Advertisement

Resource competition and allelopathy in two peat mosses: implication for niche differentiation

  • Chao Liu
  • Zhao-Jun BuEmail author
  • Azim Mallik
  • Line Rochefort
  • Xue-Feng Hu
  • Zicheng Yu
Regular Article
  • 117 Downloads

Abstract

Aims

Separating the effect of resource competition from allelopathy in plants is challenging and it has never been attempted in closely related co-occurring bryophytes. In peatlands, peat mosses (Sphagnum spp.) show niche differentiation along water table level (WTL) gradient. Our aim was to evaluate whether the hummock species, S. magellanicum would be a winner at low WTL due to its allelopathic advantage and the hollow species, S. angustifolium would win by virtue of its superior competitive ability but not of allelopathy at high WTL due to dilution of its allelochemicals.

Methods

We used a nested, field experimental design, with two WTL treatments—low WTL (hummock habitat) and high WTL (hollow habitat)—and three different inter-specific interactions: 1) monoculture; 2) mixed culture without activated charcoal; and 3) mixed culture with activated charcoal added to the neighbor. We measured growth and biochemical traits of the two species and compared the index of relative neighbor effect on each other.

Results

We discovered a trade-off between biomass production (competitive outcome) and phenolic content (allelopathy) in these species. At low WTL, allelopathy of the hummock species is the main mechanism to suppress the hollow species, whereas at high WTL, competition is the main driver to suppress the hummock species.

Conclusions

Competitive advantage in Sphagnum is mediated by both resource competition and allelopathy of the co-occurring species through niche differentiation along a WTL gradient. Unlike vascular plants, Sphagnum mosses can serve as excellent model organisms in studying allelopathic interaction since they bypass the complexity of plant-soil interactions.

Keywords

Sphagnum Water table level Trade-off Niche separation Phenolics Phenotypic responses 

Notes

Acknowledgements

This study was funded by the National Nature Science Foundation of China (No. 41871046 and 41471043), the National Key Research and Development Project (No. 2016YFA0602301 and No. 2016YFC0500407) and Jilin Provincial Science and Technology Development Project (20190101025JH). Håkan Rydin commented on the manuscript. Azim Mallik contributed to this paper during his tenure as a Visiting Professor at the School of Geographical Sciences, Northeast Normal University, Changchun.

Supplementary material

11104_2019_4350_MOESM1_ESM.docx (174 kb)
ESM 1 (DOCX 174 kb)

References

  1. Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377–1380PubMedCrossRefGoogle Scholar
  2. Bazzaz FA, Nona RC, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67CrossRefGoogle Scholar
  3. Bengtsson F, Rydin H, Hájek T (2018) Biochemical determinants of litter quality in 15 species of Sphagnum. Plant Soil 425:161–176CrossRefGoogle Scholar
  4. Bragazza L (1997) Sphagnum niche diversification in two oligotrophic mires in the southern Alps of Italy. Bryologist 100(4):507–515CrossRefGoogle Scholar
  5. Brooker RW (2006) Plant-plant interactions and environmental change. New Phytol 171:271–284PubMedCrossRefGoogle Scholar
  6. Bu ZJ, Rydin H, Chen X (2011) Direct and interaction-mediated effects of environmental changes on peatland bryophytes. Oecologia 166(2):555–563PubMedCrossRefGoogle Scholar
  7. Bu ZJ, Chen X, Rydin H, Wang SZ, Ma JZ, Zeng J (2013a) Performance of four mosses in a reciprocal transplant experiment: indication for peatland succession in NE China. J Bryol 35(3):220–227CrossRefGoogle Scholar
  8. Bu ZJ, Zheng XX, Rydin H, Moore T, Ma JZ (2013b) Facilitation vs. competition: does inter-specific interaction affect drought responses in Sphagnum? Basic Appl Ecol 14(7):574–584CrossRefGoogle Scholar
  9. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2(8):436–443CrossRefGoogle Scholar
  10. Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Pallini L, Pugnair FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848PubMedCrossRefGoogle Scholar
  11. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427(6976):731–733PubMedCrossRefGoogle Scholar
  12. Chiapusio G, Jassey VJ, Hussain MI, Binet P (2013) Evidences of bryophyte allelochemical interactions: the case of Sphagnum. In: Cheema ZA, Farooq M, Wahid A (eds) Allelopathy. Springer, Berlin Heidelberg, pp 39–54CrossRefGoogle Scholar
  13. Chiapusio G, Jassey VEJ, Bellvert F, Comte G, Weston LA, Delarue F, Buttler A, Toussaint ML, Binet P (2018) Sphagnum species modulate their phenolic profiles and mycorrhizal colonization of surrounding Andromeda polifolia along peatland microhabitats. J Chem Ecol 44(12):1146–1157PubMedCrossRefGoogle Scholar
  14. Clymo RS, Hayward PM (1982) The ecology of Sphagnum. In: smith a.J.E. (ed.) bryophyte ecology, springer NetherlandsGoogle Scholar
  15. Darwin C (1859) On the origin of species by means of natural selection or the preservation of Favoured races in the struggle for life. John Murray, LondonGoogle Scholar
  16. Dong X, Dai LM, Shao GF (2005) Forest fire risk zone mapping from satellite images and GIS for Baihe forestry bureau, Jilin, China. J For Res 16(3):169–174CrossRefGoogle Scholar
  17. Emery N, Ewanchuk PJ, Bertness MD (2001) Competition and salt-marsh plant zonation: stress tolerators may be dominant competitors. Ecology 82(9):2471–2485CrossRefGoogle Scholar
  18. Ehlers BK, Charpentier A, Grøndahl E (2014) An allelopathic plant facilitates species richness in the Mediterranean garrigue. J Ecol 102:176–185CrossRefGoogle Scholar
  19. Eshghi S, Dokhani S, Tafazoli E, Rahemi M, Emam M (2007) Changes in carbohydrate contents in shoot tips, leaves and roots of strawberry (Fragaria× ananassa Duch.) during flower-bud differentiation. Sci Hortic 113:255–260CrossRefGoogle Scholar
  20. Fernandez C, Monnier Y, Santonja M, Gallet C, Weston LA, Prévosto B, Saunier A, Baldy V, Bousquet-Mélou A (2013) The impact of competition and allelopathy on the trade-off between plant defense and growth in two contrasting tree species. Front Plant Sci 7:594Google Scholar
  21. Gatti AB, Takao LK, Pereira VC, Ferreira AG, Lima MIS, Gualtieri SCJ (2014) Seasonality effect on the allelopathy of Cerrado species. Braz J Biol 74(3):64S–69SGoogle Scholar
  22. Gignac LD (1992) Niche structure, resource partitioning, and species interactions of mire bryophytes relative to climatic and ecological gradients in western Canada. Bryologist 95(4):406–418CrossRefGoogle Scholar
  23. Granath G, Strengbom J, Rydin H (2010) Rapid ecosystem shifts in peatlands: linking plant physiology and succession. Ecology 91:3047–3056PubMedCrossRefGoogle Scholar
  24. Grime JP (1979) Plant strategies and vegetation process [M]. John Wiley & Sons, New YorkGoogle Scholar
  25. Grime JP, MacKey JML (2002) The role of plasticity in resource capture by plants. Evol Ecol 16(3):299–307CrossRefGoogle Scholar
  26. He H, Wang H, Fang C, Lin Z, Yu Z, Lin W (2012) Separation of allelopathy from resource competition using rice/barnyardgrass mixed-culture. PLoS One 7(5):e37201PubMedPubMedCentralCrossRefGoogle Scholar
  27. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  28. Inderjit WDA, Karban R, Callaway RM (2011) The ecosystem and evolutionary contexts of allelopathy. Trends Ecol Evol 26:655–662PubMedCrossRefGoogle Scholar
  29. Inderjit WLA, Duke S (2005) Challenges, achievements and opportunities in allelopathy research. J Plant Interact 1:69–81CrossRefGoogle Scholar
  30. Ingerpuu N, Vellak K (2013) Growth depends on neighbors: experiments with three Sphagnum L. species. J Bryol 35:27–32CrossRefGoogle Scholar
  31. Johansson L (1983) Effects of AC in anther cultures. Physiol Mol Plant 59:397–403CrossRefGoogle Scholar
  32. John ET, Daniel JW, Mark DS (1983) Contrasting water relations of photosynthesis for two Sphagnum mosses. Ecology 64:1109–1115CrossRefGoogle Scholar
  33. Kong CH, Hu F (2001) Planting sensation and its application. China Agriculture Press, BeijingGoogle Scholar
  34. Koocheki A, Lalegani B, Hosseini S (2013) Ecological consequences of allelopathy. In: Cheema ZA, Farooq M, Wahid A (eds) Allelopathy. Springer Verlag, Berlin Heidelberg, pp 23–38CrossRefGoogle Scholar
  35. Laine AM, Juurola E, Hájek T, Tuittila ES (2011) Sphagnum growth and ecophysiology during mire succession. Oecologia 167:1115–1125PubMedCrossRefPubMedCentralGoogle Scholar
  36. Ma J-Z, Bu Z-J, Zheng X-X, Zeng J (2015) Shading enhances the competitive advantage of Sphagnum fallax in a simulation experiment. Mires Peat 16:1–17Google Scholar
  37. Mallik AU, Biswas SR, LC Siegwart C (2016) Belowground interactions between Kalmia angustifolia and Picea mariana: roles of competition, root exudates and ectomycorrhizal association. Plant Soil 403(1–2): 471–483CrossRefGoogle Scholar
  38. Mahall BE, Callaway RM (1992) Root communication mechanisms and intracommunity distributions of two Mojave Desert shrubs. Ecology 73(6):2145–2151CrossRefGoogle Scholar
  39. Mattson WJ, Julkunen-Tiitto R, Herms DA (2005) CO2 enrichment and carbon partitioning to phenolics: do plant responses accord better with the protein competition or the growth- differentiation balance models? Oikos 111(2):337–347CrossRefGoogle Scholar
  40. Mellegård H, Stalheim T, Hormazabal V, Granum PE, Hardy SP (2009) Antibacterial activity of sphagnum acid and other phenolic compounds found in Sphagnum papillosum against food-borne bacteria. Lett Appl Microbiol 49:85–90PubMedCrossRefGoogle Scholar
  41. Mensuali-Sodi A, Panizza M, Serra G, Tognoni F (1993) Involvement of AC in the modulation of abiotic and biotic ethylene levels in tissue-cultures. Sci Hortic 54:49–57CrossRefGoogle Scholar
  42. Meynet P, Hale SE, Davenport RJ, Cornelissen G, Breedveld GD, Werner D (2012) Effect of activated carbon amendment on bacterial community structure and functions in a PAH impacted urban soil. Environ Sci Technol 46:5057–5066PubMedPubMedCentralCrossRefGoogle Scholar
  43. Michael DJ, Anders PM (2002) A survey of the statistical power of research in behavioral ecology and animal behavior. Behav Ecol 14:438–445Google Scholar
  44. Michel P, Burritt DJ, Lee WG (2011) Bryophytes display allelopathic interactions with tree species in native forest ecosystems. Oikos 120:1272–1280CrossRefGoogle Scholar
  45. Montenegro G, Portaluppi MC, Salas FA, Diaz MF (2009) Biological properties of the Chilean native moss Sphagnum magellanicum. Biol Res 42:233–237PubMedCrossRefGoogle Scholar
  46. Mulligan RC, Gignac LD (2002) Bryophyte community structure in a boreal poor fen II: interspecific competition among five mosses. Can J Bot 80(4):330–339CrossRefGoogle Scholar
  47. Nilsson MC (1994) Separation of allelopathy and resource competition by the boreal dwarf shrub Empetrum hermaphroditum Hagerup. Oecologia 98:1–7PubMedCrossRefGoogle Scholar
  48. Novoplansky A (2009) Picking battles wisely: plant behaviour under competition. Plant Cell Environ 32(6):726–741PubMedCrossRefGoogle Scholar
  49. Parepa M, Schaffner U, Bossdorf O (2012) Sources and modes of action of invasive knotweed allelopathy: the effects of leaf litter and trained soil on the germination and growth of native plants. Neobiota 13:15–30CrossRefGoogle Scholar
  50. Piatkowski BT, Shaw AJ (2019) Functional trait evolution in Sphagnum peat mosses and its relationship to niche construction. New Phytol.  https://doi.org/10.1111/nph.15825 PubMedCrossRefGoogle Scholar
  51. Pierik R, Mommer L, Voesenek L-ACJ (2013) Molecular mechanisms of plant competition: neighbor detection and response strategies. Funct Ecol 27(4):841–853CrossRefGoogle Scholar
  52. Pinto GFS, Kolb RM (2016) Seasonality affects phytotoxic potential of five native species of Neotropical savanna. Botany 94:1–9CrossRefGoogle Scholar
  53. Prati D, Bossdorf O (2004) Allelopathic inhibition of germination by Alliaria petiolata (Brassicaceae). Am J Bot 91:285–288PubMedCrossRefGoogle Scholar
  54. Rasmussen S, Wolff C, Rudolph H (1995) Compartmentalization of phenolic constituents in Sphagnum. Phytochemistry 38:35–39CrossRefGoogle Scholar
  55. Rice EL (1984) Allelopathy, 2nd edn. Academic Press, New YorkGoogle Scholar
  56. Rudolph H, Samland J (1985) Occurrence and metabolism of Sphagnum acid in the cell walls of bryophytes. Phytochemistry 24:745–749CrossRefGoogle Scholar
  57. Rydin H (1993) Inter-specific competition between Sphagnum mosses on a raised bog. Oikos 66:413–423CrossRefGoogle Scholar
  58. Rydin H (1997) Competition among bryophytes. Adv Bryol 6:135–168Google Scholar
  59. Rydin H, Barber K (2001) Long-term and fine-scale coexistence of closely related species. Folia Geobot 36(1):53–61CrossRefGoogle Scholar
  60. San Emeterio L, Damgaard C, Canals RM (2007) Modelling the combined effect of chemical interference and resource competition on the individual growth of two herbaceous populations. Plant Soil 292(1):95–103CrossRefGoogle Scholar
  61. Schenk HJ (2006) Root competition: beyond resource depletion. J Ecol 94(4):725–739CrossRefGoogle Scholar
  62. Singleton VL, Rossi JA (1964) Colorimetry of total phenolics with phosphomolybdic- phosphotungstic acid reagents. Am J Enol Vitic1 6(3):144–158Google Scholar
  63. Soudzilovskaia NA, Graae BJ, Douma JC, Grau O, Milbau A, Shevtsova A, Wolters L, Cornelissen JHC (2011) How do bryophytes govern generative recruitment of vascular plants? New Phytol 190(4):1019–1031PubMedCrossRefGoogle Scholar
  64. Trewava A, Ballare CL, Trewavas AJ (2009) What is plant behaviour? Plant Cell Environ 32(6):606–616CrossRefGoogle Scholar
  65. Tsubota H, Kuroda A, Masuzaki H, Deguchi H (2006) Preliminary study on allelopathic activity of bryophytes under laboratory conditions using the sandwich method. J Hattori Bot Lab 100:517–525Google Scholar
  66. Turetsky MR, Crow SE, Evans RJ, Vitt DH, Wieder RK (2008) Trade-offs in resource allocation among moss species control decomposition in boreal peatlands. J Ecol 96:1297–1305CrossRefGoogle Scholar
  67. Van Breemen N (1995) How Sphagnum bogs down other plants. Trends Ecol Evol 10:270–275PubMedCrossRefGoogle Scholar
  68. Van Kleunen M, Rockle M, Stift M (2015) Admixture between native and invasive populations may increase invasiveness of Mimulus guttatus. Proc R Soc B-Biol Sci 282:20151487CrossRefGoogle Scholar
  69. Verhoeven JTA, Liefveld WM (1997) The ecological significance of organochemical compounds in Sphagnum. Acta Bot Neerl 46:117–130CrossRefGoogle Scholar
  70. Veteli TO, Mattson WJ, Niemelä P, Julkunen-Tiitto R, Kellomäki S, Kuokkanen K, Lavola A (2007) Do elevated temperature and CO2 generally have counteracting effects on phenolic phytochemistry of boreal trees? J Chem Ecol 33:287–296PubMedCrossRefGoogle Scholar
  71. Vitt DH, Slack NG (1984) Niche diversification of Sphagnum relative to environmental factors in northern Minnesota peatlands. Can J Bot 62(7):1409–1430CrossRefGoogle Scholar
  72. Weißhuhn K, Prati D (2009) Activated carbon may have undesired side effects for testing allelopathy in invasive plants. Basic Appl Ecol 10(2):500–507CrossRefGoogle Scholar
  73. Weidenhamer JD, Hartnett DC, Romeo JT (1989) Density-dependent phytotoxicity: distinguishing resource competition and allelopathic interference in plants. J Appl Ecol 26:613–624CrossRefGoogle Scholar
  74. Weston LA, Mathesius U (2013) Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol 39(2):283–297PubMedCrossRefGoogle Scholar
  75. Wright A, Schnitzer SA, Reich PB (2015) Daily environmental conditions determine the competition–facilitation balance for plant water status. J Ecol 103(3):648–656CrossRefGoogle Scholar
  76. Yamawo A (2015) Relatedness of neighboring plants alters the expression of indirect defense traits in an extrafloral nectary-bearing plant. Evol Biol 42(1):12–19CrossRefGoogle Scholar
  77. Zeng RS, Mallik AZ (2006) Selected ectomycorrhizal fungi of black spruce (Picea mariana) can detoxify phenolic compounds of Kalmia angustifolia. J Chem Ecol 32(7):1473–1489PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Key Laboratory of Geographical Processes and Ecological Security in Changbai Mountains, Ministry of Education, School of Geographical SciencesNortheast Normal UniversityChangchunChina
  2. 2.Department of Plant SciencesUniversité LavalQuébecCanada
  3. 3.State Environmental Protection Key Laboratory of Wetland Ecology and Vegetation Restoration, Institute for Peat and Mire ResearchNortheast Normal UniversityChangchunChina
  4. 4.Jilin Provincial Key Laboratory for Wetland Ecological Processes and Environmental Change in the Changbai MountainsChangchunChina
  5. 5.Department of BiologyLakehead UniversityThunder BayCanada
  6. 6.Department of Earth and Environmental SciencesLehigh UniversityBethlehemUSA

Personalised recommendations