Competition between Nothofagus obliqua and Pinus ponderosa: effects on their growth and associated ectomycorrhizal communities

Authors

DOI:

https://doi.org/10.30550/j.lil/2093

Keywords:

Competition, diversity, invasion, mycorrhizas, restoration

Abstract

Plant competition can significantly influence plant growth and their symbiotic associations, which is particularly important in both ecological restoration and invasion processes. This study evaluated the effect of competition between Nothofagus obliqua and Pinus ponderosa on plant growth, colonization by ectomycorrhizal fungi, and the taxonomic and functional diversity of these symbionts growing in soils of native forest and pine plantation. The results showed that the growth of both species was greater in native forest soils, likely due to their higher nutrient content. However, contrary to expectations, the effect of competition was neutral or even positive, particularly for N. obliqua. These findings suggest a coexistence facilitated by differences in resource use strategies. Regarding mycorrhizas, each species exhibited higher colonization levels in soils previously dominated by its own species. Despite this, both soils showed distinctive taxonomic and functional compositions, with plantation soils exhibiting overall higher diversity. However, melanized fungi, crucial for coping with water stress, were absent in this soil. Our results highlight the invasive potential of P. ponderosa and the suitability of N. obliqua for restoring environments converted into pine plantations. Furthermore, these findings emphasize the importance of considering symbiotic fungal communities in such efforts, suggesting that mycorrhizal inoculum could be key to maximizing restoration success in degraded soils.

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References

Adler, P. B., Smull, D., Beard, K. H., Choi, R. T., Furniss, T., Kulmatiski, A., Meiners, J. M., Tredennick, A. T. y Veblen, K. E. (2018). Competition and coexistence in plant communities: Intraspecific competition is stronger than interspecific competition. Ecology Letters 21 (9): 1319-1329. https://doi.org/10.1111/ele.13098

Agerer, R. (Ed.). (1987). Colour atlas of ectomycorrhizae: With glossary. Delivery 2 (1th-5th del eds.). Einhorn-Verl. Dietenberger.

Agerer, R. (2001). Exploration types of ectomycorrhizae. Mycorrhiza 11 (2): 107-114. https://doi.org/10.1007/s005720100108

Asmelash, F., Bekele, T. y Birhane, E. (2016). The potential role of arbuscular mycorrhizal fungi in the restoration of degraded lands. Frontiers in Microbiology 7. https://doi.org/10.3389/fmicb.2016.01095

Averett, J. P., McCune, B., Parks, C. G., Naylor, B. J., DelCurto, T. y Mata-González, R. (2016). Non-native plant invasion along elevation and canopy closure gradients in a middle rocky mountain ecosystem. PLOS ONE 11 (1): e0147826. https://doi.org/10.1371/journal.pone.0147826

Avis, P. G., Mueller, G. M. y Lussenhop, J. (2008). Ectomycorrhizal fungal communities in two North American oak forests respond to nitrogen addition. New Phytologist 179 (2): Article 2. https://doi.org/10.1111/j.1469-8137.2008.02491.x

Azpilicueta, M. M., Gallo, L. A., Martinez, A., Varela, S. y others. (2010). Manual de viverización, cultivo y plantación de roble pellín en el norte de la región andino patagónica. 1a. edición. Buenos Aires: INTA.

Barroetaveña, C., Salomón, M. E. S. y Bassani, V. (2019). Rescuing the ectomycorrhizal biodiversity associated with South American Nothofagaceae forest, from the 19th century naturalists up to molecular biogeography. Forestry: An International Journal of Forest Research 92 (5): Article 5. https://doi.org/10.1093/forestry/cpz047

Bates, D., Mächler, M., Bolker, B. Walker, S. (2015). Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software 67 (1). https://doi.org/10.18637/jss.v067.i01

Bielak, K., Dudzinska, M. y Pretzsch, H. (2015). Volume growth of mixed-species versus pure stands: Results from selected long-term experimental plots in Central Europe. Sylwan 159: 22-35.

Bruns, T. D., Bidartondo, M. I. y Taylor, D. L. (2002). Host specificity in ectomycorrhizal communities: What do the exceptions tell us?1. Integrative and Comparative Biology 42 (2): 352-359. https://doi.org/10.1093/icb/42.2.352

Calviño-Cancela, M. y van Etten, E. J. B. (2018). Invasive potential of Eucalyptus globulus and Pinus radiata into native eucalypt forests in Western Australia. Forest Ecology and Management 424: 246-258. https://doi.org/10.1016/j.foreco.2018.05.001

Craine, J. M. y Dybzinski, R. (2013). Mechanisms of plant competition for nutrients, water and light. Functional Ecology 27 (4): 833-840. https://doi.org/10.1111/1365-2435.12081

Dickie, I. A., Bolstridge, N., Cooper, J. A. y Peltzer, D. A. (2010). Co?invasion by Pinus and its mycorrhizal fungi. New Phytologist 187 (2): 475-484. https://doi.org/10.1111/j.1469-8137.2010.03277.x

Donoso Zegers, C. (2006). Las especies arbóreas de los bosques templados de Chile y Argentina: Autoecología (1a ed.). Marisa Cuneo Ediciones.

Eagar, A. C., Mushinski, R. M., Horning, A. L., Smemo, K. A., Phillips, R. P. y Blackwood, C. B. (2022). Arbuscular mycorrhizal tree communities have greater soil fungal diversity and relative abundances of saprotrophs and pathogens than ectomycorrhizal tree communities. Applied and Environmental Microbiology 88 (1): e01782-21. https://doi.org/10.1128/AEM.01782-21

Felton, A., Nilsson, U., Sonesson, J., Felton, A. M., Roberge, J.-M., Ranius, T., Ahlström, M., Bergh, J., Björkman, C., Boberg, J., Drössler, L., Fahlvik, N., Gong, P., Holmström, E., Keskitalo, E. C. H., Klapwijk, M. J., Laudon, H., Lundmark, T., Niklasson, M., … Wallertz, K. (2016). Replacing monocultures with mixed-species stands: Ecosystem service implications of two production forest alternatives in Sweden. Ambio 45 (2): 124-139. https://doi.org/10.1007/s13280-015-0749-2

Fernandez, C. W. y Koide, R. T. (2013). The function of melanin in the ectomycorrhizal fungus Cenococcum geophilum under water stress. Fungal Ecology 6 (6): 479-486. https://doi.org/10.1016/j.funeco.2013.08.004

Fernández, N. V., Marchelli, P., Gherghel, F., Kost, G. y Fontenla, S. B. (2015). Ectomycorrhizal fungal communities in Nothofagus nervosa ( Raulí ): A comparison between domesticated and naturally established specimens in a native forest of Patagonia, Argentina. Fungal Ecology 18: 36-47. https://doi.org/10.1016/j.funeco.2015.05.011

Fichtner, A., Härdtle, W., Li, Y., Bruelheide, H., Kunz, M. y von Oheimb, G. (2017). From competition to facilitation: How tree species respond to neighbourhood diversity. Ecology Letters 20 (7): 892-900. https://doi.org/10.1111/ele.12786

Floriani, F. D., El Mujtar, V., Mateo, C., Sola, G., Peñalba, M. G., Sbrancia, R., Marchelli, P. y Fernández, N. V. (2024). Site conditions shaped the effect of silvicultural management on the biodiversity of ectomycorrhizal fungi in mixed Nothofagus forests. Forest Ecology and Management 563: 121981. https://doi.org/10.1016/j.foreco.2024.121981

Galarco, S. P. y Ramilo, D. I. (2020). Plantaciones forestales en Argentina. Editorial de la Universidad Nacional de La Plata (EDULP). https://doi.org/10.35537/10915/101543

Gazol, A., Zobel, M., Cantero, J. J., Davison, J., Esler, K. J., Jairus, T., Öpik, M., Vasar, M. y Moora, M. (2016). Impact of alien pines on local arbuscular mycorrhizal fungal communities—Evidence from two continents. FEMS Microbiology Ecology 92 (6): fiw073. https://doi.org/10.1093/femsec/fiw073

Gioria, M., Pyšek, P. y Osborne, B. A. (2018). Timing is everything: Does early and late germination favor invasions by herbaceous alien plants?. Journal of Plant Ecology 11 (1): 4-16. https://doi.org/10.1093/jpe/rtw105

Gómez, P., Murúa, M., Martín, J. S., Goncalves, E. y Bustamante, R. O. (2019). Maintaining close canopy cover prevents the invasion of Pinus radiata: Basic ecology to manage native forest invasibility. PLOS ONE 14 (5): e0210849. https://doi.org/10.1371/journal.pone.0210849

Grand, L. F. y Harvey A. E. (1982). Quantitative measurement of ectomycorrhizae on plant roots. En: Schenk, N. C. (ed.), Method and principles of mycorrhizal research. APS Press. St. Paul, Minnesota, pp: 157-164.

Haase, D. L. (2008). Understanding forest seedling quality: Measurements and interpretation. Tree Planters’ Notes 52 (2): Article 2.

Hagen, D. y Evju, M. (2013). Using Short-Term Monitoring Data to Achieve Goals in a Large-Scale Restoration. Ecology and Society 18 (3). https://www.jstor.org/stable/26269355

Hartig, F. (2020). DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.3, 3.

Hill, M. O. (1973). Diversity and Evenness: A Unifying Notation and Its Consequences. Ecology 54 (2): 427-432. https://doi.org/10.2307/1934352

Huat, O. K., Awang, K., Hashim, A. y Majid, N. M. (2002). Effects of fertilizers and vesicular–arbuscular mycorrhizas on the growth and photosynthesis of Azadirachta excelsa (Jack) Jacobs seedlings. Forest Ecology and Management 158 (1-3): Article 1-3. https://doi.org/10.1016/S0378-1127(00)00668-X

Iannone, B. V., Potter, K. M., Hamil, K.-A. D., Huang, W., Zhang, H., Guo, Q., Oswalt, C. M. y Woodall, C. W. Fei, S. (2016). Evidence of biotic resistance to invasions in forests of the Eastern USA. Landscape Ecology 31 (1): 85-99. https://doi.org/10.1007/s10980-015-0280-7

Izumi, H. (2024). Abundances of ectomycorrhizal exploration types show the type-dependent temporal dynamics over the seasons—A controlled growth container experiment. International Microbiology. https://doi.org/10.1007/s10123-024-00573-z

Janowski, D. y Leski, T. (2023). Methods for identifying and measuring the diversity of ectomycorrhizal fungi. Forestry: An International Journal of Forest Research 96 (5): 639-652. https://doi.org/10.1093/forestry/cpad017

Jo, I., Potter, K. M., Domke, G. M. y Fei, S. (2018). Dominant forest tree mycorrhizal type mediates understory plant invasions. Ecology Letters 21 (2): 217-224. https://doi.org/10.1111/ele.12884

Jonášová, M., van Hees, A. y Prach, K. (2006). Rehabilitation of monotonous exotic coniferous plantations: A case study of spontaneous establishment of different tree species. Ecological Engineering 28 (2): 141-148. https://doi.org/10.1016/j.ecoleng.2006.05.008

Kiær, L. P., Weisbach, A. N. y Weiner, J. (2013). Root and shoot competition: A meta-analysis. Journal of Ecology 101 (5): 1298-1312. https://doi.org/10.1111/1365-2745.12129

Koziol, L., Schultz, P. A., House, G. L., Bauer, J. T., Middleton, E. L. y Bever, J. D. (2018). The Plant Microbiome and Native Plant Restoration: The Example of Native Mycorrhizal Fungi. BioScience 68 (12): 996-1006. https://doi.org/10.1093/biosci/biy125

Lenth, R., Singmann, H., Love, J., Buerkner, P. y Herve, M. (2018). emmeans: Estimated marginal means, aka least-squares means (R package, Version 1.4)[Computer software].

Li, D. (2018). hillR: Taxonomic, functional, and phylogenetic diversity and similarity through Hill Numbers. Journal of Open Source Software 3 (31): 1041. https://doi.org/10.21105/joss.01041

Li, S., Di, X., Wu, D. y Zhang, J. (2013). Effects of sewage sludge and nitrogen fertilizer on herbage growth and soil fertility improvement in restoration of the abandoned opencast mining areas in Shanxi, China. Environmental Earth Sciences 70 (7): 3323-3333. https://doi.org/10.1007/s12665-013-2397-9

Liebhold, A. M., Brockerhoff, E. G., Kalisz, S., Nuñez, M. A., Wardle, D. A. y Wingfield, M. J. (2017). Biological invasions in forest ecosystems. Biological Invasions 19 (11): 3437-3458. https://doi.org/10.1007/s10530-017-1458-5

Lofgren, L., Nguyen, N. H. y Kennedy, P. G. (2018). Ectomycorrhizal host specificity in a changing world: Can legacy effects explain anomalous current associations?. New Phytologist 220 (4): 1273-1284. https://doi.org/10.1111/nph.15008

López-García, Á., Gil-Martínez, M., Navarro-Fernández, C. M., Kjøller, R., Azcón-Aguilar, C., Domínguez, M. T. y Marañón, T. (2018). Functional diversity of ectomycorrhizal fungal communities is reduced by trace element contamination. Soil Biology and Biochemistry 121: 202-211. https://doi.org/10.1016/j.soilbio.2018.03.021

Mangla, S., Sheley, R. L., James, J. J. y Radosevich, S. R. (2011). Intra and interspecific competition among invasive and native species during early stages of plant growth. Plant Ecology 212 (4): 531-542. https://doi.org/10.1007/s11258-011-9909-z

Martin, D. M. (2017). Ecological restoration should be redefined for the twenty-first century. Restoration Ecology 25 (5): 668-673. https://doi.org/10.1111/rec.12554

Martin, K. J. y Rygiewicz, P. T. (2005). Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiology 5 (1): Article 1. https://doi.org/10.1186/1471-2180-5-28

Martínez-Ramos, M., Pingarroni, A., Rodríguez-Velázquez, J., Toledo-Chelala, L., Zermeño-Hernández, I. y Bongers, F. (2016). Natural forest regeneration and ecological restoration in human-modified tropical landscapes. Biotropica 48 (6): 745-757. https://doi.org/10.1111/btp.12382

Menzel, A., Hempel, S., Klotz, S., Moora, M., Pyšek, P., Rillig, M. C., Zobel, M. y Kühn, I. (2017). Mycorrhizal status helps explain invasion success of alien plant species. Ecology 98 (1): 92-102. https://doi.org/10.1002/ecy.1621

Netherway, T. y Bahram, M. (2024). Melanized root-associated fungi: Key players in plant–soil systems. Trends in Microbiology 32 (12): 1190-1199. https://doi.org/10.1016/j.tim.2024.06.006

Neuenkamp, L., Prober, S. M., Price, J. N., Zobel, M.y Standish, R. J. (2019). Benefits of mycorrhizal inoculation to ecological restoration depend on plant functional type, restoration context and time. Fungal Ecology 40: 140-149. https://doi.org/10.1016/j.funeco.2018.05.004

Ni, M., Liu, Y., Chu, C., Xu, H. y Fang, S. (2018). Fast seedling root growth leads to competitive superiority of invasive plants. Biological Invasions 20 (7): 1821-1832. https://doi.org/10.1007/s10530-018-1664-9

Oksanen, J., Simpson, G. L., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Solymos, P., Stevens, M. H. H., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Carvalho, G., Chirico, M., Caceres, M. D., Durand, S., … Weedon, J. (2024). vegan: Community Ecology Package (Versión 2.6-8) [Software]. https://cran.r-project.org/web/packages/vegan/index.html

Orrock, J. L., Witter, M. S. y Reichman, O. J. (2008). Apparent Competition with an Exotic Plant Reduces Native Plant Establishment. Ecology 89 (4): 1168-1174. https://doi.org/10.1890/07-0223.1

Parrent, J. L., Morris, W. F. y Vilgalys, R. (2006). CO2?enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 87 (9): Article 9. https://doi.org/10.1890/0012-9658(2006)87[2278:CANAAE]2.0.CO;2

Pauchard, A., García, R., Zalba, S., Sarasola, M., Zenni, R., Ziller, S. y Nuñez, M. A. (2016). 14. Pine Invasions in South America: Reducing Their Ecological Impacts Through Active Management. En J. Canning-Clode (Ed.), Biological Invasions in Changing Ecosystems: Vectors, Ecological Impacts, Management and Predictions (pp. 318–342). De Gruyter Open Poland. https://doi.org/10.1515/9783110438666-020

Pellitier, P. T., Van Nuland, M., Salamov, A., Grigoriev, I. V. y Peay, K. G. (2024). Potential for functional divergence in ectomycorrhizal fungal communities across a precipitation gradient. ISME Communications 4 (1): ycae031. https://doi.org/10.1093/ismeco/ycae031

Pérez-Pazos, E., Certano, A., Gagne, J., Lebeuf, R., Siegel, N., Nguyen, N. y Kennedy, P. G. (2021). The slippery nature of ectomycorrhizal host specificity: Suillus fungi associated with novel pinoid (Picea) and abietoid (Abies) hosts. Mycologia 113: 891-901. https://doi.org/10.1080/00275514.2021.1921525

R Core Team. (2022). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.R-project.org/

Sabatier, Y., Azpilicueta, M. M., Marchelli, P., González-Peñalba, M., Lozano, L., García, L., Martinez, A., Gallo, L. A., Umaña, F., Bran, D. y Pastorino, M. J. (2011). Distribución natural de Nothofagus alpina y Nothofagus obliqua (Nothofagaceae) en Argentina, dos especies de primera importancia forestal de los bosques templados norpatagónicos. Boletín de la Sociedad Argentina de Botánica 46 (1-2): 131-138.

Sapsford, S. J., Wakelin, A., Peltzer, D. A. y Dickie, I. A. (2022). Pine invasion drives loss of soil fungal diversity. Biological Invasions 24 (2): 401-414. https://doi.org/10.1007/s10530-021-02649-7

Smith, S. E. y Read, D. J. (2008). Mycorrhizal Symbiosis. Elsevier. https://doi.org/10.1016/B978-0-12-370526-6.X5001-6

Souza-Alonso, P., Saiz, G., García, R. A., Pauchard, A., Ferreira, A. y Merino, A. (2022). Post-fire ecological restoration in Latin American forest ecosystems: Insights and lessons from the last two decades. Forest Ecology and Management 509: 120083. https://doi.org/10.1016/j.foreco.2022.120083

Suz, L. M., Kallow, S., Reed, K., Bidartondo, M. I. y Barsoum, N. (2017). Pine mycorrhizal communities in pure and mixed pine-oak forests: Abiotic environment trumps neighboring oak host effects. Forest Ecology and Management 406: 370-380. https://doi.org/10.1016/j.foreco.2017.09.030

Tedersoo, L., Bahram, M., Põlme, S., Kõljalg, U., Yorou, N. S., Wijesundera, R., Ruiz, L. V., Vasco-Palacios, A. M., Thu, P. Q., Suija, A., Smith, M. E., Sharp, C., Saluveer, E., Saitta, A., Rosas, M., Riit, T., Ratkowsky, D., Pritsch, K., Põldmaa, K., … Abarenkov, K. (2014). Global diversity and geography of soil fungi. Science 346 (6213): Article 6213. https://doi.org/10.1126/science.1256688

Tedersoo, L., Bahram, M., Toots, M., Diédhiou, A. G., Henkel, T. W., Kjøller, R., Morris, M. H., Nara, K., Nouhra, E., Peay, K. G., Põlme, S., Ryberg, M., Smith, M. E. y Kõljalg, U. (2012). Towards global patterns in the diversity and community structure of ectomycorrhizal fungi: Global metastudy of ectomycorrhizal fungi. Molecular Ecology 21 (17): Article 17. https://doi.org/10.1111/j.1365-294X.2012.05602.x

Theoharides, K. A. y Dukes, J. S. (2007). Plant invasion across space and time: Factors affecting nonindigenous species success during four stages of invasion. New Phytologist 176 (2): 256-273. https://doi.org/10.1111/j.1469-8137.2007.02207.x

van der Linde, S., Suz, L. M., Orme, C. D. L., Cox, F., Andreae, H., Asi, E., Atkinson, B., Benham, S., Carroll, C., Cools, N., De Vos, B., Dietrich, H.-P., Eichhorn, J., Gehrmann, J., Grebenc, T., Gweon, H. S., Hansen, K., Jacob, F., Kristöfel, F., … Bidartondo, M. I. (2018). Environment and host as large-scale controls of ectomycorrhizal fungi. Nature 558 (7709): Article 7709. https://doi.org/10.1038/s41586-018-0189-9

Wu, D., Zhang, M., Peng, M., Sui, X., Li, W. y Sun, G. (2019). Variations in Soil Functional Fungal Community Structure Associated With Pure and Mixed Plantations in Typical Temperate Forests of China. Frontiers in Microbiology 10. https://doi.org/10.3389/fmicb.2019.01636

Xia, J. y Wan, S. (2008). Global response patterns of terrestrial plant species to nitrogen addition. New Phytologist 179 (2): Article 2. https://doi.org/10.1111/j.1469-8137.2008.02488.x

Zamorano-Elgueta, C., Rey Benayas, J. M., Cayuela, L., Hantson, S. y Armenteras, D. (2015). Native forest replacement by exotic plantations in southern Chile (1985–2011) and partial compensation by natural regeneration. Forest Ecology and Management 345: 10-20. https://doi.org/10.1016/j.foreco.2015.02.025

Competencia entre Nothofagus obliqua y Pinus ponderosa: efectos sobre su crecimiento y comunidades ectomicorrícicas asociadas

Published

2025-07-03

How to Cite

Fioroni, F., Carrón, A., Caldironi, F., & Fernández, N. (2025). Competition between Nothofagus obliqua and Pinus ponderosa: effects on their growth and associated ectomycorrhizal communities. Lilloa, 61(s2), 21–44. https://doi.org/10.30550/j.lil/2093