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Effects of lichen, Sphagnum spp. and feather moss leachates on jack pine and black spruce seedling growth

Abstract

Aim

The main objective of this study was to evaluate the influence of leachates from three typical boreal forest ground layers on young tree growth and to explore the linkages between the chemical composition of the leachates, tree growth, the allocation between belowground and aboveground parts, and ectomycorrhizal colonization.

Methods

An original 6-month greenhouse experiment was set up to investigate (i) the effects of lichen (Cladonia spp.) and feather moss (Pleurozium schreberii [Brid.] Mitt.) leachates on jack pine (Pinus banksiana Lamb.) growth and (ii) the effects of feather moss and Sphagnum spp. leachates on black spruce (Picea mariana [Mill.] B.S.P.) growth.

Results

Belowground growth and root allocation was reduced by lichen leachates in 2-year-old pine seedlings, while the impact was significant on both below- and aboveground growth in 6-month-old pine seedlings. A substance having the same migration time as usnic acid was detected in the lichen leachates by high-performance liquid chromatography. Sphagnum spp. and feather moss leachates were not found to have any effect on black spruce seedling growth, despite a higher supply of dissolved inorganic N in the feather moss leachates compared to the leachates of Sphagnum spp. and the control.

Conclusions

These results demonstrate that ground layer composition plays a crucial role in shaping the plant community in boreal ecosystems by influencing the chemical composition of the soil solution. They suggest that chemical interference may be another mechanism by which lichens promote the self-perpetuation of open woodlands in the closed-crown boreal forest.

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References

  • Agerer R (1987–2008) Colour atlas of Ectomycorrhizae. Einhorn-Verlag Eduard Dietenberger, Schwäbisch Gmünd

  • Basile A, Sorbo S, Lopez-Saez JA, Cobianchi RC (2003) Effects of seven pure flavonoids from mosses on germination and growth of Tortula muralis HEDW. (Bryophyta) and Raphanus sativus L.(Magnoliophyta). Phytochemistry 62:1145–1151

    Article  CAS  Google Scholar 

  • Bergeron JF, Grondin P, Blouin J (1999) Rapport de classification écologique du sous-domaine bioclimatique de la pessière à mousses de l'ouest. Ministère des ressources naturelles, Forêt Québec

  • Bisbee KE, Gower ST, Norman JM, Nordheim EV (2001) Environmental controls on ground cover species composition and productivity in a boreal black spruce forest. Oecologia 129:261–270

    Article  Google Scholar 

  • Boudreault C, Zouaoui S, Drapeau P, Bergeron Y, Stevenson S (2013) Canopy openings created by partial cutting increase growth rates and maintain the cover of three Cladonia species in the Canadian boreal forest. For Ecol Manag 304:473–481

    Article  Google Scholar 

  • Brown RT, Mikola P (1974) The influence of fruticose soil lichens upon the mycorrhizae and seedling growth of forest trees. Acta Forest Fennica 141:1-23

  • Cardarelli M, Serino G, Campanella L, Ercole P, Nardone FDC, Alesiani O, Rossiello F (1997) Antimitotic effects of usnic acid on different biological systems. Cell Mol Life Sci 53:667–672

    Article  CAS  Google Scholar 

  • Carleton TJ, Read DJ (1991) Ectomycorrhizas and nutrient transfer in conifer – feather moss ecosystems. Can J Bot 69:778–785

    Article  Google Scholar 

  • Chapin F, Oechel W, Cleve KV, Lawrence W (1987) The role of mosses in the phosphorus cycling of an Alaskan black spruce forest. Oecologia 74:310–315

    Article  Google Scholar 

  • Chiapusio G, Jassey VE, Hussain MI, Binet P (2013) Evidences of bryophyte Allelochemical interactions: the case of Sphagnum. Allelopathy, pp. 39–54. Springer

  • Clymo RS (1963) Ion exchange in Sphagnum and its relation to bog ecology. Ann Bot 27:309–324

    Article  CAS  Google Scholar 

  • Cornelissen JHC, Lang SI, Soudzilovskaia NA, During HJ (2007) Comparative cryptogam ecology: a review of bryophyte and lichen traits that drive biogeochemistry. Ann Bot 99:987–1001

    Article  CAS  Google Scholar 

  • Crittenden P (2000) Aspects of the ecology of mat-forming lichens. Rangifer 20:127–139

    Article  Google Scholar 

  • DeLuca T, Zackrisson O, Bergman I, Hörnberg G (2013) Historical land use and resource depletion in spruce-Cladina forests of subarctic Sweden. Anthropocene 1:14–22

    Article  Google Scholar 

  • Dommanget F, Evette A, Spiegelberger T, Gallet C, Pacé M, Imbert M, Navas ML (2014) Differential allelopathic effects of Japanese knotweed on willow and cottonwood cuttings used in riverbank restoration techniques. J Environ Manag 132:71–78

    Article  Google Scholar 

  • Fenton N, Légaré S, Bergeron Y, Paré D (2006) Soil oxygen within boreal forests across an age gradient. Can J Soil Sci 86:1–9

    Article  CAS  Google Scholar 

  • Fox J, Weisberg S (2012) Bootstrapping regression models in R. an appendix to an R companion to applied regression, 2nd edn. Sage, Thousand Oaks

    Google Scholar 

  • Fox J, Weisberg S, Adler D, Bates D, Baud-Bovy G, Ellison S, Firth D, Friendly M, Gorjanc G, Graves S (2016) Package ‘car’. An R Companion to Applied Regression, Third edition. Sage, Thousand Oaks.  https://socialsciences.mcmaster.ca/jfox/Books/Companion/.

  • Gornall JL, Woodin SJ, Jonsdottir IS, van der Wal R (2011) Balancing positive and negative plant interactions: how mosses structure vascular plan communities. Oecologia 166(3):769–782

    Article  Google Scholar 

  • Gross J, Ligges U (2015) Nortest: tests for normality. R package version 1.0–4. https://CRAN.R-project.org/package=nortest

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

    Article  CAS  Google Scholar 

  • Ingleby K, Mason PA, Last FT, Fleming LV (1990) Identification of Ectomycorrhizae. Institute of Terrestrial Ecology, Natural Environment Research Council, London

    Google Scholar 

  • Kytöviita M-M, Stark S (2009) No allelopathic effect of the dominant forest-floor lichen Cladonia stellaris on pine seedlings. Funct Ecol 23:435–441

    Article  Google Scholar 

  • Lafleur B, Paré D, Fenton NJ, Bergeron Y (2011) Growth and nutrition of black spruce seedlings in response to disruption of Pleurozium and Sphagnum moss carpets in boreal forested peatlands. Plant Soil 345:141–153

    Article  CAS  Google Scholar 

  • Lang SI, Cornelissen JH, Klahn T, Van Logtestijn RS, Broekman R, Schweikert W, Aerts R (2009) An experimental comparison of chemical traits and litter decomposition rates in a diverse range of subarctic bryophyte, lichen and vascular plant species. J Ecol 97:886–900

    Article  CAS  Google Scholar 

  • Lavoie M, Paré D, Bergeron Y (2007a) Quality of growth substrates of post-disturbed lowland black spruce sites for black spruce (Picea mariana) seedling growth. New For 33:207–216

    Article  Google Scholar 

  • Lavoie M, Paré D, Bergeron Y (2007b) Relationships between microsite type and the growth and nutrition of young black spruce on post-disturbed lowland black spruce sites in eastern Canada. Can J For Res 37:62–73

    Article  CAS  Google Scholar 

  • Lett S, Nilsson M-C, Wardle DA, Dorrepaal E (2017) Bryophyte traits explain climate-warming effects on tree seedling establishment. J Ecol 105:496–506

    Article  Google Scholar 

  • Michel P, Burritt DJ, Lee WG (2011) Bryophytes display allelopathic interactions with tree species in native forest ecosystems. Oikos 120:1272–1280

    Article  Google Scholar 

  • Molnár K, Farkas E (2010) Current results on biological activities of lichen secondary metabolites: a review. Z Naturforsch C 65:157–173

    Article  Google Scholar 

  • Nybakken L, Julkunen-Tiito R (2006) UV-B induces usnic acid in reindeer lichens. Lichenologist 38(5):477–485

    Article  Google Scholar 

  • Pacé M, Fenton NJ, Paré D, Bergeron Y (2017) Ground layer composition affects tree fine root biomass and soil nutrient availability in jack pine and black spruce forests under extreme drainage conditions. Can J For Res 47(4):433–444

  • Pacé M, Fenton NJ, Paré D, Bergeron Y (2018) Differential effects of feather mosses and Sphagnum spp. on black spruce germination and growth. For Ecol Manag 415:10–18

    Article  Google Scholar 

  • Pacé M, Fenton NJ, Paré D, Stefani FOP, Massicotte HB, Tackaberry LE, Bergeron Y (2019) Lichens contribute to open woodland stability in the boreal forest through detrimental effects on pine growth and root ectomycorrhizal development. Ecosystems 22(1):189–201

    Article  CAS  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1–117. http://CRAN.R-project.org/package=nlme

  • Pizňak M, Bačkor M (2019) Lichens affect boreal forest ecology and plant metabolism. S Afr J Bot 124:530–539

    Article  CAS  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ripley B, Venables B, Bates DM, Hornik K, Gebhardt A, Firth D, Ripley MB (2013) Package ‘MASS’. CRAN Repository http://cran.r-project.org/web/packages/MASS/MASS.pdf

  • Robertson SJ, Tackaberry LE, Egger KN, Massicotte HB (2006) Ectomycorrhizal fungal communities of black spruce differ between wetland and upland forests. Can J For Res 36(4):972–985

    Article  Google Scholar 

  • Romagni JG, Meazza G, Nanayakkara DNP, Dayan FE (2000) The phytotoxic lichen metabolite, usnic acid, is a potent inhibitor of plant p-hydroxyphenyl-pyruvate dioxygenase. Fed Eur Biochem Soc Lett 480:301–305

    Article  CAS  Google Scholar 

  • Sedia EG, Ehrenfeld JG (2003) Lichens and mosses promote alternate stable plant communities in the New Jersey pinelands. Oikos 100:447–458

    Article  Google Scholar 

  • Simard M, Lecomte N, Bergeron Y, Bernier PY, Paré D (2007) Forest productivity decline caused by successional paludification of boreal soils. Ecol Appl 17:1619–1637

    Article  Google Scholar 

  • Soudzilovskaia NA, Cornelissen JHC, During HJ, van Logtestijn RSP, Lang SI, Aerts R (2010) Similar cation exchange capacities among bryophyte species refute a presumed mechanism of peatland acidification. Ecology 91:2716–2726

    Article  CAS  Google Scholar 

  • Stark S, Hyvärinen M (2003) Are phenolics leaching from the lichen Cladina stellaris sources of energy rather than allelopathic agents for soil microorganisms? Soil Biol Biochem 35:1381–1385

    Article  CAS  Google Scholar 

  • Stark S, Kytöviita MM, Neumann AB (2007) The phenolic compounds in Cladonia lichens are not antimicrobial in soils. Oecologia 152:299–306

    Article  Google Scholar 

  • Sulyma R, Coxson DS (2001) Microsite displacement of terrestrial lichens by feather moss mats in late seral pine-lichen woodlands of north-Central British Columbia. Bryologist 104:505–516

    Article  Google Scholar 

  • Viard-Crétat F, Gallet C, Lefebvre M, Lavorel S (2009) A leachate a day keeps the seedlings away: mowing and the inhibitory effects of Festuca paniculata in subalpine grasslands. Ann Bot 103:1271–1278

    Article  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van Der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  CAS  Google Scholar 

  • Wheeler JA, Hermanutz L, Marino PM (2011) Feathermoss seedbeds facilitate black spruce seedling recruitment in the forest-tundra ecotone (Labrador, Canada). Oikos 120:1263–1271

    Article  Google Scholar 

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Acknowledgments

This work was financially supported by the Natural Sciences and Engineering Research Council of Canada (NSERC), the Fonds de Recherche du Québec - Nature et Technologies, the Chair in Sustainable Forest Management (NSERC-Université du Québec en Abitibi-Temiscamingue, UQAT-Université du Québec à Montréal) and an NSERC Collaborative Research and Development UQAT-Tembec-Chantiers Chibougamau grant. We thank D. Labrecque (Ministère des forêts, de la Faune et des Parcs du Québec) for seed and seedling supply; E. Pouliot, F. Pelletier, S. Dagnault, F. Michaud and J. Morissette for their help and advice in the greenhouse; H. Massicotte and S. Gauthier for their advice and support; J. Beguin for his support in statistical analyses; B. Gadet, L. Auger, S. Laflèche, R. Plusquellec and R. Julien for their help and advice in the field; S. Rousseau for soil analysis; and M. Cusson for his help and advice regarding HPLC analysis.

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Correspondence to M. Pacé.

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Data access

The datasets generated during and analysed during the current study are available in the Data inventory of Natural Resources Canada, https://doi.org/10.23687/0f3008be-d40e-4179-a2cc-cfaccf3720a1

Responsible Editor: François Teste.

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Pacé, M., Paré, D., Fenton, N.J. et al. Effects of lichen, Sphagnum spp. and feather moss leachates on jack pine and black spruce seedling growth. Plant Soil 452, 441–455 (2020). https://doi.org/10.1007/s11104-020-04587-0

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  • DOI: https://doi.org/10.1007/s11104-020-04587-0

Keywords

  • Allelopathy
  • Forest productivity
  • Ground layer
  • Regeneration failure
  • Soil solution
  • Usnic acid