Abstract
Aims
Understanding the distribution pattern of biodiversity in fragmented landscapes is important for conserving biodiversity. The mutualistic interaction between mycorrhizal fungi and plants is an important trait influencing ecological processes, such as plant response to environmental conditions; however, we lack a general understanding of how habitat fragmentation differently affects plant diversity of different mycorrhizal types.
Methods
The diversity of arbuscular mycorrhizal (AM) and ectomycorrhizal (EcM) plants, including the number of species on islands, the number of species per plot, and the number of individuals per plot, were calculated on 11 islands within a hydroelectric reservoir in China. We tested the influence of island attributes (island area and isolation), abiotic and biotic variables on the diversity of AM and EcM plants.
Results
There was a significant positive correlation between island area and species diversity of AM plants, but not EcM plants. After controlling for island attributes, abiotic variables and the diversity of AM fungi significantly affected the diversity of AM plants per plot. The abiotic and biotic variables explained more variance in the number of AM plant species (58%) and number of individuals of AM plants per plot (52%) than EcM plants (less than 20%). The diversity of AM plants but not EcM plants was higher in interior than in edge plots of the islands.
Conclusion
The results indicate that the decrease of plant species diversity with habitat loss was probably related to the extinction of AM plants caused by selection of abiotic variables and diversity of AM fungi.
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Data availability
The data presented in this study are available in the supplementary material.
References
Aerts R (2002) The role of various types of mycorrhizal fungi in nutrient cycling and plant competition. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Springer, Berlin, pp 117–133. https://doi.org/10.1007/978-3-540-38364-2_5
Bennett JA, Maherali H, Reinhart KO et al (2017) Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355(6321):181–184. https://doi.org/10.1126/science.aai8212
Bever JD, Dickie IA, Facelli E et al (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25(8):468–478. https://doi.org/10.1016/j.tree.2010.05.004
Boeraeve M, Honnay O, Jacquemyn H (2019) Forest edge effects on the mycorrhizal communities of the dual-mycorrhizal tree species Alnus glutinosa (L.) Gaertn. Sci Total Environ 666:703–712. https://doi.org/10.1016/j.scitotenv.2019.02.290
Bokulich NA, Subramanian S, Faith JJ et al (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10(1):57–59. https://doi.org/10.1038/nmeth.2276
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bueno CG, Meng Y, Neuenkamp L (2022) How can mycorrhizal symbiosis mediate multiple abiotic stresses in woody plants? Flora 295:152146. https://doi.org/10.1016/j.flora.2022.152146
Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information theoretic approach. Springer, Berlin
Carteron A, Vellend M, Laliberte E (2022) Mycorrhizal dominance reduces local tree species diversity across US forests. Nat Ecol Evol 6(4):370–374. https://doi.org/10.1038/s41559-021-01634-6
Chapman SK, Langley JA, Hart SC, Koch GW (2005) Plants actively control nitrogen cycling: uncorking the microbial bottleneck. New Phytol 169(1):27–34. https://doi.org/10.1111/j.1469-8137.2005.01571.x
Chase JM, Blowes SA, Knight TM, Gerstner K, May F (2020) Ecosystem decay exacerbates biodiversity loss with habitat loss. Nature 584(7820):238–243. https://doi.org/10.1038/s41586-020-2531-2
Chaudhary VB, Nolimal S, Sosa-Hernandez MA, Egan C, Kastens J (2020) Trait-based aerial dispersal of arbuscular mycorrhizal fungi. New Phytol 228:238–252. https://doi.org/10.1111/nph.16667
Corrales A, Henkel TW, Smith ME (2018) Ectomycorrhizal associations in the tropics - biogeography, diversity patterns and ecosystem roles. New Phytol 220(4):1076–1091. https://doi.org/10.1111/nph.15151
Crockatt ME (2012) Are there edge effects on forest fungi and if so do they matter? Fungal Bio Rev 26(2–3):94–101. https://doi.org/10.1016/j.fbr.2012.08.002
Davison J, Moora M, Opik M et al (2018) Microbial island biogeography: isolation shapes the life history characteristics but not diversity of root-symbiotic fungal communities. ISME J 12(9):2211–2224. https://doi.org/10.1038/s41396-018-0196-8
Delavaux CS, Smith-Ramesh LM, Kuebbing SE (2017) Beyond nutrients: a meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 98(8):2111–2119. https://doi.org/10.1002/ecy.1892
Delavaux CS, Weigelt P, Dawson W et al (2019) Mycorrhizal fungi influence global plant biogeography. Nat Ecol Evol 3(3):424–429. https://doi.org/10.1038/s41559-019-0823-4
Delavaux CS, Weigelt P, Dawson W et al (2021) Mycorrhizal types influence island biogeography of plants. Commun Biol 4(1):1128. https://doi.org/10.1038/s42003-021-02649-2
Delavaux CS, Weigelt P, Magnoli SM et al (2022) Nitrogen-fixing symbiotic bacteria act as a global filter for plant establishment on islands. Commun Biol 5(1):1209. https://doi.org/10.1038/s42003-022-04133-x
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. https://doi.org/10.1038/nmeth.2604
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Franklin O, Nasholm T, Hogberg P, Hogberg MN (2014) Forests trapped in nitrogen limitation--an ecological market perspective on ectomycorrhizal symbiosis. New Phytol 203(2):657–666. https://doi.org/10.1111/nph.12840
Grilli G, Longo S, Huais PY et al (2017) Fungal diversity at fragmented landscapes: synthesis and future perspectives. Curr Opin Microbiol 37:161–165. https://doi.org/10.1016/j.mib.2017.09.003
Hart MM, Reader RJ, Klironomos J (2001) Life-history strategies of arbuscular mycorrhizal fungi in relation to their successional dynamics. Mycologia 93(6):1186–1194. https://doi.org/10.2307/3761678
House GL, Bever JD (2018) Disturbance reduces the differentiation of mycorrhizal fungal communities in grasslands along a precipitation gradient. Ecol Appl 28(3):736–748. https://doi.org/10.1002/eap.1681
Keller AB, Phillips RP (2019) Leaf litter decay rates differ between mycorrhizal groups in temperate, but not tropical, forests. New Phytol 222(1):556–564. https://doi.org/10.1111/nph.15524
Kiesewetter KN, Afkhami ME (2021) Microbiome-mediated effects of habitat fragmentation on native plant performance. New Phytol 232(4):1823–1838. https://doi.org/10.1111/nph.17595
Koljalg U, Nilsson RH, Abarenkov K et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22(21):5271–5277. https://doi.org/10.1111/mec.12481
Krishnadas M, Comita LS (2019) Edge effects on seedling diversity are mediated by impacts of fungi and insects on seedling recruitment but not survival. Front For Glob Chang 2:76. https://doi.org/10.3389/ffgc.2019.00076
Krishnadas M, Stump SM (2021) Dispersal limitation and weaker stabilizing mechanisms mediate loss of diversity with edge effects in forest fragments. J Ecol 109(5):2137–2151. https://doi.org/10.1111/1365-2745.13626
Krishnadas M, Bagchi R, Sridhara S, Comita LS (2018) Weaker plant-enemy interactions decrease tree seedling diversity with edge-effects in a fragmented tropical forest. Nat Commun 9(1):4523. https://doi.org/10.1038/s41467-018-06997-2
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82(13):1–25. https://doi.org/10.18637/jss.v082.i1
Li SP, Wang P, Chen Y et al (2020) Island biogeography of soil bacteria and fungi: similar patterns, but different mechanisms. ISME J 14(7):1886–1896. https://doi.org/10.1038/s41396-020-0657-8
Li T, Li X, Wu C et al (2022) Herbivory rather than root competition and environmental factors determines plant establishment in fragmented forests. Forests 13(5):767. https://doi.org/10.3390/f13050767
Liu J, Vellend M, Wang Z, Yu M (2018) High beta diversity among small islands is due to environmental heterogeneity rather than ecological drift. J Biogeogr 45:2252–2261. https://doi.org/10.1111/jbi.13404
Liu J, Coomes DA, Hu G et al (2019) Larger fragments have more late-successional species of woody plants than smaller fragments after 50 years of secondary succession. J Ecol 107(2):582–594. https://doi.org/10.1111/1365-2745.13071
Liu Y, Li X, Kou Y (2020) Ectomycorrhizal fungi: participation in nutrient turnover and community assembly pattern in forest ecosystems. Forests 11(4):453. https://doi.org/10.3390/f11040453
Liu J, Matthews TJ, Zhong L et al (2020a) Environmental filtering underpins the island species–area relationship in a subtropical anthropogenic archipelago. J Ecol 108(108):424–432. https://doi.org/10.1111/1365-2745.13272
Liu J, Zhong Y, Zhong L et al (2020b) The asymmetric relationships of the distribution of conspecific saplings and adults in forest fragments. J Plant Ecol 13(4):398–404. https://doi.org/10.1093/jpe/rtaa026
Liu J, MacDonald ZG, Si X et al (2022) SLOSS-based inferences in a fragmented landscape depend on fragment area and species-area slope. J Biogeogr 49:1075–1085. https://doi.org/10.1111/jbi.14366
Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Miller-Rushing AJ, Primack RB, Devictor V et al (2019) How does habitat fragmentation affect biodiversity? A controversial question at the core of conservation biology. Biol Conserv 232:271–273. https://doi.org/10.1016/j.biocon.2018.12.029
Nguyen NH, Song Z, Bates ST et al (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006
Oksanen J, Blanchet FG, Kindt R et al (2013) Vegan: community ecology package. In. R package version 2.0–10
Ruffell J, Didham RK (2016) Towards a better mechanistic understanding of edge effects. Landsc Ecol 31(10):2205–2213. https://doi.org/10.1007/s10980-016-0397-3
Soudzilovskaia NA, Vaessen S, Barcelo M et al (2020) FungalRoot: global online database of plant mycorrhizal associations. New Phytol 227(3):955–966. https://doi.org/10.1111/nph.16569
Tedersoo L, Bahram M, Zobel M (2020) How mycorrhizal associations drive plant population and community biology. Science 367(6480):eaba1223. https://doi.org/10.1126/science.aba1223
Teste FP, Jones MD, Dickie IA (2020) Dual-mycorrhizal plants: their ecology and relevance. New Phytol 225(5):1835–1851. https://doi.org/10.1111/nph.16190
van der Heijden MGA, Klironomos JN, Ursic M et al (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396(6706):69–72. https://doi.org/10.1038/23932
van der Heijden MGA, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205(4):1406–1423. https://doi.org/10.1111/nph.13288
Viji R, Rajesh PP (2011) Assessment of water holding capacity of major soil series of Lalgudi, Trichy, India. J Environ Res Develop 7:393–398
Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16(5):299–363. https://doi.org/10.1007/s00572-005-0033-6
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 73(16):5261–5267. https://doi.org/10.1128/AEM.00062-07
Wardle DA, Lindahl BD (2014) Global diversity and geography of soil fungi. Science 346(6213):1256688. https://doi.org/10.1126/science.aaa1185
Willing CE, Pierroz G, Guzman A et al (2021) Keep your friends close: host compartmentalisation of microbial communities facilitates decoupling from effects of habitat fragmentation. Ecol Lett 24(12):2674–2686. https://doi.org/10.1111/ele.13886
Wilson MC, Chen X-Y, Corlett RT et al (2016) Habitat fragmentation and biodiversity conservation: key findings and future challenges. Landsc Ecol 31(2):219–227. https://doi.org/10.1007/s10980-015-0312-3
Zhang H-Y, Lü X-T, Hartmann H et al (2018) Foliar nutrient resorption differs between arbuscular mycorrhizal and ectomycorrhizal trees at local and global scales. Glob Ecol Biogeogr 27(7):875–885. https://doi.org/10.1111/geb.12738
Zhong Y, Chu C, Myers JA et al (2021) Arbuscular mycorrhizal trees influence the latitudinal beta-diversity gradient of tree communities in forests worldwide. Nat Commun 12(1):3137. https://doi.org/10.1038/s41467-021-23236-3
Acknowledgments
We thank Wenjie Deng, Tengteng Liu, and Weiyong Liu and many students at the Wenzhou University and Zhejiang University, and many local farmers for their contribution to the fieldwork. We thank Xin’an River Ecological Development Group Corporation and the Forestry Bureau of Chun’an County for the permits necessary to conduct our research in Thousand Island Lake. This research was funded by the Zhejiang Provincial Natural Science Foundation of China (grant number: LY21C030003), National Natural Science Foundation of China (grant number: 32271606, 32101269, 31930073), and “Pioneer” and “Leading Goose” R&D Program of Zhejiang (2023C03137).
Funding
This work was supported by the Zhejiang Provincial Natural Science Foundation of China (grant number: LY21C030003), National Natural Science Foundation of China (grant numbers: 32271606, 32101269, and 31930073), and “Pioneer” and “Leading Goose” R&D Program of Zhejiang (2023C03137).
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All authors contributed to the study conception and design. Conceptualization of the project was led by Jinliang Liu. Data collection and analysis were performed by Xue Li, Tianxiang Li, Lei Zhong, Jing Guo, and Mingjian Yu. Data analysis was performed by Xue Li and Jinliang Liu. The first draft of the manuscript was written by Jinliang Liu and Xue Li. All authors commented on previous versions of the manuscript and gave final approval for publication.
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Supplementary Information
Appendix S1
Plant species list and the references for mycorrhiza type. (XLSX 105 kb)
Appendix S2
The abiotic variables in 32 plots on 11 islands. (XLSX 13 kb)
Appendix S3
The biotic variables in 32 plots on 11 islands. (XLSX 12 kb)
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Li, X., Li, T., Zhong, L. et al. Species diversity of arbuscular mycorrhizal but not ectomycorrhizal plants decreases with habitat loss due to environmental filtering. Plant Soil 489, 211–224 (2023). https://doi.org/10.1007/s11104-023-06007-5
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DOI: https://doi.org/10.1007/s11104-023-06007-5