Abstract
For tree seedlings in boreal forests, ectomycorrhizal (EM) fungal networks may promote, while root competition may impede establishment. Thus, disruption to EM fungal networks may decrease seedling establishment owing to the loss of positive interactions among neighbors. Widespread tree mortality can disrupt EM networks, but it is not clear whether seedling establishment will be limited by the loss of positive interactions or increased by the loss of negative interactions with surrounding roots. Depending upon the relative influence of these mechanisms, widespread tree mortality may have complicated consequences on seedling establishment, and in turn, the composition of future forests. To discern between these possible outcomes and the drivers of seedling establishment, we determined the relative importance of EM fungal networks, root presence, and the bulk soil on the establishment of lodgepole pine and white spruce seedlings along a gradient of beetle-induced tree mortality. We manipulated seedling contact with EM fungal networks and roots through the use of mesh-fabric cylinders installed in soils of lodgepole pine forests experiencing a range of overstorey tree mortality caused by mountain pine beetle. Lodgepole pine seedling survival was higher with access to EM fungal networks in undisturbed pine forests in comparison with that in beetle-killed stands. That is, overstorey tree mortality shifted fungal networks from being a benefit to a cost on seedling survival. In contrast, overstorey tree mortality did not change the relative strength of EM fungal networks, root presence and the bulk soil on survival and biomass of white spruce seedlings. Furthermore, the relative influence of EM fungal networks, root presence, and bulk soils on foliar N and P concentrations was highly contingent on seedling species and overstorey tree mortality. Our results highlight that following large-scale insect outbreak, soil-mediated processes can enable differential population growth of two common conifer species, which may result in species replacement in the future.
![](https://cdn.statically.io/img/media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00572-020-00940-4/MediaObjects/572_2020_940_Fig1_HTML.png)
![](https://cdn.statically.io/img/media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00572-020-00940-4/MediaObjects/572_2020_940_Fig2_HTML.png)
![](https://cdn.statically.io/img/media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00572-020-00940-4/MediaObjects/572_2020_940_Fig3_HTML.png)
![](https://cdn.statically.io/img/media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00572-020-00940-4/MediaObjects/572_2020_940_Fig4_HTML.png)
Similar content being viewed by others
References
Astrup R, Coates KD, Hall E (2008) Recruitment limitation in forests: lessons from an unprecedented mountain pine beetle epidemic. For Ecol Manag 256:1743–1750
Beiler KJ, Durall DM, Simard SW, Maxwell SA, Kretzer AM (2010) Architecture of the wood-wide web: Rhizopogon spp. genets link multiple Douglas-fir cohorts. New Phytol 185:543–553. https://doi.org/10.1111/j.1469-8137.2009.03069.x
Beiler KJ, Simard SW, Durall DM (2015) Topology of tree–mycorrhizal fungus interaction networks in xeric and mesic Douglas-fir forests. J Ecol 103:616–628. https://doi.org/10.1111/1365-2745.12387
Bingham M, Simard S (2012) Ectomycorrhizal networks of Pseudotsuga menziesii var. glauca trees facilitate establishment of conspecific seedlings under drought. Ecosystems 15:188–199. https://doi.org/10.1007/s10021-011-9502-2
Booth MG, Hoeksema JD (2010) Mycorrhizal networks counteract competitive effects of canopy trees on seedling survival. Ecology 91:2294–2302. https://doi.org/10.1890/09-1139.1
Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055. https://doi.org/10.2307/1940179
Brearley FQ, Saner P, Uchida A et al (2016) Testing the importance of a common ectomycorrhizal network for dipterocarp seedling growth and survival in tropical forests of Borneo. Plant Ecol Divers 9:563–576. https://doi.org/10.1080/17550874.2017.1283649
Brooker RW, Maestre FT, Callaway RM et al (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34. https://doi.org/10.1111/j.1365-2745.2007.01295.x
Burton PJ (2008) The mountain pine beetle as an agent of forest disturbance. BC J Ecosyst Manag 9:9–13
Cáceres MD, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574. https://doi.org/10.1890/08-1823.1
Callaway RM (1997) Positive interactions in plant communities and the individualistic-continuum concept. Oecologia 112:143–149. https://doi.org/10.1007/s004420050293
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Chen Y, Yuan Z, Bi S, Wang X, Ye Y, Svenning JC (2018) Macrofungal species distributions depend on habitat partitioning of topography, light, and vegetation in a temperate mountain forest. Sci Rep 8:13589. https://doi.org/10.1038/s41598-018-31795-7
Cigan P, Karst J, Cahill J Jr et al (2015) Influence of bark beetle outbreaks on nutrient cycling in native pine stands in western Canada. Plant Soil 390:29–47. https://doi.org/10.1007/s11104-014-2378-0
Collins BJ, Rhoades CC, Hubbard RM, Battaglia MA (2011) Tree regeneration and future stand development after bark beetle infestation and harvesting in Colorado lodgepole pine stands. For Ecol Manag 261:2168–2175. https://doi.org/10.1016/j.foreco.2011.03.016
Coomes DA, Grubb PJ (2000) Impacts of root competition in forests and woodlands: a theoretical framework and review of experiments. Ecol Monogr 70:171–207
Cullingham CI, Cooke JEK, Dang S, Davis CS, Cooke BJ, Coltman DW (2011) Mountain pine beetle host-range expansion threatens the boreal forest. Mol Ecol 20:2157–2171. https://doi.org/10.1111/j.1365-294X.2011.05086.x
Despain DG (2001) Dispersal ecology of lodgepole pine (Pinus contorta Dougl.) in its native environment as related to Swedish forestry. For Ecol Manag 141:59–68. https://doi.org/10.1016/S0378-1127(00)00489-8
Environment Canada (2011) Historical Data - Climate - Environment and Climate Change Canada. http://climate.weather.gc.ca/historical_data/search_historic_data_e.html. Accessed 20 Sep 2019
Gärtner SM, Lieffers VJ, Macdonald SE (2011) Ecology and management of natural regeneration of white spruce in the boreal forest. Environ Rev 19:461–478. https://doi.org/10.1139/a11-017
Goodman D, Durall D, Trofymow T, Berch S (1998) A manual of concise descriptions of North American ectomycorrhizae. Mycorrhiza 8:57–59. https://doi.org/10.1007/s005720050212
Grace JB (2008) Structural equation modeling for observational studies. J Wildl Manag 72:14–22. https://doi.org/10.2193/2007-307
Halloran IPO, Cade-Menun BJ (2007) Total and Organic Phosphorus. In: Soil Sampling and Methods of Analysis, Second Edition. CRC Press
Harvey BJ, Donato DC, Turner MG (2014) Recent mountain pine beetle outbreaks, wildfire severity, and postfire tree regeneration in the US Northern Rockies. Proc Natl Acad Sci 111:15120–15125. https://doi.org/10.1073/pnas.1411346111
Högberg P, Näsholm T, Franklin O, Högberg MN (2017) Tamm review: on the nature of the nitrogen limitation to plant growth in Fennoscandian boreal forests. For Ecol Manag 403:161–185. https://doi.org/10.1016/j.foreco.2017.04.045
Hopkins AJM, Ruthrof KX, Fontaine JB et al (2018) Forest die-off following global-change-type drought alters rhizosphere fungal communities. Environ Res Lett 13:095006. https://doi.org/10.1088/1748-9326/aadc19
Horton TR, Bruns TD, Parker VT (1999) Ectomycorrhizal fungi associated with Arctostaphylos contribute to Pseudotsuga menziesii establishment. Can J Bot 77:93–102
Johnson NC, Gehring C, Jansa J (2017) Mycorrhizal mediation of soil: fertility, structure, and carbon storage. Elsevier
Karst J, Erbilgin N, Pec GJ, et al (2015) Ectomycorrhizal fungi mediate indirect effects of a bark beetle outbreak on secondary chemistry and establishment of pine seedlings. New Phytol 208:904–914. https://doi.org/10.1111/nph.13492
Karst J, Randall MJ, Gehring CA (2014) Consequences for ectomycorrhizal fungi of the selective loss or gain of pine across landscapes. Botany 92:855–865. https://doi.org/10.1139/cjb-2014-0063
Kobe RK, Coates KD (1997) Models of sapling mortality as a function of growth to characterize interspecific variation in shade tolerance of eight tree species of northwestern British Columbia. Can J For Res 27(2):227–236
Kranabetter JM (2005) Understory conifer seedling response to a gradient of root and ectomycorrhizal fungal contact. Can J Bot 83:638–646. https://doi.org/10.1139/b05-035
Kranabetter JM (2000) The effect of refuge trees on a paper birch ectomycorrhiza community. Can J Bot 77:1523–1528. https://doi.org/10.1139/b99-132
Leake J, Johnson D, Donnelly D et al (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 82:1016–1045. https://doi.org/10.1139/b04-060
Legendre P, De Cáceres M (2013) Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecol Lett 16:951–963. https://doi.org/10.1111/ele.12141
Lotan JE, Perry DA (1983) Ecology and regeneration of lodgepole pine. Agric Handb 28:51
van Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD, Franklin JF, Fulé PZ, Harmon ME, Larson AJ, Smith JM, Taylor AH, Veblen TT (2009) Widespread increase of tree mortality rates in the Western United States. Science 323:521–524. https://doi.org/10.1126/science.1165000
Martin KJ, Rygiewicz PT (2005) Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiol 5:28. https://doi.org/10.1186/1471-2180-5-28
McGuire KL (2007) Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest. Ecology 88:567–574. https://doi.org/10.1890/05-1173
Nara K (2006) Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytol 169:169–178. https://doi.org/10.1111/j.1469-8137.2005.01545.x
Nelson DW, Sommers LE (1996) Total Carbon, Organic Carbon, and Organic Matter. In: Page AL, Helmke PA, Loeppert RH (eds) Methods of Soil Analysis Part 3—Chemical Methods. Soil Science Society of America, American Society of Agronomy, Madison, WI, pp 961–1010
Nigh GD, Antos JA, Parish R (2008) Density and distribution of advance regeneration in mountain pine beetle killed lodgepole pine stands of the Montane Spruce zone of southern British Columbia. Can J For Res 38:2826–2836. https://doi.org/10.1139/X08-117
Oksanen J, Blanchet FG, Kindt R, et al (2013) Package ‘vegan.’ Community Ecol Package Version 2:
Oliver CD, Larson BC (1990) Forest stand dynamics. McGraw-Hill Pub. Co., New York
Paudel SK, Nitschke CR, Simard SW, Innes JL (2015) Regeneration dynamics of white spruce, trembling aspen, and balsam poplar in response to disturbance, climatic, and edaphic factors in the cold, dry boreal forests of the Southwest Yukon, Canada. J For 113:463–474. https://doi.org/10.5849/jof.14-086
Pec GJ, Karst J, Sywenky AN, Cigan PW, Erbilgin N, Simard SW, Cahill JF Jr (2015) Rapid increases in forest understory diversity and productivity following a mountain pine beetle (Dendroctonus ponderosae) outbreak in pine forests. PLoS One 10:e0124691. https://doi.org/10.1371/journal.pone.0124691
Pec GJ, Karst J, Taylor DL, Cigan PW, Erbilgin N, Cooke JE, Simard SW, Cahill JF Jr (2017) Change in soil fungal community structure driven by a decline in ectomycorrhizal fungi following a mountain pine beetle (Dendroctonus ponderosae) outbreak. New Phytol 213:864–873. https://doi.org/10.1111/nph.14195
Peng C, Ma Z, Lei X et al (2011) A drought-induced pervasive increase in tree mortality across Canada’s boreal forests. Nat Clim Chang 1:467–471. https://doi.org/10.1038/nclimate1293
Perry DA, Oren, R, Hart, S (2008) Forest ecosystems, 2nd edition. John Hopkins Univ Press
Pickett S, White P (1985) The ecology of natural disturbance and patch dynamics. Academic Press, New York
Purdy BG, Macdonald SE, Dale MRT (2002) The regeneration niche of white spruce following fire in the mixedwood boreal forest. Silva Fenn 36:289–306
R Development Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna URL http://www.r-project.org/
Rideout JR, He Y, Navas-Molina JA, Walters WA, Ursell LK, Gibbons SM, Chase J, McDonald D, Gonzalez A, Robbins-Pianka A, Clemente JC, Gilbert JA, Huse SM, Zhou HW, Knight R, Caporaso JG (2014) Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. PeerJ 2:e545. https://doi.org/10.7717/peerj.545
Saravesi K, Aikio S, Wäli P, Ruotsalainen AL, Kaukonen M, Huusko K, Suokas M, Brown SP, Jumpponen A, Tuomi J, Markkola A (2015) Moth outbreaks Alter root-associated fungal communities in subarctic mountain birch forests. Microb Ecol 69:788–797. https://doi.org/10.1007/s00248-015-0577-8
Selosse MA, Richard F, He X, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol 21:621–628. https://doi.org/10.1016/j.tree.2006.07.003
Simard M-J, Bergeron Y, Sirois L (1998) Conifer seedling recruitment in a southeastern Canadian boreal forest: the importance of substrate. J Veg Sci 9:575–582. https://doi.org/10.2307/3237273
Simard SW (2009) Response diversity of ectomycorrhizas in forest succession following disturbance. C Azcon-Aguilar Al Eds Mycorrhizas-Funct Process Ecol Impact Springer-Verl
Simard SW, Beiler KJ, Bingham MA et al (2012) Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev 26:39–60. https://doi.org/10.1016/j.fbr.2012.01.001
Simard SW, Durall DM (2004) Mycorrhizal networks: a review of their extent, function, and importance. Can J Bot 82:1140–1165. https://doi.org/10.1139/b04-116
Simard SW, Perry DA, Jones MD et al (1997) Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579–582
Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, London
Stursova M, Snajdr J, Cajthaml T et al (2014) When the forest dies: the response of forest soil fungi to a bark beetle-induced tree dieback. ISME J 8:1920–1931. https://doi.org/10.1038/ismej.2014.37
Teste F, Simard S (2008) Mycorrhizal networks and distance from mature trees alter patterns of competition and facilitation in dry Douglas-fir forests. Oecologia 158:193–203. https://doi.org/10.1007/s00442-008-1136-5
Teste FP, Karst J, Jones MD et al (2006) Methods to control ectomycorrhizal colonization: effectiveness of chemical and physical barriers. Mycorrhiza 17:51–65
Teste FP, Simard SW, Durall DM, Guy RD, Jones MD, Schoonmaker AL (2009) Access to mycorrhizal networks and roots of trees: importance for seedling survival and resource transfer. Ecology 90:2808–2822. https://doi.org/10.2307/25592815
Treu R, Karst J, Randall M, Pec GJ, Cigan PW, Simard SW, Cooke JE, Erbilgin N, Cahill JF Jr (2014) Decline of ectomycorrhizal fungi following a mountain pine beetle epidemic. Ecology 95:1096–1103. https://doi.org/10.1890/13-1233.1
Weed AS, Ayres MP, Hicke JA (2013) Consequences of climate change for biotic disturbances in North American forests. Ecol Monogr 83:441–470. https://doi.org/10.1890/13-0160.1
Williams AP, Allen CD, Macalady AK et al (2013) Temperature as a potent driver of regional forest drought stress and tree mortality. Nat Clim Chang 3:292–297. https://doi.org/10.1038/nclimate1693
Acknowledgments
We thank members of the Cahill Lab for providing helpful comments during the development of this manuscript. We also thank P.W. Cigan, M. Devine, M. Randall, and A. Sywenky with field assistance, F. Najari with sample processing, and C. Narang with molecular assistance.
Funding
This work was funded by a Natural Sciences and Engineering Research Council of Canada Strategic Grant (NSERC) awarded to J. Cooke, N. Erbilgin, S.W. Simard, and J.F. Cahill, Jr. and NSERC Discovery Grants awarded to N. Erbilgin, S.W. Simard, and J.F. Cahill, Jr.
Author information
Authors and Affiliations
Contributions
All authors conceived the ideas and designed methodology; GJP and JK collected the data; GJP analyzed the data; GJP and JK led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 880 kb)
Rights and permissions
About this article
Cite this article
Pec, G.J., Simard, S.W., Cahill, J.F. et al. The effects of ectomycorrhizal fungal networks on seedling establishment are contingent on species and severity of overstorey mortality. Mycorrhiza 30, 173–183 (2020). https://doi.org/10.1007/s00572-020-00940-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-020-00940-4