Lichens Contribute to Open Woodland Stability in the Boreal Forest Through Detrimental Effects on Pine Growth and Root Ectomycorrhizal Development
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.
Keywords
Cladonia spp. ecosystem stability ectomycorrhiza feather moss ground cover jack pine lichen woodland pine regeneration stable alternative state terricolous lichenNotes
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.
Supplementary material
References
- Agerer R. 1987–2008. Colour Atlas of Ectomycorrhizae. Einhorn-Verlag Eduard Dietenberger, Schwäbisch Gmünd, Germany.Google Scholar
- Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic alignment search toom. Journal of Molecular Biology 215(3):403–10.CrossRefGoogle 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.CrossRefGoogle Scholar
- Bonan GB, Shugart HH. 1989. Environmental factors and ecological processes in boreal forests. Annual Review of Ecology and Systematics 20:1–28.CrossRefGoogle Scholar
- Borcard D, Gillet F, Legendre P. 2011. Numerical Ecology with R. New York: Springer.CrossRefGoogle 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.CrossRefGoogle 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.Google Scholar
- Carleton TJ, Read DJ. 1991. Ectomycorrhizas and nutrient transfer in conifer-feather moss ecosystems. Canadian Journal of Botany 69:778–85.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle Scholar
- Crittenden P. 2000. Aspects of the ecology of mat-forming lichens. Rangifer 20:127–39.CrossRefGoogle 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.CrossRefGoogle Scholar
- Duchesne S, Sirois L. 1995. Phase initiale de régénération après feu des populations conifériennes subarctiques. Canadian Journal of Forest Research 25:307–18.CrossRefGoogle 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.CrossRefGoogle 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.Google Scholar
- 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle Scholar
- Hinsinger P, Bengough AG, Vetterlein D, Young IM. 2009. Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant and Soil 321:117–52.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle Scholar
- Lafleur PM, Schreader CP. 1994. Water loss from the floor of a subarctic forest. Arctic and Alpine Research 26:152–8.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle Scholar
- Lindo Z, Gonzalez A. 2010. The bryosphere: an integral and influential component of the Earth’s biosphere. Ecosystems 13(4):612–27.CrossRefGoogle Scholar
- Molnár K, Farkas E. 2010. Current results on biological activities of lichen secondary metabolites: a review. Zeitschrift für Naturforschung 65:157–73.CrossRefGoogle Scholar
- Nara K. 2006. Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytologist 169:169–78.CrossRefGoogle Scholar
- Ohtonen R, Väre H. 1998. Vegetation composition determines microbial activities in a boreal forest soil. Microbial Ecology 36:328–35.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.Google Scholar
- 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.CrossRefGoogle 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.CrossRefGoogle Scholar
- Sedia EG, Ehrenfeld JG. 2003. Lichens and mosses promote alternate stable plant communities in the New Jersey Pinelands. Oikos 100:447–58.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle Scholar
- Venables WN, Ripley BD. 2002. Modern Applied Statistics with S. 4th edn. New York: Springer.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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