trends in annual growth rates. Annals of Botany 97: 155-163.
57. Niklas, K.J. & Enquist, B.J. 2003. An allometric model for seed plant reproduction. Evolutionary Ecology Research 5: 79-88.
58. Obeso, J.R. 2002. The costs of reproduction in plants. New Phytologist 155: 321-348.
59. Olff, H., de Leeuw, J., Bakker, J.P., Platerink, R.J., van Wijnen, H.J. & de Munck, W. 1997. Vegetation succession and herbivory in a salt marsh: changes induced by sea level rise and silt deposition along an elevation gradient. Journal of Ecology 85: 799-814.
60. Pontes, L.D.S., Soussana, J.F., Louault, F., Andueza, D. & Carrere, P. 2007. Leaf traits affect the above-ground productivity and quality of pasture grasses. Functional Ecology 21: 844-853.
61. Poorter, H. & de Jong, R. 1999. A comparison of specific leaf area, chemical composition and leaf construction costs of field plants from 15 habitats differing in productivity. New Phytologist 143: 163-176.
62. Pott, R. 1995. Farbatlas Nordseeküste und Nordseeinseln.. Ulmer Verlag, Stuttgart, DE.
63. Rozema, J., Bijwaard, P., Prast, G. & Broekman, R. 1985. Ecophysiological adaptations of coastal halophytes from foredunes and salt marshes. Vegetatio 62: 499-521.
64. Schirmer, U. & Breckle, S.W. 1982. The role of bladders for salt removal in some Chenopodiaceae (mainly Atriplex species). In: Sen, D.N. & Rajpurohit, K.S. (eds.) Contributions to the ecology of halophytes. pp. 215-231. Dr Junk, The Hague, NL.
65. Schlichting, E., Blume, H.P. & Stahr, K. 1995. Bodenkundliches praktikum. Blackwell, Berlin, DE.
66. Shipley, B. 2004. Analysing the allometry of multiple interacting traits. Perspectives in Plant Ecology, Evolution and Systematics 6: 235-241.
67. Steward, G.R., Larher, F., Ahmand, I. & Lee, J.A. 1979. Nitrogen metabolism and salt tolerance in higher plants - halophytes. In: Jefferies, R.L. & Davy, A.J. (eds.) Ecological processes in coastal environments. pp. 229-241. Blackwell, Oxford, UK.
68. Suding, K.N., Lavorel, S., Chapin III, F.S., Cornelissen, J.H.C., Díaz, S., Garnier, E., Goldberg, D.E., Hooper, D.U., Jackson, S.T. & Navas, M.L. 2008. Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants. Global Change Biology 14: 1125-1140.
69. SynBioSys Species Checklist 2010. Available at (accessed: 7 June 2010)
70. Tarczynski, M.C., Jensen, R.G. & Bohnert, H.J. 1993. Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259: 508-510.
71. Thompson, B.K., Weiner, J. & Warwick, S.I. 1991. Size-dependent reproductive output in agricultural weeds. Canadian Journal of Botany-Revue Canadienne De Botanique 69: 442-446.
72. Tilman, D. 1988. Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton, NJ, US.
73. Van Diggelen, J., Rozema, J., Dickson, D.M. & Broekman, R. 1986. β-3-Dimethylsulphoniopropionate, proline and quaternary ammonium compounds in Spartina anglica in relation to sodium chloride, nitrogen and sulphur. New Phytologist 103: 573-586.
74. Walker, B., Kinzig, A. & Langridge, J. 1999. Plant attribute diversity, resilience, and ecosystem function: the nature and significance of dominant and minor species. Ecosystems 2: 95-113.
75. Warton, D.I., Wright, I.J., Falster, D.S. & Westoby, M. 2006. Bivariate line-fitting methods for allometry. Biological Reviews 81: 259-291.
76. Weiner, J., Campbell, L.G., Pino, J. & Echarte, L. 2009. The allometry of reproduction within plant populations. Journal of Ecology 97: 1220-1233.
77. Westoby, M., Falster, D.S., Moles, A.T., Vesk, P.A. & Wright, I.J. 2002. Plant ecological strategies: some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33: 125-159.
78. Wright, I.J., Reich, P.B., Westoby, M., Ackerly, D.D., Baruch, Z., Bongers, F., Cavenders-Bares, J., Chapin, T., Cornelissen, J.H.C., Diemer, M., Flexas, J., Garnier, E., Groom, P.K., Gulias, J., Hikosaka, K., Lamont, B.B., Lee, T., Lee, W., Lusk, C., Midgley, J.J., Navas, M.-L., Niinements, Ü., Oleksyn, J., Osada, N., Poorter, H., Poot, P., Prior, L., Pyankow, V.I., Roumet, C., Thomas, S.C., Tjoelker, M.G., Veneklaas, E.J. & Villar, R. 2004. The worldwide leaf economics spectrum. Nature 428: 821-827.