Oecologia

pp 1–13 | Cite as

Competition along productivity gradients: news from heathlands

  • Florian Delerue
  • Maya Gonzalez
  • David L. Achat
  • Luc Puzos
  • Laurent Augusto
Community ecology – original research

Abstract

The importance of competition in low productive habitats is still debated. Studies which simultaneously evaluate preemption of resources and consequences for population dynamics are needed for a comprehensive view of competitive outcomes. We cultivated two emblematic species of European heathlands (Calluna vulgaris and Molinia caerulea) in a nursery for 2 years at two fertility levels, reproducing the productivity gradient found in phosphorus (P)-depleted heathlands in southwest France. The second year, we planted Ulex europaeus seedlings, a ubiquitous heathland species, under the cover of the two species to evaluate its ability to regenerate. Half of the seedlings were placed in tubes for exclusion of competitor roots. We measured the development of the competitors aboveground and belowground and their interception of resources (light, water, inorganic P). Ulex seedlings’ growth and survival were also measured. Our results on resources interception were consistent with species distribution in heathlands. Molinia, which dominates rich heathlands, was the strongest competitor for light and water in the rich soil. Calluna, which dominates poor heathlands, increased its root allocation in the poor soil, decreasing water and inorganic P availability. However, the impact of total competition and root competition on Ulex seedlings decreased in the poor soil. Other mechanisms, especially decrease of water stress under neighbouring plant cover, appeared to have more influence on the seedlings’ response. We found no formal contradiction between Tilman and Grime’s theories. Root competition has a primary role in acquisition of soil resources in poor habitats. However, the importance of competition decreases with decreasing fertility.

Keywords

Grime–Tilman debate Competition importance Resource-ratio hypothesis Resource supply pre-emption Plant–plant interactions 

Notes

Acknowledgements

This study was funded by the Bordeaux Sciences Agro—Institute of Agricultural Sciences and the French National Institute of Agricultural Research (INRA). We thank Patrick Pastuszka, Frederic Bernier, and all the INRA-UE570 Forêt Pierroton team for making the tree nursery available and for experimental support. We are grateful to Helene Budzinsky and Karine Lemenach from the CNRS UMR 5805 EPOC for N isotope measurements and %Ndfa determination. We thank Catherine Lambrot, Sylvie Milin and Nathalie Gallegos for measurements of nutrient concentrations, Christian Morel and Anne Gallet-Budynek for help regarding 32P labelling and isotopic dilution method. We thank Christophe Chipeaux for help with the soil water content probes. We thank Sylvie Niollet for field support. We also thank Daphne Goodfellow and Fabien Delerue for revising the English.

Author contribution statement

FD, MG, LP and LA conceived and designed the experiments. FD and LP coordinated fieldwork. DLA took in charge phosphorus availability estimation. FD analysed the data. FD, MG, DLA and LA wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2018_4120_MOESM1_ESM.pdf (877 kb)
Supplementary material 1 (PDF 877 kb)

References

  1. Achat DL, Bakker MR, Augusto L et al (2009) Evaluation of the phosphorus status of P-deficient podzols in temperate pine stands: combining isotopic dilution and extraction methods. Biogeochemistry 92:183–200.  https://doi.org/10.1007/s10533-008-9283-7 CrossRefGoogle Scholar
  2. Achat D, Augusto L, Morel C, Bakker MR (2011) Predicting available phosphate ions from physical–chemical soil properties in acidic sandy soils under pine forests. J Soils Sedim 11:452–466.  https://doi.org/10.1007/s11368-010-0329-9 CrossRefGoogle Scholar
  3. Achat DL, Pousse N, Nicolas M et al (2016) Soil properties controlling inorganic phosphorus availability: general results from a national forest network and a global compilation of the literature. Biogeochemistry 127:255–272.  https://doi.org/10.1007/s10533-015-0178-0 CrossRefGoogle Scholar
  4. Aerts R (1989) Aboveground biomass and nutrient dynamics of Calluna vulgaris and Molinia caerulea in a dry heathland. Oikos 56:31–38.  https://doi.org/10.2307/3566084 CrossRefGoogle Scholar
  5. Aerts R (1990) Nutrient use efficiency in evergreen and deciduous species from heathlands. Oecologia 84:391–397CrossRefPubMedGoogle Scholar
  6. Aerts R (1999) Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks. J Exp Bot 50:29–37.  https://doi.org/10.1093/jxb/50.330.29 CrossRefGoogle Scholar
  7. Aerts R, Boot RGA, van der Aart PJM (1991) The relation between above- and belowground biomass allocation patterns and competitive ability. Oecologia 87:551–559.  https://doi.org/10.1007/BF00320419 CrossRefPubMedGoogle Scholar
  8. Aerts R, Bakker C, Caluwe HD (1992) Root turnover as determinant of the cycling of C, N, and P in a dry heathland ecosystem. Biogeochemistry 15:175–190.  https://doi.org/10.1007/BF00002935 CrossRefGoogle Scholar
  9. Augusto L, Bakker MR, Morel C et al (2010) Is ‘grey literature’ a reliable source of data to characterize soils at the scale of a region? A case study in a maritime pine forest in southwestern France. Eur J Soil Sci 61:807–822.  https://doi.org/10.1111/j.1365-2389.2010.01286.x CrossRefGoogle Scholar
  10. Ballester A, Vieitez AM, Vieitez E (1982) Allelopathic potential of Erica vagans, Calluna vulgaris, and Daboecia cantabrica. J Chem Ecol 8:851–857.  https://doi.org/10.1007/BF00994785 CrossRefPubMedGoogle Scholar
  11. Bonanomi G, Legg C, Mazzoleni S (2005) Autoinhibition of germination and seedling establishment by leachate of Calluna vulgaris leaves and litter. Community Ecol 6:203–208CrossRefGoogle Scholar
  12. Brooker RW, Kikvidze Z (2008) Importance: an overlooked concept in plant interaction research. J Ecol 96:703–708.  https://doi.org/10.1111/j.1365-2745.2008.01373.x CrossRefGoogle Scholar
  13. Brooker R, Kikvidze Z, Pugnaire FI et al (2005) The importance of importance. Oikos 109:63–70.  https://doi.org/10.1111/j.0030-1299.2005.13557.x CrossRefGoogle Scholar
  14. Brooker RW, Maestre FT, Callaway RM et al (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34.  https://doi.org/10.1111/j.1365-2745.2007.01295.x CrossRefGoogle Scholar
  15. Buckland SM, Grime JP (2000) The effects of trophic structure and soil fertility on the assembly of plant communities: a microcosm experiment. Oikos 91:336–352.  https://doi.org/10.1034/j.1600-0706.2000.910214.x CrossRefGoogle Scholar
  16. Cahill J, James F, Casper BB (2000) Investigating the relationship between neighbor root biomass and belowground competition: field evidence for symmetric competition belowground. Oikos 90:311–320.  https://doi.org/10.1034/j.1600-0706.2000.900211.x CrossRefGoogle Scholar
  17. Casper BB, Jackson RB (1997) Plant competition underground. Annu Rev Ecol Syst 28:545–570CrossRefGoogle Scholar
  18. Chapin FS, Autumn K, Pugnaire F (1993) Evolution of suites of traits in response to environmental stress. Am Nat 142:S78–S92.  https://doi.org/10.2307/2462710 CrossRefGoogle Scholar
  19. Craine JM (2005) Reconciling plant strategy theories of Grime and Tilman. J Ecol 93:1041–1052.  https://doi.org/10.1111/j.1365-2745.2005.01043.x CrossRefGoogle Scholar
  20. Craine JM, Dybzinski R (2013) Mechanisms of plant competition for nutrients, water and light. Funct Ecol 27:833–840.  https://doi.org/10.1111/1365-2435.12081 CrossRefGoogle Scholar
  21. Craine JM, Fargione J, Sugita S (2005) Supply pre-emption, not concentration reduction, is the mechanism of competition for nutrients. New Phytol 166:933–940.  https://doi.org/10.1111/j.1469-8137.2005.01386.x CrossRefPubMedGoogle Scholar
  22. Delerue F (2013) Population dynamic of an understory legume (Ulex europaeus) in the context of forestry of maritime pine in the ‘Landes de Gascogne’. Proposition for a conceptual model. Ph.D. dissertation, University of Bordeaux, Bordeaux, France (in French)Google Scholar
  23. Delerue F, Gonzalez M, Atlan A et al (2013) Plasticity of reproductive allocation of a woody species (Ulex europaeus) in response to variation in resource availability. Ann For Sci 70:219–228.  https://doi.org/10.1007/s13595-012-0260-x CrossRefGoogle Scholar
  24. Delerue F, Gonzalez M, Michalet R et al (2015) Weak evidence of regeneration habitat but strong evidence of regeneration niche for a leguminous shrub. PLoS One 10:e0130886.  https://doi.org/10.1371/journal.pone.0130886 CrossRefPubMedPubMedCentralGoogle Scholar
  25. DeMalach N, Zaady E, Weiner J, Kadmon R (2016) Size asymmetry of resource competition and the structure of plant communities. J Ecol 104:899–910.  https://doi.org/10.1111/1365-2745.12557 CrossRefGoogle Scholar
  26. Demounen R (1979) An attempt to define and characterize ecophysiological levels in the forest of the Landes de Gascogne. Ph.D. dissertation, University of Grenoble-I, Grenoble, France (in French)Google Scholar
  27. Díaz S, Kattge J, Cornelissen JHC et al (2016) The global spectrum of plant form and function. Nature 529:167–171.  https://doi.org/10.1038/nature16489 CrossRefPubMedGoogle Scholar
  28. Díaz-Sierra R, Verwijmeren M, Rietkerk M et al (2017) A new family of standardized and symmetric indices for measuring the intensity and importance of plant neighbour effects. Methods Ecol Evol 8:580–591.  https://doi.org/10.1111/2041-210X.12706 CrossRefGoogle Scholar
  29. Domingo F, Villagarcı́a L, Brenner AJ, Puigdefábregas J (1999) Evapotranspiration model for semi- arid shrub-lands tested against data from SE Spain. Agric For Meteorol 95:67–84.  https://doi.org/10.1016/S0168-1923(99)00031-3 CrossRefGoogle Scholar
  30. Forey E, Touzard B, Michalet R (2010) Does disturbance drive the collapse of biotic interactions at the severe end of a diversity–biomass gradient? Plant Ecol 206:287–295.  https://doi.org/10.1007/s11258-009-9642-z CrossRefGoogle Scholar
  31. Gaudio N, Balandier P, Dumas Y, Ginisty C (2011a) Growth and morphology of three forest understorey species (Calluna vulgaris, Molinia caerulea and Pteridium aquilinum) according to light availability. For Ecol Manag 261:489–498.  https://doi.org/10.1016/j.foreco.2010.10.034 CrossRefGoogle Scholar
  32. Gaudio N, Balandier P, Philippe G et al (2011b) Light-mediated influence of three understorey species (Calluna vulgaris, Pteridium aquilinum, Molinia caerulea) on the growth of Pinus sylvestris seedlings. Eur J For Res 130:77–89.  https://doi.org/10.1007/s10342-010-0403-2 CrossRefGoogle Scholar
  33. Goldberg D, Novoplansky A (1997) On the relative importance of competition in unproductive environments. J Ecol 85:409–418.  https://doi.org/10.2307/2960565 CrossRefGoogle Scholar
  34. Grime JP (1977) Evidence for existence of 3 primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194CrossRefGoogle Scholar
  35. Grime JP (2001) Plant strategies, vegetation processes and ecosystem properties, 2nd edn. Wiley, ChichesterGoogle Scholar
  36. Grime JP (2007) Plant strategy theories: a comment on Craine (2005). J Ecol 95:227–230.  https://doi.org/10.1111/j.1365-2745.2006.01163.x CrossRefGoogle Scholar
  37. Güsewell S, Bollens U, Ryser P, Klötzli F (2003) Contrasting effects of nitrogen, phosphorus and water regime on first- and second-year growth of 16 wetland plant species. Funct Ecol 17:754–765.  https://doi.org/10.1111/j.1365-2435.2003.00784.x CrossRefGoogle Scholar
  38. Hartley MJ, Thaï PH (1982) Effects of pasture species, fertiliser, and grazing management on the survival of gorse seedlings. N Z J Exp Agric 10:193–196Google Scholar
  39. Hulme PD, Merrell BG, Torvell L et al (2002) Rehabilitation of degraded Calluna vulgaris (L.) hull-dominated wet heath by controlled sheep grazing. Biol Conserv 107:351–363.  https://doi.org/10.1016/S0006-3207(02)00073-3 CrossRefGoogle Scholar
  40. Jabot F, Pottier J (2012) A general modelling framework for resource-ratio and CSR theories of plant community dynamics. J Ecol 100:1296–1302.  https://doi.org/10.1111/j.1365-2745.2012.02024.x CrossRefGoogle Scholar
  41. Koyama A, Tsuyuzaki S (2013) Facilitation by tussock-forming species on seedling establishment collapses in an extreme drought year in a post-mined Sphagnum peatland. J Veg Sci 24:473–483.  https://doi.org/10.1111/j.1654-1103.2012.01474.x CrossRefGoogle Scholar
  42. Lortie CJ, Brooker RW, Choler P et al (2004) Rethinking plant community theory. Oikos 107:433–438.  https://doi.org/10.1111/j.0030-1299.2004.13250.x CrossRefGoogle Scholar
  43. Mallik AU, Pellissier F (2000) Effects of Vaccinium myrtillus on spruce regeneration: testing the notion of coevolutionary significance of allelopathy. J Chem Ecol 26:2197–2209.  https://doi.org/10.1023/A:1005528701927 CrossRefGoogle Scholar
  44. McConnaughay KDM, Coleman JS (1999) Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients. Ecology 80:2581–2593.  https://doi.org/10.2307/177242 CrossRefGoogle Scholar
  45. McLaughlin MJ, Malik KA, Memon KS, Idris M (1989) The role of phosphorus in nitrogen fixation in upland crops. In: Phosphorus Requirements for Sustainable Agriculture in Asia and Oceania. International Rice Research Institute (IRRI), Low Banos, Philippines, pp 295–305Google Scholar
  46. Michalet R, Brooker RW, Cavieres LA et al (2006) Do biotic interactions shape both sides of the humped-back model of species richness in plant communities? Ecol Lett 9:767–773.  https://doi.org/10.1111/j.1461-0248.2006.00935.x CrossRefPubMedGoogle Scholar
  47. Michalet R, Le Bagousse-Pinguet Y, Maalouf J-P, Lortie CJ (2014) Two alternatives to the stress-gradient hypothesis at the edge of life: the collapse of facilitation and the switch from facilitation to competition. J Veg Sci 25:609–613.  https://doi.org/10.1111/jvs.12123 CrossRefGoogle Scholar
  48. Morel C, Tunney P, Plenet D, Pellerin S (2000) Transfer of phosphate ions between soil and solution: perspectives in soil testing. J Environ Qual 29:50–59CrossRefGoogle Scholar
  49. Porte AJ, Samalens JC, Dulhoste R et al (2009) Using cover measurements to estimate aboveground understorey biomass in maritime pine stands. Ann For Sci 66:307.  https://doi.org/10.1051/forest/2009005 CrossRefGoogle Scholar
  50. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492.  https://doi.org/10.1046/j.1469-8137.2003.00704.x CrossRefGoogle Scholar
  51. Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301.  https://doi.org/10.1111/1365-2745.12211 CrossRefGoogle Scholar
  52. Rizopoulos D (2010) JM: an R package for the joint modelling of longitudinal and time-to-event data. J Stat Softw 35:1–33CrossRefGoogle Scholar
  53. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-0051-07-0. http://www.R-project.org/
  54. Shahzad T, Chenu C, Genet P et al (2015) Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol Biochem 80:146–155.  https://doi.org/10.1016/j.soilbio.2014.09.023 CrossRefGoogle Scholar
  55. Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. J Evol Biol 2:388–390.  https://doi.org/10.1046/j.1420-9101.1989.2050388.x Google Scholar
  56. Tilman D, Wedin D (1991) Dynamics of nitrogen competition between successional grasses. Ecology 72:1038–1049.  https://doi.org/10.2307/1940604 CrossRefGoogle Scholar
  57. Trichet P, Bakker MR, Augusto L et al (2009) Fifty years of fertilization experiments on pinus pinaster in southwest France: the importance of phosphorus as a fertilizer. For Sci 55:390–402Google Scholar
  58. Valladares F, Wright SJ, Lasso E et al (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936.  https://doi.org/10.1890/0012-9658(2000)081[1925:pprtlo]2.0.co;2 CrossRefGoogle Scholar
  59. Vázquez de Aldana BR, Geerts RHEM, Berendse F (1996) Nitrogen losses from perennial grass species. Oecologia 106:137–143.  https://doi.org/10.1007/BF00328592 CrossRefPubMedGoogle Scholar
  60. Wilson SD, Tilman D (1993) Plant competition and resource availability in response to disturbance and fertilization. Ecology 74:599–611CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.EA 4592, G&EBordeaux INPPessacFrance
  2. 2.EA 4592, G&EUniv. Bordeaux MontaignePessacFrance
  3. 3.UMR 1391 ISPAINRAVillenave d’OrnonFrance
  4. 4.UMR 1391 ISPABordeaux Science AgroGradignanFrance
  5. 5.UE Forêt PierrotonINRACestasFrance

Personalised recommendations