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Lichens Contribute to Open Woodland Stability in the Boreal Forest Through Detrimental Effects on Pine Growth and Root Ectomycorrhizal Development

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Abstract

In the boreal forest, open lichen woodlands have been described as an alternative stable state to closed-crown feather moss forest. In this study, we addressed the role of terricolous lichens in stabilizing open woodlands by hindering tree regeneration and/or growth. Based on field and greenhouse experiments, we compared germination and growth of jack pine (Pinus banksiana) on feather mosses (primarily Pleurozium schreberi) and lichens (primarily Cladonia stellaris), using bare mineral soil as a control. Drivers were investigated by (1) manipulating nutrient supply, (2) simulating shade of a closed canopy on the ground layer with the assumption this would mitigate lichen influence on pine growth, and (3) examining pine root ectomycorrhizal colonization and diversity as indicators of pine ability to take up nutrients. Total growth of 6-month-old greenhouse and 2–3-year-old field seedlings, as well as belowground growth of 2-year-old greenhouse seedlings, was significantly greater in moss than in lichen. Seed germination was not affected by ground cover type. Although field phosphorus and base cation availability was greater in mosses than in lichens, fertilization did not entirely compensate for the negative effects of lichens on pine growth in the greenhouse. Ground layer shading had no impact on pine growth. Lichens were associated with reduced abundance and modified composition of the root ectomycorrhizal community. By suggesting that terricolous lichens constitute a less favorable growth substrate than mosses for pine, our results support the hypothesis that lichens contribute to open woodland stability in the potentially closed-crown feather moss forest.

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References

  • Agerer R. 1987–2008. Colour Atlas of Ectomycorrhizae. Einhorn-Verlag Eduard Dietenberger, Schwäbisch Gmünd, Germany.

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic alignment search toom. Journal of Molecular Biology 215(3):403–10.

    Article  CAS  PubMed  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. Forêt Québec: Ministère des Ressources Naturelles.

    Google Scholar 

  • Bernier PY, Desjardins RL, Karimi-Zindashty Y, Worth D, Beaudoin Y, Luo Y, Wang S. 2011. Boreal lichen woodlands: a possible negative feedback to climate change in eastern North America. Agricultural and Forest Meteorology 151:521–8.

    Article  Google Scholar 

  • Bonan GB, Shugart HH. 1989. Environmental factors and ecological processes in boreal forests. Annual Review of Ecology and Systematics 20:1–28.

    Article  Google Scholar 

  • Borcard D, Gillet F, Legendre P. 2011. Numerical Ecology with R. New York: Springer.

    Book  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. Forest Ecology and Management 304:473–81.

    Article  Google Scholar 

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

    Google Scholar 

  • Cappellazzi J, Kimmerer R, Horton T. 2007. The influence of forest floor moss cover on ectomycorrhizal abundance in the central-western Oregon Cascade Mountains. Ph.D. Thesis. SUNY-ESF.

  • Carleton TJ, Read DJ. 1991. Ectomycorrhizas and nutrient transfer in conifer-feather moss ecosystems. Canadian Journal of Botany 69:778–85.

    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 74:310–15.

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crittenden P. 2000. Aspects of the ecology of mat-forming lichens. Rangifer 20:127–39.

    Article  Google Scholar 

  • DeLuca TH, 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 

  • Duchesne S, Sirois L. 1995. Phase initiale de régénération après feu des populations conifériennes subarctiques. Canadian Journal of Forest Research 25:307–18.

    Article  Google Scholar 

  • Fauria MM, Helle T, Niva A, Posio H, Timonen M. 2008. Removal of the lichen mat by reindeer enhances tree growth in a northern Scots pine forest. Canadian Journal of Forest Research 38:2981–93.

    Article  CAS  Google Scholar 

  • Fox J, Weisberg S. 2011. An R companion to applied regression. 2nd edn. Thousand Oaks: Sage.

    Google Scholar 

  • Fox J, Weisberg S. 2012. Bootstrapping regression models in R. An appendix to An R companion to applied regression. 2nd ed. Sage, Thousand Oaks, CA, US.

  • Fukasawa Y, Ando Y, Song Z. 2017. Comparison of fungal communities associated with spruce seedling roots and bryophyte carpets on logs in an old-growth subalpine coniferous forest in Japan. Fungal Ecology 30:122–31.

    Article  Google Scholar 

  • Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Molecular Ecology 2:113–18.

    Article  CAS  PubMed  Google Scholar 

  • Gauthier S, Bergeron Y, Simon JP. 1996. Effects of fire regime on the serotiny level of jack pine. Journal of Ecology 84:539–48.

    Article  Google Scholar 

  • Girard F, Payette S, Gagnon R. 2008. Rapid expansion of lichen woodlands within the closed-crown boreal forest zone over the last 50 years caused by stand disturbances in eastern Canada. Journal of Biogeography 35:529–37.

    Article  Google Scholar 

  • Girard F, Payette S, Gagnon R. 2011. Dendroecological analysis of black spruce in lichen-spruce woodlands of the closed-crown forest zone in eastern Canada. Ecoscience 18:279–94.

    Article  Google Scholar 

  • Gornall JL, Woodin SJ, Jónsdóttir IS, van der Wal R. 2011. Balancing positive and negative plant interactions: How mosses structure vascular plant communities. Oecologia 166(3):769–82.

    Article  PubMed  Google Scholar 

  • Greene DF, Splawinski T, Gauthier S, Bergeron Y. 2013. Seed abscission schedules and the timing of post-fire salvage of Picea mariana and Pinus banksiana. Forest Ecology and Management 303:20–4.

    Article  Google Scholar 

  • Haughian SR, Burton PJ. 2015. Microhabitat associations of lichens, feathermosses, and vascular plants in a caribou winter range, and their implications for understory development. Botany 93:221–31.

    Article  CAS  Google Scholar 

  • Hesketh M, Greene D, Pounden E. 2009. Early establishment of conifer recruits in the northern Rocky Mountains as a function of postfire duff depth. Canadian Journal of Forest Research 39(11):2059–64.

    Article  Google Scholar 

  • Hinsinger P, Bengough AG, Vetterlein D, Young IM. 2009. Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant and Soil 321:117–52.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Jasinski JP, Payette S. 2005. The creation of alternative stable states in the southern boreal forest, Quebec, Canada. Ecological Monographs 75:561–83.

    Article  Google Scholar 

  • Kershaw KA, Rouse WR. 1971. Studies on lichen-dominated systems. I. The water relations of Cladonia alpestris in spruce-lichen woodland in Northern Ontario. Canadian Journal of Botany 49:1389–99.

    Article  Google Scholar 

  • Lafleur PM, Schreader CP. 1994. Water loss from the floor of a subarctic forest. Arctic and Alpine Research 26:152–8.

    Article  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. Journal of Ecology 97:886–900.

    Article  CAS  Google Scholar 

  • Lesmerises R, Ouellet JP, St-Laurent MH. 2011. Assessing terrestrial lichen biomass using ecoforest maps: a suitable approach to plan conservation areas for forest-dwelling caribou. Canadian Journal of Forest Research 41:632–42.

    Article  Google Scholar 

  • Lindo Z, Gonzalez A. 2010. The bryosphere: an integral and influential component of the Earth’s biosphere. Ecosystems 13(4):612–27.

    Article  Google Scholar 

  • Molnár K, Farkas E. 2010. Current results on biological activities of lichen secondary metabolites: a review. Zeitschrift für Naturforschung 65:157–73.

    Article  PubMed  Google Scholar 

  • Nara K. 2006. Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytologist 169:169–78.

    Article  CAS  PubMed  Google Scholar 

  • Ohtonen R, Väre H. 1998. Vegetation composition determines microbial activities in a boreal forest soil. Microbial Ecology 36:328–35.

    Article  CAS  PubMed  Google Scholar 

  • Pacé M, Fenton NJ, Paré D, Bergeron Y. 2017a. Ground layer composition affects tree fine root biomass and soil nutrient availability in jack pine and black spruce forests under extreme drainage conditions. Canadian Journal of Forest Research 47:433–44.

    Article  CAS  Google Scholar 

  • Pacé M, Barrette M, Fenton NJ, Paré D, Bergeron Y. 2017b. Ground layer composition may limit the positive impact of precommercial thinning on stand productivity. Forest Science 63:559–68.

    Article  Google Scholar 

  • Payette S, Bhiry N, Delwaide A, Simard M. 2000. Origin of the lichen woodland at its southern range limit in eastern Canada: the catastrophic impact of insect defoliators and fire on the spruce-moss forest. Canadian Journal of Forest Research 30:288–305.

    Article  Google Scholar 

  • Peterson RL, Massicotte HB, Melville LH. 2004. Mycorrhizas: anatomy and cell biology. Ottawa: NRC Research Press.

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. 2014. nlme: linear and nonlinear mixed effects models. R package version 3.1-117.

  • Pinno BD, Errington RC, Thompson DK. 2013. Young jack pine and high severity fire combine to create potentially expansive areas of understocked forest. Forest Ecology and Management 310:517–22.

    Article  Google Scholar 

  • Robertson SJ, Tackaberry LE, Egger KN, Massicotte HB. 2006. Ectomycorrhizal fungal communities of black spruce differ between wetland and upland forests. Canadian Journal of Forest Research 36(4):972–85.

    Article  Google Scholar 

  • Sedia EG, Ehrenfeld JG. 2003. Lichens and mosses promote alternate stable plant communities in the New Jersey Pinelands. Oikos 100:447–58.

    Article  Google Scholar 

  • Sedia EG, Ehrenfeld JG. 2005. Differential effects of lichens, mosses and grasses on respiration and nitrogen mineralisation in soils of the New Jersey Pinelands. Oecologia 144:137–47.

    Article  PubMed  Google Scholar 

  • Sedia EG, Ehrenfeld JG. 2006. Differential effects of lichens and mosses on soil enzyme activity and litter decomposition. Biology and Fertility of Soils 43:177–89.

    Article  CAS  Google Scholar 

  • Sirois L. 1993. Impact of fire on Picea mariana and Pinus banksiana seedlings in subarctic lichen woodlands. Journal of Vegetation Science 4:795–802.

    Article  Google Scholar 

  • Soudzilovskaia NA, Bodegom PM, Cornelissen JH. 2013. Dominant bryophyte control over high-latitude soil temperature fluctuations predicted by heat transfer traits, field moisture regime and laws of thermal insulation. Functional Ecology 27(6):1442–54.

    Article  Google Scholar 

  • Steijlen I, Nilsson MC, Zackrisson O. 1995. Seed regeneration of Scots pine in boreal forest stands dominated by lichen and feather moss. Canadian Journal of Forest Research 25:713–23.

    Article  Google Scholar 

  • Struve DK. 2009. Tree establishment: A review of some of the factors affecting transplant survival and establishment. Arboriculture and urban forestry 35(1):10–13.

    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. The Bryologist 104:505–16.

    Article  Google Scholar 

  • Tremblay P, Boucher JF, Tremblay M, Lord D. 2013. Afforestation of boreal open woodlands: Early performance and ecophysiology of planted black spruce seedlings. Forests 4:433–54.

    Article  Google Scholar 

  • Venables WN, Ripley BD. 2002. Modern Applied Statistics with S. 4th edn. New York: Springer.

    Book  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 304:1629–33.

    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 120:1263–71.

    Article  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor JW. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, Eds. PCR Protocols: A guide to methods and applications. New York: Academic Press. p 315–22.

    Google Scholar 

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Acknowledgements

This work was financially supported by the Natural Sciences and Engineering Research Council of Canada, by the Fonds de Recherche du Québec—Nature et Technologies, the Chair in Sustainable Forest Management (NSERC-UQAT-UQAM), and a 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; 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; N. Sukdeo, D. Lachance, K. Egger and A. Séguin for their support in DNA analysis and manuscript review; and I. Lamarre for her linguistic revision.

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Authors and Affiliations

  1. Forest Research Institute, Université du Québec en Abitibi-Témiscamingue, Rouyn-Noranda, Québec, J9X 5E4, Canada

    Marine Pacé, Nicole J. Fenton & Yves Bergeron

  2. Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec, Québec, G1V 4C7, Canada

    Marine Pacé & David Paré

  3. Agriculture and Agri-Food Canada, Ottawa, Ontario, K1A 0C5, Canada

    Franck O. P. Stefani

  4. University of Northern British Columbia, Prince George, British Columbia, V2N 4Z9, Canada

    Hugues B. Massicotte & Linda E. Tackaberry

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  1. Marine Pacé
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Correspondence to Marine Pacé.

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Authors’ Contributions

MP, NF, DP, YB and HM conceived the main ideas and designed the methodology; MP, HM, FS and LT conceived and designed the analysis of ectomycorrhizal roots. MP collected and analyzed the data, and led the manuscript writing. All authors contributed critically to the drafts and gave final approval for publication.

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Open data portal of Canada, http://doi.org/10.23687/cc0010c9-b066-493e-9ee1-84c353e4c8c6.

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Pacé, M., Fenton, N.J., Paré, D. et al. Lichens Contribute to Open Woodland Stability in the Boreal Forest Through Detrimental Effects on Pine Growth and Root Ectomycorrhizal Development. Ecosystems 22, 189–201 (2019). https://doi.org/10.1007/s10021-018-0262-0

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