Skip to main content
SpringerLink
Log in

Belowground interactions between Kalmia angustifolia and Picea mariana: roles of competition, root exudates and ectomycorrhizal association

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Belowground competition and allelopathic interference of neighbouring plants play important roles in shaping plant performance. We assessed the effect of belowground interactions involving root competition, root exudates and ectomycorrhizal (ECM) association between Kalmia and black spruce on above- and belowground biomass increment and foliar nutrient content of black spruce seedlings. We predicted that root competition and root exudates of Kalmia would exert a negative impact on black spruce performance, while ECM in black spruce would exert positive impacts on its performance.

Methods

In a greenhouse experiment, using the neutral growth medium of peat-vermiculite, we planted Kalmia and black spruce seedling in pairs. We controlled root competition by placing fine wire mesh between the seedlings and applied benomyl fungicide to control ectomycorrhizae. We used activated charcoal to neutralize the potential allelopathic effects associated with root exudates. After 8 months, we evaluated the performance of black spruce seedlings in terms of biomass, abundance of ectomycorrhizal short roots and foliar nutrient concentrations. To determine treatment effects on soil processes, we also analysed soil pH, total phenols, C:N ratio and bioavailable nitrogen (NO3− and NH4+) at the end of the experiment.

Results

We found a significant effect of root competition on root-shoot ratio and biomass increment in black spruce seedlings, which achieved the highest root-shoot ratio and biomass increment when major root competition was controlled. Kalmia produced twice the root biomass than black spruce. Surprisingly, charcoal and benomyl treatments—which remove the effects of Kalmia allelopathy on black spruce and suppress ECM growth, respectively—had little or no significant effect on overall biomass of black spruce. In contrast, Kalmia biomass increment and root-shoot ratio were maximized in benomyl treatment. Soil pH and C:N ratio were significantly higher in free competition than root exclusion and benomyl treatments and with activated charcoal.

Conclusions

Kalmia root competition mediated by high root biomass is the predominant driver shaping neighbourhood interactions between Kalmia and black spruce, which in turn shape the performance of black spruce seedlings. Root exudates of Kalmia have a very weak effect on black spruce seedling growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abhilasha D, Quintana N, Vivanco J, Joshi J (2008) Do allelopathic compounds in invasive Solidago Canadensis s.l. restrain the native European flora? J Ecol 96:993–1001

    Article  Google Scholar 

  • Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681. doi:10.1111/j.1365-3040.2009.01926.x

    Article  CAS  PubMed  Google Scholar 

  • Baker AJM, Reeves RD, Hajar ASM (1994) Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl (Brassicaceae). New Phytol 127:61–68

    Article  CAS  Google Scholar 

  • Bending GD, Read JR (1996a) Effects of soluble polyphenol tannic acid on the activities of ectomycorrhizal fungi. Soil Biol Biochem 28:1595–1602

    Article  CAS  Google Scholar 

  • Bending GD, Read JR (1996b) Nitrogen mobilization from protein-polyphenol complex by ericoid and ectomycorrhizal fungi. Soil Biol Biochem 28:1603–1612

    Article  CAS  Google Scholar 

  • Bever JD, Platt TG, Morton ER (2012) Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbial 66:265–283. doi:10.1146/annurev-micro-092611-150107

    Article  CAS  Google Scholar 

  • Bloom R, Mallik AU (2006) Relationship between ericaceous vegetation and soil nutrient status in a post-fire Kalmia angustifolia-black spruce chronosequence. Plant Soil 289:211–226

    Article  CAS  Google Scholar 

  • Bradley RL, Fyles JW (1995) Growth of paper birch (Betula papyrifera) seedlings increases soil available C and microbial acquisition of soil-nutrients. Soil Biol Biochem 27:1565–1571

    Article  CAS  Google Scholar 

  • Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cahill JF (2003) Lack of relationship between belowground competition and allocation to roots in 10 grassland species. J Ecol 91:532–540

    Article  Google Scholar 

  • Cairney JWG, Mehrag AA (2003) Ericoidmycorrhiza: a partnership that exploits harsh edaphic conditions. Eur J Soil Sci 54:735–740

    Article  Google Scholar 

  • Callaway RM (2002) The detection of neighbors by plants. TREE 17:104–105

    Google Scholar 

  • Callaway RM, Aschehoug ET (2000) Invasive plants versus their new neighbors: a mechanism for exotic invasion. Science 290:521–523

    Article  CAS  PubMed  Google Scholar 

  • Carter MR (ed.) (1993) Soil sampling and methods of analysis. CRC Press, Boca Raton, pp 25–27

  • Cipollini D, Rigsby CM, Barto EK (2012) Microbes as targets and mediators of allelopathy in plants. J Chem Ecol 38:714–727

    Article  CAS  PubMed  Google Scholar 

  • Cumming J, Weinstein L (1990) Aluminum-mycorrhizal interactions in the physiology of pitch pine seedlings. Plant Soil 125:7–18

    Article  CAS  Google Scholar 

  • Damman AWH (1971) Effects of vegetation changes on the fertility of a Newfoundland forest site. Ecol Monogr 41:253–270

    Article  Google Scholar 

  • Development Core Team R (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Fitter A (2005) Darkness visible: reflections on underground ecology. J Ecol 93:231–243

    Article  Google Scholar 

  • Gersani M, Brown JS, O’Brien EE, Maina GM, Abramsky Z (2001) Tragedy of the commons as a result of root competition. J Ecol 89:660–669

    Article  Google Scholar 

  • Grenon F, Bradley RL, Joanisse G, Titus BD, Prescotte CF (2004) Mineral availability for conifer growth following clearcutting: responsive versus non-responsive ecosystems. For Ecol Manag 188:305–316

    Article  Google Scholar 

  • Inderjit, Callaway RM (2003) Experimental designs for the study of allelopathy. Plant Soil 256:1–11

    Article  CAS  Google Scholar 

  • Inderjit, Dakshini KMM (1994) Allelopathic effects of Pluchea lanceolata (Asteraceae) on characteristics of four soils and mustard and tomato growth. Am J Bot 81:799–804

    Article  Google Scholar 

  • Inderjit, Mallik AU (1996) The nature of interference potential of Kalmia angustifolia. Can J For Res 26:1899–1904

    Article  Google Scholar 

  • Inderjit, Mallik AU (2002) Can Kalmia angustifolia interference to black spruce (Picea mariana) be explained by allelopathy? For Ecol Manag 160:75–84

    Article  Google Scholar 

  • Inderjit, Weston LA (2003) Root exudates: an overview. In: de Kroon H, Visser EJW (eds) Root ecology. Springer, Berlin, pp 235–255

    Chapter  Google Scholar 

  • Joanisse GD, Bradley RL, Preston CM, Bending GD (2009) Sequestration of soil nitrogen as tannin-protein complexes may improve the competitive ability of sheep laurel (Kalmia angustifolia) relative to black spruce (Picea mariana). New Phytol 181:187–198

    Article  CAS  PubMed  Google Scholar 

  • Karla YP, Maynard DG (1991) Methods manual for forest soil and plant analysis. Forestry Canada, Edmonton, pp 62–68

    Google Scholar 

  • Lau JA, Puliafico KP, Kopshever JA, Steltze H, Jarvis EP, Schwarzländer M, Strauss SY, Hufbauer RA (2008) Inference of allelopathy is complicated by effects of activated carbon on plant growth. New Phytol 178:412–423

    Article  CAS  PubMed  Google Scholar 

  • Leak JR, Read DJ (1989) The effect of phenolic compounds on nitrogen mobilization by ericoid mycorrhizal system. Agric Ecosyst Environ 29:225–236

    Article  Google Scholar 

  • LeBel P, Thiffault N, Bradley RL (2008) Kalmia removal increases nutrient supply and growth of black spruce seedlings: an effect fertilizer cannot emulate. For Ecol Manag 256:1780–1784

    Article  Google Scholar 

  • Lorenzo P, Rodríguez-Echeverría S, Freitas H (2013) No allelopathic effect of the invader Acacia dealbata on the potential infectivity of arbuscular mycorrhizal fungi from native soils. Eur J Soil Biol 58:42–44

    Article  Google Scholar 

  • Mallik AU (1987) Allelopathic potential of Kalmia angustifolia to black spruce. For Ecol Manag 20:43–51

    Article  Google Scholar 

  • Mallik AU (1993) Ecology of a forest weed of Newfoundland: vegetative regeneration strategies of Kalmia angustifolia. Can J Bot 71:161–166

    Article  Google Scholar 

  • Mallik AU (2003) Conifer regeneration problems in boreal and temperate forests with ericaceous understorey: role of disturbance, seedbed limitation and keystone species change. Crit Rev Plant Sci 22:341–366

    Article  Google Scholar 

  • Mallik AU, Kravchenko D (2016) Black spruce (Picea mariana) restoration in Kalmia heath by scarification and microsite mulching. For Ecol Manag 362:10–19

    Article  Google Scholar 

  • Mallik AU, Bloom RG, Whisenant SG (2010) Seedbed filter controls post-fire succession. Basic Appl Ecol 11:170–181

    Article  Google Scholar 

  • Michelsen A, Graglia E, Schmidt IK, Jonasson S, Sleep D, Quarmby C (1999) Differential responses of grass and a dwarf shrub to long-term changes in soil microbial biomass C, N and P following factorial addition of NPK fertilizer, fungicide and labile carbon to a heath. New Phytol 143:523–538

    Article  Google Scholar 

  • Molina R, Amaranthus M (1990) Rhizosphere biology: ecological linkages between soil process, plant growth and community dynamics. Paper presented at the Symposium on Management and Productivity of Westem-Montane Forest Soils, Boise, ID, April 10–12, 1990

  • Nilsson LO, Wallander H (2003) The production of external mycelium by ectomycorrhizal fungi on a Norway spruce forest was reduced in response to nitrogen fertilization. New Phytol 158:409–416

    Article  Google Scholar 

  • Perotto S, Martino E, Abba S, Vallino M (2012) Genetic diversity and functional aspects of ericoid mycorrhizal fungi. In: Hock B (ed) Fungal associations, 2nd edn. Springer, Berlin, pp 255–277

    Chapter  Google Scholar 

  • Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water. Aust J Plant Physiol 27:595–607

    Article  CAS  Google Scholar 

  • Read DJ, Leake JR, Perez-Moreno J (2004) Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Bot 82:1243–1263

    Article  CAS  Google Scholar 

  • Robinson D, Davidson H, Trinder C, Brooker B (2010) Root-shoot growth responses during interspecific competition quantified using allometric modelling. Ann Bot 106:921–926

    Article  PubMed  PubMed Central  Google Scholar 

  • Schenk HJ (2006) Root competition: beyond resource depletion. J Ecol 94(4):725–739

    Article  Google Scholar 

  • Shaw G, Read DJ (1989) The biology of mycorrhiza in the Ericaceae XIV: effects of iron and aluminium on the activity of acid phosphatase in the ericoid endophyte Hymenoscyphus ericae (Read) Korf and Kernan. New Phytol 113:529–533

    Article  CAS  Google Scholar 

  • Siegwart-Collier LC, Mallik AU (2010) Does post-fire abiotic habitat filtering create divergent plant communities in black spruce forests of eastern Canada? Oecologia 164(2):465–477

    Article  Google Scholar 

  • Summerbell RC (1988) Benomyl—tolerant microfungi associated with mycorrhiza of black pruce. Can J Bot 66:553–557

    Article  CAS  Google Scholar 

  • Veiga RSL, Faccio A, Genre A, Pieterse CMJ, Bonfante P, Van Der Heijden MGA (2012) Arbuscular mycorrhizal fungi reduce growth and infect roots of the non-host plant Arabidopsis thaliana. Plant Cell Environ 36:1926–1937

    Google Scholar 

  • Walker GR, Mallik AU (2009) Black spruce reforestation in Kalmia heath: seedling response to forest floor mixing and mycorrhizal inoculation with Paxillus involutus. Can J For Res 39:2007–2020

    Article  CAS  Google Scholar 

  • Wallstedt A, Coughlan A, Munson A, Nilsson M, Margolis H (2002) Mechanisms of interaction between Kalmia angustifolia cover and Picea mariana seedlings. Can J For Res 32(11):2022–2031

    Article  Google Scholar 

  • Wardle DA, Zackrisson O, Nilsson M-C (1998) Charcoal effect in boreal forests: mechanism and ecological consequences. Oecologia 115(3):419–426

    Article  Google Scholar 

  • Weißhuhn K, Prati D (2009) Activated carbon may have undesired side effects for testing allelopathy in invasive plants. Basic Appl Ecol 10(2):500–507

    Article  Google Scholar 

  • Wurst S, Vender V, Rillig MC (2010) Testing for allelopathic effects in plant competition: does activated carbon disrupt plant symbioses? Plant Ecol 211:19–26

    Article  Google Scholar 

  • Yamasaki SH, Fyles JW, Egger KN, Titus BD (1998) The effect of Kalmia angustifolia on the growth, nutrition, and ectomycorrhizal symbiont community of black spruce. For Ecol Manag 105:197–207

    Article  Google Scholar 

  • Zabinski CA, Quinn L, Callaway RM (2002) Phosphorus uptake, not carbon transfer, explains arbuscular mycorrhizal enhancement of Centaurea maculosa in the presence of native grassland species. Funct Ecol 16:758–765

    Article  Google Scholar 

  • Zackrisson O, Nilsson M-C, Wardle DA (1996) Key ecological function of charcoal from wildfire in the boreal forest. Oikos 77:10–19

    Article  Google Scholar 

  • Zeng R-S, Mallik AU (2006) Selected ectomycorrhizal fungi of black spruce can detoxify Kalmia angustifolia phenolic compounds. J Chem Ecol 32:1473–1489

    Article  CAS  PubMed  Google Scholar 

  • Zhu H, Mallik AU (1994) Interactions between Kalmia and black spruce: isolation and identification of allelopathic compounds. J Chem Ecol 20(2):407–421

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by a Natural Science and Engineering Council (NSERC) Discovery Grant of Canada awarded to AUM (grant no. RGPIN/46483-2009). A sabbatical leave from Lakehead University enabled this author to work on the paper. We thank the two anonymous reviewers and the handling editor for their helpful comments on earlier versions of the manuscript.

Author information

Authors and Affiliations

  1. Department of Biology, Lakehead University, Thunder Bay, ON, Canada, P7B 5E1

    Azim U. Mallik, Shekhar R. Biswas & Laura C. Siegwart Collier

Authors
  1. Azim U. Mallik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shekhar R. Biswas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura C. Siegwart Collier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Azim U. Mallik.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Responsible Editor: Leslie A. Weston.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 37 kb)

ESM 2

(DOCX 40 kb)

ESM 3

(DOCX 42 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mallik, A.U., Biswas, S.R. & Collier, L.C.S. Belowground interactions between Kalmia angustifolia and Picea mariana: roles of competition, root exudates and ectomycorrhizal association. Plant Soil 403, 471–483 (2016). https://doi.org/10.1007/s11104-016-2819-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-2819-z

Keywords

Search

Navigation