Abstract
Changes in soil biota following fire and its successive influence on their interactions with plants may have direct implications on the invasion success of woody alien species in fire-prone ecosystems. In this work, we experimentally addressed if soil biota from burned and unburned areas differentially affect growth and nutrition of two dominant woody natives (Lithraea molleoides and Vachellia caven) and three woody invaders (Gleditsia triacanthos, Ligustrum lucidum and Pyracantha angustifolia) that occur on fire-prone ecosystems of central Argentina. Our results indicate that growth and P content in tissues of both woody natives Lithraea and Vachellia were generally benefited by arbuscular mycorrhizal fungi (AMF) and that these effects did not strongly differ between AMF communities from burned and unburned soils. In the case of alien species, differences in growth and nutrition in response to AMF were related more to the identity of the invader than on the provenance of the soil biota. This study provides evidence on the important role that soil biota may have in the success of woody aliens in these ecosystems and on the functional stability of AMF communities facing disturbances.
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References
Allen EB, Allen MF, Helm DJ, Trappe JM, Molina R, Rincon E (1995) Patterns and regulation of mycorrhizal plant and fungal diversity. Plant Soil 170:47–62. https://doi.org/10.1007/BF02183054
Anacker BL, Klironomos JN, Maherali H, Reinhart KO, Strauss SY (2014) Phylogenetic conservatism in plant–soil feedback and its implications for plant abundance. Ecol Lett 17(12):1613–1621. https://doi.org/10.1111/ele.12378
Argañaraz JP, Pizarro GG, Zak M, Bellis LM (2015) Fire regime, climate, and vegetation in the Sierras de Córdoba, Argentina. Fire Ecol 11:55–73. https://doi.org/10.4996/fireecology.1101055
Bellgard SE, Whelan RJ, Muston RM (1994) The impact of wildfire on vesicular–arbuscular mycorrhizal fungi and their potential to influence the reestablishment of post-fire plant communities. Mycorrhiza 4:139–146
Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. https://doi.org/10.13140/2.1.4880.5444
Bunn RA, Ramsey PW, Lekberg Y (2015) Do native and invasive plants differ in their interactions with arbuscular mycorrhizal fungi? A meta-analysis. J Ecol 103:1547–1556. https://doi.org/10.1111/1365-2745.12456
Cabrera A (1976) Regiones fitogeográficas argentinas. In: Enciclopedia Argentina de Agricultura y Jardinería, 2nd edn. ACME, Buenos Aires
Carvalho LM, Antunes PM, Martins LMA, Klironomos JN (2010) Disturbance influences the outcome of plant–soil biota interactions in the invasive Acacia longifolia and in native species. Oikos 119:1172–1180. https://doi.org/10.1111/j.1600-0706.2009.18148.x
Chagnon PL, Robert L, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491. https://doi.org/10.1016/j.tplants.2013.05.001
Cingolani AM, Vaieretti MV, Giorgis MA, La Torre N, Whitworth-Hulse JI, Renison D (2013) Can livestock and fires convert the sub-tropical mountain rangelands of central Argentina into a rocky desert? Rangel J 35:285–297. https://doi.org/10.1071/RJ12095
Davison J, Öpik M, Daniell TJ, Moora M, Zobel M (2011) Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. FEMS Microbiol Ecol 78:103–115. https://doi.org/10.1111/j.1574-6941.2011.01103.x
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2013) InfoStat versión 2013. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina
Dickie IA, Bufford JL, Cobb RC, Desprez-Loustau ML, Grelet G, Hulme PE, Klironomos J, Makiola A, Nuñez M, Pringle A, Thrall PH, Tourtellot SG, Waller L, Williams NM (2017) The emerging science of linked plant-fungal invasions. N Phytol 215:1314–1332. https://doi.org/10.1111/nph.14657
Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139. https://doi.org/10.1016/S0169-5347(98)01554-7
Ferreras AE, Funes G, Galetto L (2015) The role of seed germination in the invasion process of Honey locust (Gleditsia triacanthos L., Fabaceae): comparison with a native confamilial. Plant Species Biol 30:126–136. https://doi.org/10.1111/1442-1984.12041
García de León DG, Moora M, Öpik M, Jairus T, Neuenkamp L, Vasar M, Bueno CG, Gerz M, Davison J, Zobel M (2016) Dispersal of arbuscular mycorrhizal fungi and plants during succession. Acta Oecol 77:128–135
Giorgis MA, Cingolani AM, Chiarini F, Chiapella J, Barboza G, Ariza Espinar L, Morero R, Gurvich DE, Tecco PA, Subils R, Cabido M (2011) Composición florística del Bosque Chaqueño Serrano de la provincia de Córdoba, Argentina. Kurtziana 36:9–43
Giorgis MA, Cingolani AM, Cabido M (2013) El efecto del fuego y las características topográficas sobre la vegetación y las propiedades del suelo en la zona de transición entre bosques y pastizales de las sierras de Córdoba Argentina. Bol Soc Argent Bot 48(3–4):493–513
Giorgis MA, Cingolani AM, Gurvich DE, Tecco PA, Chiapella J, Chiarini F, Cabido M (2017) Changes in floristic composition and physiognomy are decoupled along elevation gradients in central Argentina. Appl Veg Sci 20(4):558–571
Gosling P, Jones J, Bending GD (2016) Evidence for functional redundancy in arbuscular mycorrhizal fungi and implications for agroecosystem management. Mycorrhiza 26(1):77–83. https://doi.org/10.1007/s00572-015-0651-6
Grace C, Stribley DP (1991) A safer procedure for routine staining of vesicular arbuscular mycorrhizal fungi. Mycol Res 95:1160–1162. https://doi.org/10.1016/S0953-7562(09)80005-1
Grilli G, Urcelay C, Galetto L (2012) Forest fragment size and nutrient availability: complex responses of mycorrhizal fungi in native–exotic hosts. Plant Ecol 2132:155–165. https://doi.org/10.1007/s11258-011-9966-3
Grilli G, Urcelay C, Galetto L, Davison J, Vasar M, Saks Ü, Jairus T, Öpik M (2015) The composition of arbuscular mycorrhizal fungal communities in the roots of a ruderal forb is not related to the forest fragmentation process. Environ Microbiol 17:2709–2720. https://doi.org/10.1111/1462-2920.12623
Gundale MJ, Wardle DA, Kardol P, Nilsson MC (2019) Comparison of plant–soil feedback experimental approaches for testing soil biotic interactions among ecosystems. N Phytol 221(1):577–587
Herrero ML, Torres RC, Renison D (2015) Do wildfires promote woody species invasion in a fire-adapted ecosystem? Post-fire resprouting of native and non-native woody plants in central Argentina. Environ Manag 57:308–317. https://doi.org/10.1007/s00267-015-0616-8
Holden SR, Treseder KK (2013) A meta-analysis of soil microbial biomass responses to forest disturbances. Front Microbiol 4:163. https://doi.org/10.3389/fmicb.2013.00163
Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? N Phytol 177(3):779–789
Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci USA 107:2093–2098
Jones JB, Wolf B, Mills HA (1991) Plant analysis handbook. A practical sampling, preparation, analysis, and interpretation guide. Micro-Macro Publishing Inc., Athens
Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301. https://doi.org/10.1890/02-0413
Kucey RMN (1983) Phosphate solubilizing bacteria and fungi in various cultivated and virgin Alberta soils. Can J Soil Sci 63:671–678
Longo S, Nouhra E, Goto B, Berbara R, Urcelay C (2014) Effects of fire on arbuscular mycorrhizal fungi in the Mountain Chaco Forest. For Ecol Manag 314:86–94. https://doi.org/10.1016/j.foreco.2013.12.027
Longo S, Cofré N, Soteras F, Grilli G, Lugo M, Urcelay C (2016) Taxonomic and functional response of arbuscular mycorrhizal fungi to land use change in central Argentina. In: Recent advances on mycorrhizal fungi, pp 81–90. https://doi.org/10.1007/978-3-319-24355-9_7
Luti R, Bertrán de Solís MA, Galera MF, Müller de Ferreira N, Berzal M, Nores M, Herrera MA, Barrera JC (1979) Vegetación. In: Vázquez J, Miatello R, Roque M (eds) Geografía Física de la provincia de Córdoba. Boldt Press, Buenos Aires, pp 297–368
McGonigle T, Miller M, Evans D, Fairchild G, Swan J (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi.New Phytol 115:495–501
Meisner A, Hol WG, de Boer W, Krumins JA, Wardle DA, van der Putten WH (2014) Plant–soil feedbacks of exotic plant species across life forms: a meta-analysis. Biol Invasions 16:2551–2561. https://doi.org/10.1007/s10530-014-0685-2
Moglia G, Giménez AM (1998) Rasgos anatómicos característicos del hidrosistema de las principales especies arbóreas de la región chaqueña argentina. Investig Agrar Sist Recur 7:53–71
Moora M, Berger S, Davison J et al (2011) Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. J Biogeogr 38:1305–1317. https://doi.org/10.1111/j.1365-2699.2011.02478.x
Moreschi EG, Funes G, Zeballos SR, Tecco PA (2019) Post-burning germination responses of woody invaders in a fire-prone ecosystem. Austral Ecol 44(7):1163–1173
Nuñez MA, Dickie IA (2014) Invasive belowground mutualists of woody plants. Biol Invasions 16:645–661. https://doi.org/10.1007/s10530-013-0612-y
Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24:497–504. https://doi.org/10.1016/j.tree.2009.03.016
Pyšek P, Richardson DM (2008) Traits associated with invasiveness in alien plants: where do we stand? In: Biological invasions. Springer, Berlin, pp 97–125
Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. N Phytol 170:445–457. https://doi.org/10.1111/j.1469-8137.2006.01715.x
Richardson DM, Allsopp N, D’Antonio C, Milton SJ, Rejmánek M (2000) Plant invasions the role of mutualism. Biol Rev 75:65–93. https://doi.org/10.1111/j.1469-185X.1999.tb00041.x
Seifert E, Bever J, Maron A (2009) Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology 90:1055–1062. https://doi.org/10.1890/08-0419.1
Sepp SK, Davison J, Jairus T, Vasar M, Moora M, Zobel M, Öpik M (2019) Non-random association patterns in a plant–mycorrhizal fungal network reveal host-symbiont specificity. Mol Ecol 28:365–378. https://doi.org/10.1111/mec.14924
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London
Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133(1):16–20
Tecco PA, Urcelay C, Díaz S, Cabido M, Perez Harguindeguy N (2013) Contrasting functional trait syndromes underlay woody alien success in the same ecosystem. Austral Ecol 38:443–451. https://doi.org/10.1111/j.1442-9993.2012.02428.x
Uibopuu A, Moora M, Öpik M, Zobel M (2012) Temperate forest understorey species performance is altered by local arbuscular mycorrhizal fungal communities from stands of different successional stages. Plant Soil 356:331–339. https://doi.org/10.1007/s11104-011-1116-0
Urcelay C, Díaz S, Gurvich DE, Chapin FS, Cuevas E, Domínguez LS (2009) Mycorrhizal community resilience in response to experimental plant functional type removals in a woody ecosystem. J Ecol 97:1291–1301. https://doi.org/10.1111/j.1365-2745.2009.01582.x
Urcelay C, Longo S, Geml J, Tecco PA (2019) Can arbuscular mycorrhizal fungi from non-invaded montane ecosystems facilitate the growth of alien trees? Mycorrhiza 29:39–49
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72. https://doi.org/10.1038/23932
van der Heyde M, Ohsowski B, Abbott LK, Hart M (2017) Arbuscular mycorrhizal fungus responses to disturbance are context-dependent. Mycorrhiza 27:431–440. https://doi.org/10.1007/s00572-016-0759-3
Vestergård M, Rønn R, Ekelund F (2015) Above-belowground interactions govern the course and impact of biological invasions. AoB Plants 7:plv025. https://doi.org/10.1093/aobpla/plv025
Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478
Walker C (1992) Systematics and taxonomy of the arbuscular endomycorrhizal fungi (Glomales): a possible way forward. Agronomie 12:887–897
Williamson M (1999) Invasions. Ecography 22:5–12. https://doi.org/10.1111/j.1600-0587.1999.tb00449.x
Zak MR, Cabido M, Hodgson JG (2004) Do subtropical seasonal forests in the Gran Chaco, Argentina, have a future? Biol Conserv 120:589–598. https://doi.org/10.1016/j.biocon.2004.03.034
Acknowledgements
The authors wish to acknowledge the assistance of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and the Universidad Nacional de Córdoba (U.N.C), both of which have provided facilities used for this study. This research program is funded by Secretaría de Ciencia y Tecnología: Universidad Nacional de Córdoba (Secyt) (Universidad Nacional de Córdoba) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). S.L., E.N., P.A.T., and C.U. are Researchers of CONICET, and Professors at the U.N.C. The editors and three anonymous reviewers provided critical comments and suggestions that improved the quality of this manuscript.
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Longo, S., Nouhra, E., Tecco, P.A. et al. Functional stability of mycorrhizal interactions in woody natives and aliens facing fire disturbance. Plant Ecol 221, 321–331 (2020). https://doi.org/10.1007/s11258-020-01014-3
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DOI: https://doi.org/10.1007/s11258-020-01014-3