Abstract
The differential ability of forest herbs to colonize secondary forests on former agricultural land is generally attributed to different rates of dispersal. After propagule arrival, however, establishing individuals still have to cope with abiotic soil legacies from former agricultural land use. We focused on the plastic responses of forest herbs to increased phosphorus availability, as phosphorus is commonly found to be persistently bioavailable in post-agricultural forest soils. In a pot experiment performed under field conditions, we applied three P levels to four forest herbs with contrasting colonization capacities: Anemone nemorosa, Primula elatior, Circaea lutetiana and Geum urbanum. To test interactions with light availability, half of the replicas were covered with shade cloths. After two growing seasons, we measured aboveground P uptake as well as vegetative and regenerative performance. We hypothesized that fast-colonizing species respond the most opportunistically to increased P availability, and that a low light availability can mask the effects of P on performance. All species showed a significant increase in P uptake in the aboveground biomass. The addition of P had a positive effect on the vegetative performances of two of the species, although this was unrelated to their colonization capacities. The regenerative performance was affected by light availability (not by P addition) and was related to the species’ phenology. Forest herbs can obviously benefit from the increased availability of P in post-agricultural forests, but not all species respond in the same way. Such differential patterns of plasticity may be important in community dynamics, as they affect the interactions among species.
Similar content being viewed by others
References
Anderson WB (2003) Interactions of nutrient effects with other biotic factors in the herbaceous layer. In: Gilliam FS, Roberts MR (eds) The herbaceous layer in forests of eastern North America. Oxford University Press, Oxford, pp 91–101
Baeten L, Hermy M, Verheyen K (2009) Environmental limitation contributes to the differential colonization capacity of two forest herbs. J Veg Sci 20:209–223
Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155
Callaway RM, Pennings SC, Richards CL (2003) Phenotypic plasticity and interactions among plants. Ecology 84:1115–1128
Dambrine E, Dupouey JL, Laut L, Humbert L, Thinon M, Beaufils T, Richard H (2007) Present forest biodiversity patterns in France related to former Roman agriculture. Ecology 88:1430–1439
De Keersmaeker L, Martens L, Verheyen K, Hermy M, De Schrijver A, Lust N (2004) Impact of soil fertility and insolation on diversity of herbaceous woodland species colonizing afforestations in Muizen Forest (Belgium). For Ecol Manag 188:291–304
DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81
Donohue K, Pyle EH, Messiqua D, Heschel MS, Schmitt J (2001) Adaptive divergence in plasticity in natural populations of Impatiens capensis and its consequences for performance in novel habitats. Evolution 55:692–702
Eickmeier WG, Schussler EE (1993) Responses of the spring ephemeral Claytonia virginica L. to light and nutrient manipulations and implications for the Vernal-Dam hypothesis. Bull Torrey Bot Club 120:157–165
Elemans M (2004) Light, nutrients and the growth of herbaceous forest species. Acta Oecol Int J Ecol 26:197–202
Endels P, Adriaens D, Verheyen K, Hermy M (2004) Population structure and adult plant performance of forest herbs in three contrasting habitats. Ecography 27:225–241
Falkengren-Grerup U, ten Brink DJ, Brunet J (2006) Land use effects on soil N, P, C and pH persist over 40–80 years of forest growth on agricultural soils. For Ecol Manag 225:74–81
Flinn KM (2007) Microsite-limited recruitment controls fern colonization of post-agricultural forests. Ecology 88:3103–3114
Flinn KM, Marks PL (2007) Agricultural legacies in forest environments: tree communities, soil properties, and light availability. Ecol Appl 17:452–463
Flinn KM, Vellend M (2005) Recovery of forest plant communities in post-agricultural landscapes. Frontiers Ecol Environ 3:243–250
Fraterrigo JM, Turner MG, Pearson SM, Dixon P (2005) Effects of past land use on spatial heterogeneity of soil nutrients in southern Appalachian forests. Ecol Monogr 75:215–230
Fraterrigo JM, Turner MG, Pearson SM (2006) Previous land use alters plant allocation and growth in forest herbs. J Ecol 94:548–557
Gilliam FS (2007) The ecological significance of the herbaceous layer in temperate forest ecosystems. Bioscience 57:845–858
Gress SE, Nichols TD, Northcraft CC, Peterjohn WT (2007) Nutrient limitation in soils exhibiting differing nitrogen availabilities: what lies beyond nitrogen saturation? Ecology 88:119–130
Griffith TM, Sultan SE (2005) Shade tolerance plasticity in response to neutral vs green shade cues in Polygonum species of contrasting ecological breadth. New Phytol 166:141–147
Grime JP, Thompson K, Hunt R, Hodgson JG, Cornelissen JHC, Rorison IH, Hendry GAF, Ashenden TW, Askew AP, Band SR, Booth RE, Bossard CC, Campbell BD, Cooper JEL, Davison AW, Gupta PL, Hall W, Hand DW, Hannah MA, Hillier SH, Hodkinson DJ, Jalili A, Liu Z, Mackey JML, Matthews N, Mowforth MA, Neal AM, Reader RJ, Reiling K, RossFraser W, Spencer RE, Sutton F, Tasker DE, Thorpe PC, Whitehouse J (1997) Integrated screening validates primary axes of specialisation in plants. Oikos 79:259–281
Hermy M, Verheyen K (2007) Legacies of the past in the present-day forest biodiversity: a review of past land-use effects on forest plant species composition and diversity. Ecol Res 22:361–371
Hilborn R, Mangel M (1997) The ecological detective: confronting models with data. Princeton University Press, Princeton
Hipps NA, Davies MJ, Dodds P, Buckley GP (2005) The effects of phosphorus nutrition and soil pH on the growth of some ancient woodland indicator plants and their interaction with competitor species. Plant Soil 271:131–141
Honnay O, Verheyen K, Butaye J, Jacquemyn H, Bossuyt B, Hermy M (2002) Possible effects of habitat fragmentation and climate change on the range of forest plant species. Ecol Lett 5:525–530
Jacquemyn H, Vandepitte K, Roldan-Ruiz I, Honnay O (2009) Rapid loss of genetic variation in a founding population of Primula elatior (Primulaceae) after colonization. Ann Bot 103:777–783
Koerner W, Dupouey JL, Dambrine E, Benoit M (1997) Influence of past land use on the vegetation and soils of present day forest in the Vosges mountains, France. J Ecol 85:351–358
Marschner H (ed) (1995) Mineral nutrition of higher plants. Academic, London
Meekins JF, McCarthy BC (2000) Responses of the biennial forest herb Alliaria petiolata to variation in population density, nutrient addition and light availability. J Ecol 88:447–463
Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692
Muller RN (2003) Nutrient relations of the herbaceous layer in deciduous forest ecosystems. In: Gilliam FS, Roberts MR (eds) The herbaceous layer in forests of eastern North America. Oxford University Press, Oxford, pp 15–37
Pigott CD, Taylor K (1964) The distribution of some woodland herbs in relation to the supply of nitrogen and phosphorus in the soil. J Ecol 52:175–185
Pons TL (1977) Ecophysiological study in field layer of ash coppice. 3. Influence of diminishing light-intensity during growth on Geum urbanum and Cirsium palustre. Acta Bot Neerl 26:251–263
R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna (ISBN 3-900051-07-0; http://www.R-project.org)
Richter DD, Allen HL, Li JW, Markewitz D, Raikes J (2006) Bioavailability of slowly cycling soil phosphorus: major restructuring of soil P fractions over four decades in an aggrading forest. Oecologia 150:259–271
Rorison IH (1968) Response to phosphorus of some ecologically distinct plant species. I. Growth rates and phosphorus absorption. New Phytol 67:913–923
Scheel KC (1936) Colorimetric determination of phosphoric acid in fertilizers with the Pulfrich photometer. Z Anal Chem 105:256–269
Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annu Rev Ecol Syst 17:667–693
Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–542
Sultan SE (2001) Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. Ecology 82:328–343
Taylor K (2009) Biological flora of the British Isles: Urtica dioica L. J Ecol 97:1436–1458
Valladares F, Sanchez-Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116
Valladares F, Gianoli E, Gomez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytol 176:749–763
Vellend M (2004) Parallel effects of land-use history on species diversity and genetic diversity of forest herbs. Ecology 85:3043–3055
Vellend M (2005) Land-use history and plant performance in populations of Trillium grandiflorum. Biol Conserv 124:217–224
Verburg R, Grava D (1998) Differences in allocation patterns in clonal and sexual offspring in a woodland pseudo-annual. Oecologia 115:472–477
Verheyen K, Hermy M (2001) The relative importance of dispersal limitation of vascular plants in secondary forest succession in Muizen Forest, Belgium. J Ecol 89:829–840
Verheyen K, Hermy M (2004) Recruitment and growth of herb-layer species with different colonizing capacities in ancient and recent forests. J Veg Sci 15:125–134
Verheyen K, Bossuyt B, Hermy M, Tack G (1999) The land use history (1278–1990) of a mixed hardwood forest in western Belgium and its relationship with chemical soil characteristics. J Biogeogr 26:1115–1128
Verheyen K, Honnay O, Motzkin G, Hermy M, Foster DR (2003) Response of forest plant species to land-use change: a life-history trait-based approach. J Ecol 91:563–577
Acknowledgments
The authors thank Greet De bruyn, Luc Willems, Bert Schamp and Raphaël Cielen for sample preparation and chemical analyses of the samples. We also thank Meelis Pärtel and two anonymous referees for helpful comments on the manuscript. This paper was written while the first author held a scholarship from the Institute for the Promotion of Innovation Through Science and Technology in Flanders (IWT-Vlaanderen). The second and the third authors held Ph.D. fellowships from the Research Foundation—Flanders (FWO), and the fourth author held a postdoctoral fellowship from the FWO.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Meelis Partel.
Rights and permissions
About this article
Cite this article
Baeten, L., Vanhellemont, M., De Frenne, P. et al. Plasticity in response to phosphorus and light availability in four forest herbs. Oecologia 163, 1021–1032 (2010). https://doi.org/10.1007/s00442-010-1599-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-010-1599-z