Abstract
Background
Alien invasive plants have severely threatened the invaded habitats' structural stability and species diversity. The positive impacts of arbuscular mycorrhizal (AM) fungi on the successful invasion of some alien plants have been well documented, whereas soil phosphorus (P) frequently affects AM fungi benefits. Nevertheless, how soil P availability affects AM fungal function and then shifts the competitive direction of congeneric invasive and native plants remains unclear.
Methods
A pot experiment was conducted. Specifically, the AM fungus treatments were inoculation or non-inoculation with Claroideoglomus etunicatum; the P addition treatments included three different rates of P supply; the competition styles contained intraspecific competition of invasive Eupatorium adenophorum and congeneric native Eupatorium lindleyanum respectively and interspecific competition when the two plant species were grown together. Plant biomass and nutrients were analyzed.
Results
The results showed that AM fungus promoted the growth and nutrients of E. adenophorum and E. lindleyanum. P addition decreased the mycorrhizal response of the two species under intraspecific competition but increased the mycorrhizal responses of E. lindleyanum under interspecific competition. The relative yield and competitive aggressivity showed that E. lindleyanum had significantly greater competitiveness than E. adenophorum. AM fungus further improved the competitive aggressivity of E. lindleyanum under moderate P addition, while it did not influence the competitive aggressivity in biomass of the two species under low and high P conditions.
Conclusion
AM fungus enhances the competitiveness of a native plant over an invasive plant with a moderate soil P supply.
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Data availability
All data generated or analyzed during this study are included in this article (and its supplementary information files).
References
Awaydul A, Wanyingzhu, Yuan Y, Jing X, Lei C (2019) Common mycorrhizal networks influence the distribution of mineral nutrients between an invasive plant, Solidago canadensis, and a native plant, Kummerowa striata. Mycorrhiza. https://doi.org/10.1007/s00572-018-0873-5
Bao SD (2000) Soil and agricultural chemistry analysis. China agriculture press, Beijing
Barto K, Friese C, Cipollini D (2010) Arbuscular mycorrhizal fungi protect a native plant from allelopathic effects of an invader. J Chem Ecol 36:351–360. https://doi.org/10.1007/s10886-010-9768-4
Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115. https://doi.org/10.1111/nph.14976
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
Burns JH, Strauss SY (2011) More closely related species are more ecologically similar in an experimental test. Proc Natl Acad Sci U S A 108:5302–5307. https://doi.org/10.1073/pnas.1013003108
Carter MR, Gregorich EG (2007) Soil sampling and methods of analysis. CRC Press
Chen E, Liao H, Chen B, Peng S (2020) Arbuscular mycorrhizal fungi are a double‐edged sword in plant invasion controlled by phosphorus concentration. New Phytol 226. https://doi.org/10.1111/nph.16359
Cheng JK, Yue MF, Yang HR, Chen BM, Xin GR (2019) Do arbuscular mycorrhizal fungi help the native species Bidens biternata resist the invasion of Bidens alba? Plant Soil 444:443–455. https://doi.org/10.1007/s11104-019-04297-2
Cheng JK, Cao MY, Yang HR, Yue MF, Xin GR, Chen BM (2022) Interactive effects of allelopathy and arbuscular mycorrhizal fungi on the competition between the invasive species Bidens alba and its native congener Bidens biternata. Weed Res 62:268–276. https://doi.org/10.1111/wre.12534
Daehler, Curtis C (2001) Darwin’s naturalization hypothesis revisited. Am Nat 158:324–330. https://doi.org/10.1086/321316
Darwin, C (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London: John Murray
Elbon A, Whalen JK (2015) Phosphorus supply to vegetable crops from arbuscular mycorrhizal fungi: a review. Biol Agric Hortic 31:73–90. https://doi.org/10.1080/01448765.2014.966147
Fagúndez J, Lema M (2019) A competition experiment of an invasive alien grass and two native species: are functionally similar species better competitors? Biol. Invasions 21:3619–3631. https://doi.org/10.1007/s10530-019-02073-y
Feng J, Song Y, Zhu B (2023) Ecosystem-dependent responses of soil carbon storage to phosphorus enrichment. New Phytol. https://doi.org/10.1111/nph.18907
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol: 489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
He Y, Jiang C, Yang H, Wang Y, Zhong Z (2017) Arbuscular mycorrhizal fungal composition affects the growth and nutrient acquisition of two plants from a karst area. Sains Malays 46:1701–1708. https://doi.org/10.17576/jsm-2017-4610-05
He Y, Cornelissen JH, Wang P, Dong M, Ou J (2019) Nitrogen transfer from one plant to another depends on plant biomass production between conspecific and heterospecific species via a common arbuscular mycorrhizal network. Environ Sci Pollut R 26:8828–8837. https://doi.org/10.1007/s11356-019-04385-x
He XL, Zheng ZC, Li TX, He SQ, Li Z (2022) Effects of phosphorus fertilizer application rates on colloidal phosphorus leaching in purple soil in Southwest China. Water 14. https://doi.org/10.3390/w14152391
Hu CC, Lei YB, Tan YH, Sun XC, Xu H, Liu CQ, Liu XY (2019) Plant nitrogen and phosphorus utilization under invasive pressure in a montane ecosystem of tropical China. J Ecol 107:372–386. https://doi.org/10.1111/1365-2745.13008
Huangfu C, Li K, Hui D (2019) Influences of plant interspecific competition and arbuscular mycorrhizal fungi on nitrogen form preference of an invasive plant. Biogeochemistry 145. https://doi.org/10.1007/s10533-019-00607-z
Javaid A (2009) Arbuscular mycorrhizal mediated nutrition in plants. J Plant Nutr 32:1595–1618. https://doi.org/10.1080/01904160903150875
Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647. https://doi.org/10.1111/j.1469-8137.2009.03110.x
Jonathan P, LynchKathleen M, Brown (2001) Topsoil foraging – an architectural adaptation of plants to low phosphorus availability. Plant Soil. https://doi.org/10.1023/A:1013324727040
Kisa M, Sanon A, Thioulouse J, Assigbetse K, Sylla S, Spichiger R, Dieng L, Berthelin J, Prin Y, Galiana A (2007) Arbuscular mycorrhizal symbiosis can counterbalance the negative influence of the exotic tree species Eucalyptus camaldulensis on the structure and functioning of soil microbial communities in a sahelian soil. FEMS Microbiol Ecol 62. https://doi.org/10.1111/j.1574-6941.2007.00363.x
Knauf AE, Litton CM, Cole RJ, Sparks JP, Giardina CP, Gerow KG, Quiñones-Santiago M (2021) Nutrient-use strategy and not competition determines native and invasive species response to changes in soil nutrient availability. Restor Ecol 29:e13374. https://doi.org/10.1111/rec.13374
Levin SC, Crandall RM, Pokoski T, Stein C, Knight TM (2020) Phylogenetic and functional distinctiveness explain alien plant population responses to competition. Proc Biol Sci 287. https://doi.org/10.1098/rspb.2020.1070
Li C, Dai Q, Cheng F (2015) Effects of different karst slope farmland microtopography on soil nutrients. Chin Agric Sci Bull 31:219–225
Li J, Guo Q, Zhang J, Korpelainen H, Li C (2016a) Effects of nitrogen and phosphorus supply on growth and physiological traits of two Larix species. Environ Exp Bot 130:206–215. https://doi.org/10.1016/j.envexpbot.2016.06.006
Li M, Jordan NR, Koide RT, Yannarell AC, Davis AS (2016b) Meta-analysis of crop and weed growth responses to arbuscular mycorrhizal fungi: implications for integrated weed management. Weed Sci 64:642–652. https://doi.org/10.1614/WS-D-16-00050.1
Liu HF, Wu Y, Xu HW, Ai ZM, Zhang JY, Liu GB, Xue S (2021) Mechanistic understanding of interspecific interaction between a C4 grass and a C3 legume via arbuscular mycorrhizal fungi, as influenced by soil phosphorus availability using a C-13 and N-15 dual-labelled organic patch. Plant J 108:183–196. https://doi.org/10.1111/tpj.15434
Lu SG, Cheng Dong XU, Xiao Dong D, Yu Qing D, Yi W (2006) The impacts of the alien invasive plants on biodiversity in longitudinal range-gorge region of Southwest China. Plant Diversity 28:607
Majewska ML, Rola K, Stefanowicz AM, Nobis M, Błaszkowski J, Zubek S (2018) Do the impacts of alien invasive plants differ from expansive native ones? An experimental study on arbuscular mycorrhizal fungi communities. Biol Fertility Soils 54:631–643. https://doi.org/10.1007/s00374-018-1283-8
Malhotra H, Sharma S, Pandey R (2018) Phosphorus nutrition: plant growth in response to deficiency and excess. Springer, pp 171–190
McGilchrist C, Trenbath B (1971) A revised analysis of plant competition experiments. Biometrics: 659–671. https://doi.org/10.2307/2528603
Office NSS (1998) Chinese Soil (in Chinese). China Agriculture Press, Beijing
Ordonez A (2014) Functional and phylogenetic similarity of alien plants to co-occurring natives. Ecology 95:1191–1202. https://doi.org/10.1890/13-1002.1
Qi S, Wang J, Wan L, Dai Z, da Silva Matos DM, Du D, Egan S, Bonser SP, Thomas T, Moles AT (2022) Arbuscular mycorrhizal fungi contribute to phosphorous uptake and allocation strategies of Solidago canadensis in a phosphorous-deficient environment. Front Plant Sci 13:831654–831654. https://doi.org/10.3389/fpls.2022.831654
Qin ZF, Zhang HY, Feng G, Christie P, Zhang JL, Li XL, Gai JP (2020) Soil phosphorus availability modifies the relationship between AM fungal diversity and mycorrhizal benefits to maize in an agricultural soil. Soil Biol Biochem 144. https://doi.org/10.1016/j.soilbio.2020.107790
Raven JA, Lambers H, Smith SE, Westoby M (2018) Costs of acquiring phosphorus by vascular land plants: patterns and implications for plant coexistence. New Phytol 217:1420–1427. https://doi.org/10.1111/nph.14967
Rychter AM, Rao IM (2005) Role of phosphorus in photosynthetic carbon metabolism and partitioning. Handbook of Photosynthesis (3rd Edition). https://doi.org/10.1201/9781315372136
Scheublin TR, Van Logtestijn RS, van der Heijden MG (2007) Presence and identity of arbuscular mycorrhizal fungi influence competitive interactions between plant species. J Ecol 95:631–638. https://doi.org/10.1111/j.1365-2745.2007.01244.x
Schleuss PM, Widdig M, Heintz-Buschart A, Kirkman K, Spohn M (2020) Interactions of nitrogen and phosphorus cycling promote P acquisition and explain synergistic plant-growth responses. Ecology 101. https://doi.org/10.1002/ecy.3003
Shen K, Cornelissen JHC, Wang Y, Wu C, He Y, Ou J, Tan Q, Xia T, Kang L, Guo Y (2020) AM fungi alleviate phosphorus limitation and enhance nutrient competitiveness of invasive plants via mycorrhizal networks in karst areas. Front Ecol Evol 8:125. https://doi.org/10.3389/fevo.2020.00125
Simard SW (2009) The foundational role of mycorrhizal networks in self-organization of interior Douglas-fir forests. For Ecol Manage 258:S95–S107. https://doi.org/10.1016/j.foreco.2009.05.001
Smith SE, Read FD (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York
Standish RJ, Albornoz FE, Morald TK, Hobbs RJ, Tibbett M (2021) Mycorrhizal symbiosis and phosphorus supply determine interactions among plants with contrasting nutrient-acquisition strategies. J Ecol 109:3892–3902. https://doi.org/10.1111/1365-2745.13766
Sterner RW, Andersen T, Elser JJ, Hessen DO, Hood JM, McCauley E, Urabe J (2008) Scale-dependent carbon : nitrogen : phosphorus seston stoichiometry in marine and freshwaters. Limnol Oceanogr 53:1169–1180. https://doi.org/10.4319/lo.2008.53.3.1169
Suding KN, Seastedt LJR (2004) Competitive impacts and responses of an invasive weed: dependencies on nitrogen and phosphorus availability. Oecologia 141:526–535. https://doi.org/10.1007/s00442-004-1678-0
Sun X, Gao C, Guo LD (2013) Changes in arbuscular mycorrhizal fungus community along an exotic plant Eupatorium adenophorum invasion in a chinese secondary forest. J Microbiol 51:295–300. https://doi.org/10.1007/s12275-013-3169-7
Tao ZB, Shen CC, Qin WC, Nie BG, Chen PD, Wan JL, Zhang KP, Huang W, Siemann E (2022) Fluctuations in resource availability shape the competitive balance among non-native plant species. Ecol Appl: e2795. https://doi.org/10.1002/eap.2795
van der Putten WH, Kowalchuk GA, Brinkman EP, Doodeman GTA, van der Kaaij RM, Kamp AFD, Menting FBJ, Veenendaal EM (2007) Soil feedback of exotic savanna grass relates to pathogen absence and mycorrhizal selectivity. Ecology 88:978–988. https://doi.org/10.1890/06-1051
Ven A, Verlinden MS, Verbruggen E, Vicca S (2019) Experimental evidence that phosphorus fertilization and arbuscular mycorrhizal symbiosis can reduce the carbon cost of phosphorus uptake. Funct Ecol 33:2215–2225. https://doi.org/10.1111/1365-2435.13452
Venegas RAP, Lee SJ, Thuita M, Mlay DP, Masso C, Vanlauwe B, Rodriguez A, Sanders IR (2021) The phosphate inhibition paradigm: host and fungal genotypes determine arbuscular mycorrhizal fungal colonization and responsiveness to inoculation in cassava with increasing phosphorus supply. Front Plant Sci 12. https://doi.org/10.3389/fpls.2021.693037
Veresoglou S, Rillig M (2014) Do closely related plants host similar arbuscular mycorrhizal fungal communities? A meta-analysis. Plant Soil 377:395–406. https://doi.org/10.1007/s11104-013-2008-2
Vilà M, Weiner J (2004) Are invasive plant species better competitors than native plant species? - evidence from pair-wise experiments. Oikos 105:229–238. https://doi.org/10.1111/j.0030-1299.2004.12682.x
Wan FH, Liu WX, Guo JY, Qiang S, Li BP, Wang JJ, Yang GQ, Niu HB, Gui FR, Huang WK, Jiang ZL, Wang WQ (2010) Invasive mechanism and control strategy of Ageratina adenophora (Sprengel). Sci China Life Sci 53:1291–1298. https://doi.org/10.1007/s11427-010-4080-7
Wang G, George TS, Pan Q, Feng G, Zhang L (2022) Two isolates of Rhizophagus irregularis select different strategies for improving plants phosphorus uptake at moderate soil P availability. Geoderma 421:115910. https://doi.org/10.1016/j.geoderma.2022.115910
Wang J, Li SP, Ge Y, Wang XY, Gao S, Chen T, Yu FH (2023) Darwin’s naturalization conundrum reconciled by changes of species interactions. Ecology 104:e3850. https://doi.org/10.1002/ecy.3850
Wei Y, Wang SJ, Liu XM, Huang TZ (2012) Molecular diversity and distribution of arbuscular mycorrhizal fungi in karst ecosystem, Southwest China. Afr J Biotechnol 11:14561–14568. https://doi.org/10.5897/AJB12.587
Weremijewicz J, Sternberg LdSLOR, Janos DP (2016) Common mycorrhizal networks amplify competition by preferential mineral nutrient allocation to large host plants. New Phytol 212:461–471. https://doi.org/10.1111/nph.14041
Xia T, Wang Y, He Y, Wu C, Shen K, Tan Q, Kang L, Guo Y, Wu B, Han X (2020) An invasive plant experiences greater benefits of root morphology from enhancing nutrient competition associated with arbuscular mycorrhizae in karst soil than a native plant. PLoS One 15:e0234410. https://doi.org/10.1371/journal.pone.0234410
Yannelli FA, Koch C, Jeschke JM, Kollmann J (2017) Limiting similarity and Darwin’s naturalization hypothesis: understanding the drivers of biotic resistance against invasive plant species. Oecologia 183:775–784. https://doi.org/10.1007/s00442-016-3798-8
Yuan YG, Tang JJ, Leng D, Hu SJ, Yong JWH, Chen X (2014) An invasive plant promotes its arbuscular mycorrhizal symbioses and competitiveness through its secondary metabolites: indirect evidence from activated carbon. PLoS One 9. https://doi.org/10.1371/journal.pone.0097163
Zhang Y, Wang Y, Qiao LI, Zhang F, Wan F (2015) Mechanism of AM fungi on competitive growth between invasive plant Flaveria bidentis and native plant Setaria viridis. Acta Bot Boreali-Occidential Sinica 35:1215–1221. https://doi.org/10.7606/j.issn.1000-4025.2015.06.1215
Zhang FJ, Li Q, Chen FX, Xu HY, Inderjit, Wan FH (2017) Arbuscular mycorrhizal fungi facilitate growth and competitive ability of an exotic species Flaveria bidentis. Soil Biol Biochem 115:275–284. https://doi.org/10.1016/j.soilbio.2017.08.019
Zhang FJ, Li Q, Yerger EH, Chen X, Shi Q, Wan FH (2018) AM fungi facilitate the competitive growth of two invasive plant species, Ambrosia artemisiifolia and Bidens pilosa. Mycorrhiza 28:703–715. https://doi.org/10.1007/s00572-018-0866-4
Zhang Y, Leng Z, Wu Y, Jia H, Yan C, Wang X, Ren G, Wu G, Li J (2022) Interaction between nitrogen, phosphorus, and invasive alien plants. Sustainability 14:746. https://doi.org/10.3390/su14020746
Zhao CY, Liu YY, Shi XP, Wang YJ (2020) Effects of soil nutrient variability and competitor identify on growth and co-existence among invasive alien and native clonal plants. Environ Pollut 261. https://doi.org/10.1016/j.envpol.2019.113894
Zheng YL, Burns JH, Wang RF, Yang AD, Feng YL (2021) Identity recognition and the invasion of exotic plant. Flora 280. https://doi.org/10.1016/j.flora.2021.151828
Zhou Y, Li X, Gao Y, Liu H, Gao YB, van der Heijden MGA, Ren AZ (2018) Plant endophytes and arbuscular mycorrhizal fungi alter plant competition. Funct Ecol 32:1168–1179. https://doi.org/10.1111/1365-2435.13084
Zhu Q, Zhou Z, Shi Y, Yongbo WU, Xue J (2018) Effects of biochar-based fertilizer on phosphorus content of karst calcareous soil. Acta Ecol Sin 38:4037–4044. https://doi.org/10.5846/stxb201706161097
Acknowledgements
This study was supported by the National Natural Science Foundation of China (NSFC: 32260268), the Science and Technology Project of Guizhou Province [(2021) General-455], the Guizhou Hundred-level Innovative Talents Project [Qian-ke-he platform talents (2020) 6004], the Natural Science Project of Guizhou Minzu University [GZMUZK (2022) YB14], and the Scientific research project of Department of Water Resources of Guizhou Province [(2023) KT202313].
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Yuejun He designed this research. Tingting Xia and Kaiping Shen conducted this experiment and collected data. Xu Han, Bangli Wu, Ying Zhao, Hongchun Chen, Yan Zhao, Xihong Yang, Menglin Lei and Jiahao Xiao analyzed the data. Tingting Xia wrote the first draft of the manuscript. Yun Guo and Danmei Chen revised the manuscript. All authors contributed advice to improving this manuscript.
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Xia, T., Shen, K., Guo, Y. et al. AM fungus improves the competitiveness of a native plant against an invasive plant under moderate soil P supply. Plant Soil 492, 541–556 (2023). https://doi.org/10.1007/s11104-023-06199-w
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DOI: https://doi.org/10.1007/s11104-023-06199-w