The invasive cactus Opuntia stricta creates fertility islands in African savannas and benefits from those created by native trees
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
34675315
PubMed Central
PMC8531129
DOI
10.1038/s41598-021-99857-x
PII: 10.1038/s41598-021-99857-x
Knihovny.cz E-zdroje
- MeSH
- ekosystém MeSH
- Opuntia fyziologie MeSH
- půda chemie MeSH
- půdní mikrobiologie MeSH
- stromy * fyziologie MeSH
- voda analýza MeSH
- zavlečené druhy * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Jihoafrická republika MeSH
- Názvy látek
- půda MeSH
- voda MeSH
The patchy distribution of trees typical of savannas often results in a discontinuous distribution of water, nutrient resources, and microbial communities in soil, commonly referred to as "islands of fertility". We assessed how this phenomenon may affect the establishment and impact of invasive plants, using the invasion of Opuntia stricta in South Africa's Kruger National Park as case study. We established uninvaded and O. stricta-invaded plots under the most common woody tree species in the study area (Vachellia nilotica subsp. kraussiana and Spirostachys africana) and in open patches with no tree cover. We then compared soil characteristics, diversity and composition of the soil bacterial communities, and germination performance of O. stricta and native trees between soils collected in each of the established plots. We found that the presence of native trees and invasive O. stricta increases soil water content and nutrients, and the abundance and diversity of bacterial communities, and alters soil bacterial composition. Moreover, the percentage and speed of germination of O. stricta were higher in soils conditioned by native trees compared to soils collected from open patches. Finally, while S. africana and V. nilotica trees appear to germinate equally well in invaded and uninvaded soils, O. stricta had lower and slower germination in invaded soils, suggesting the potential release of phytochemicals by O. stricta to avoid intraspecific competition. These results suggest that the presence of any tree or shrub in savanna ecosystems, regardless of origin (i.e. native or alien), can create favourable conditions for the establishment and growth of other plants.
Department of Biological Sciences Macquarie University Sydney NSW 2109 Australia
Department of Botany and Zoology Stellenbosch University Stellenbosch South Africa
Department of Ecology Faculty of Science Charles University Viničná 7 128 44 Prague Czech Republic
Scientific Services South African National Parks P Bag X402 Skukuza 1350 South Africa
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Pyšek P, et al. Naturalized alien flora of the world. Preslia. 2017;89:203–274. doi: 10.23855/preslia.2017.203. DOI
Pyšek, P. et al. Scientists’ warning on invasive alien species. Biol. Rev. (2020). PubMed PMC
Vilà M, et al. Ecological impacts of invasive alien plants: A meta-analysis of their effects on species, communities and ecosystems. Ecol. Lett. 2011;14:702–708. doi: 10.1111/j.1461-0248.2011.01628.x. PubMed DOI
Pyšek P, et al. A global assessment of invasive plant impacts on resident species, communities and ecosystems: The interaction of impact measures, invading species’ traits and environment. Glob. Chang. Biol. 2012;18:1725–1737. doi: 10.1111/j.1365-2486.2011.02636.x. PubMed DOI
Le Roux JJ, et al. Recent anthropogenic plant extinctions differ in biodiversity hotspots and coldspots. Curr. Biol. 2019;29:2912–2918.e2. doi: 10.1016/j.cub.2019.07.063. PubMed DOI
Hulme PE, et al. Greater focus needed on alien plant impacts in protected areas. Conserv. Lett. 2014;7:459–466. doi: 10.1111/conl.12061. DOI
Foxcroft LC, Pyšek P, Richardson DM, Genovesi P, MacFadyen S. Plant invasion science in protected areas: progress and priorities. Biol. Invasions. 2017;19:1353–1378. doi: 10.1007/s10530-016-1367-z. DOI
Novoa A, et al. Invasion syndromes: A systematic approach for predicting biological invasions and facilitating effective management. Biol. Invasions. 2020;22:1801–1820. doi: 10.1007/s10530-020-02220-w. DOI
Foxcroft LC, Pickett STA, Cadenasso ML. Expanding the conceptual frameworks of plant invasion ecology. Perspect. Plant Ecol. Evol. Syst. 2011;13:89–100. doi: 10.1016/j.ppees.2011.03.004. DOI
Scholes RJ, Archer SR. Tree-grass interactions in savannas. Annu. Rev. Ecol. Syst. 1997;28:517–544. doi: 10.1146/annurev.ecolsys.28.1.517. DOI
Millennium Ecosystem Assessment . Ecosystems and Human Well-Being: Biodiversity Synthesis. Island Press; 2005.
Foxcroft LC, Richardson DM, Rejmánek M, Pyšek P. Alien plant invasions in tropical and sub-tropical savannas: Patterns, processes and prospects. Biol. Invasions. 2010;12:3913–3933. doi: 10.1007/s10530-010-9823-7. DOI
Rejmánek M, Huntley BJ, Le Roux JJ, Richardson DM. A rapid survey of the invasive plant species in western Angola. Afr. J. Ecol. 2017;55:56–69. doi: 10.1111/aje.12315. DOI
Shackleton RT, Foxcroft LC, Pyšek P, Wood LE, Richardson DM. Assessing biological invasions in protected areas after 30 years: Revisiting nature reserves targeted by the 1980s SCOPE programme. Biol. Conserv. 2020;243:108424. doi: 10.1016/j.biocon.2020.108424. DOI
Skarpe C. Dynamics of savanna ecosystems. J. Veg. Sci. 1992;3:293–300. doi: 10.2307/3235754. DOI
Okin GS, et al. Spatial patterns of soil nutrients in two southern African savannas. J. Geophys. Res. Biogeosci. 2008;113:G2. doi: 10.1029/2007JF000758. DOI
Ridolfi L, Laio F, D’Odorico P. Fertility island formation and evolution in dryland ecosystems. Ecol. Soc. 2008;13:5. doi: 10.5751/ES-02302-130105. DOI
Perroni-Ventura Y, Montaña C, Garcí-a-Oliva F. Carbon-nitrogen interactions in fertility island soil from a tropical semi-arid ecosystem. Funct. Ecol. 2010;24:233–242. doi: 10.1111/j.1365-2435.2009.01610.x. DOI
Belnap J, Susan LP. Soil biota in an ungrazed grassland: response to annual grass (Bromus tectorum) invasion. Ecol. Appl. 2001;51:1261–1275. doi: 10.1890/1051-0761(2001)011[1261:SBIAUG]2.0.CO;2. DOI
Ludwig F, Kroon H, Prins HHT, Berendse F. Effects of nutrients and shade on tree-grass interactions in an East African savanna. J. Veg. Sci. 2001;12:579–588. doi: 10.2307/3237009. DOI
Reinhart KO, Callaway RM. Soil biota and invasive plants. New Phytol. 2006;170:445–457. doi: 10.1111/j.1469-8137.2006.01715.x. PubMed DOI
Weidenhamer JD, Callaway RM. Direct and indirect effects of invasive plants on soil chemistry and ecosystem function. J. Chem. Ecol. 2010;36:59–69. doi: 10.1007/s10886-009-9735-0. PubMed DOI
Levine JM, Pachepsky E, Kendall BE, Yelenik SG, Lambers JHR. Plant-soil feedbacks and invasive spread. Ecol. Lett. 2006;9:1005–1014. doi: 10.1111/j.1461-0248.2006.00949.x. PubMed DOI
du Toit, J. T., Rogers, K. H. & Biggs, H. C. The Kruger Experience: Ecology and Management of Savanna Heterogeneity. (Island Press, 2003).
Foxcroft LC, Van Wilgen NJ, Baard JA, Cole NS. Biological invasions in South African National Parks. Bothalia. 2017;47:11. doi: 10.4102/abc.v47i2.2158. DOI
Pyšek P, et al. Into the great wide open: do alien plants spread from rivers to dry savanna in the Kruger National Park? NeoBiota. 2020;60:61–77. doi: 10.3897/neobiota.60.54608. DOI
Kueffer C, Pyšek P, Richardson DM. Integrative invasion science: Model systems, multi-site studies, focused meta-analysis and invasion syndromes. New Phytol. 2013;200:615–633. doi: 10.1111/nph.12415. PubMed DOI
Lotter WD, Hoffmann JH. An integrated management plan for the control of Opuntia stricta (Cactaceae) in the Kruger National Park, South Africa. Koedoe. 1998;41:63–68. doi: 10.4102/koedoe.v41i1.247. DOI
Hoffmann JH, Moran VC, Zimmermann HG, Impson FAC. Biocontrol of a prickly pear cactus in South Africa: Reinterpreting the analogous, renowned case in Australia. J. Appl. Ecol. 2020;13737:1365–2664.
Foxcroft LC, Rouget M, Richardson DM, MacFadyen S. Reconstructing 50 years of Opuntia stricta invasion in the Kruger National Park, South Africa: Environmental determinants and propagule pressure. Divers. Distrib. 2004;10:427–437. doi: 10.1111/j.1366-9516.2004.00117.x. DOI
Novoa A, Le Roux JJ, Robertson MP, Wilson JRU, Richardson DM. Introduced and invasive cactus species: A global review. AoB Plants. 2015;7:1. doi: 10.1093/aobpla/plu078. PubMed DOI PMC
Foxcroft LC, Hoffmann JH, Viljoen JJ, Kotze JJ. Environmental factors influencing the distribution of Opuntia stricta, an invasive alien plant in the Kruger National Park, South Africa. S. Afr. J. Bot. 2007;73:109–112. doi: 10.1016/j.sajb.2006.09.008. DOI
Foxcroft LC, Rejmánek M. What helps Opuntia stricta invade Kruger National Park, South Africa: Baboons or elephants? Appl. Veg. Sci. 2007;10:265–270. doi: 10.1111/j.1654-109X.2007.tb00525.x. DOI
Anderson, E. F. The Cactus Family. (Timber Press, 2001).
Reyes-Agüero JA, Aguirre RJR, Valiente-Banuet A. Reproductive biology of Opuntia: A review. J. Arid Environ. 2006;64:549–585. doi: 10.1016/j.jaridenv.2005.06.018. DOI
Robertson MP, et al. Assessing local scale impacts of Opuntia stricta (Cactaceae) invasion on beetle and spider diversity in Kruger National Park, South Africa. Afr. Zool. 2011;46:205–223. doi: 10.3377/004.046.0202. DOI
Butterfield BJ, Briggs JM. Patch dynamics of soil biotic feedbacks in the Sonoran Desert. J. Arid Environ. 2009;73:96–102. doi: 10.1016/j.jaridenv.2008.09.012. DOI
Neffar, S., Chenchouni, H., Beddiar, A. & Redjel, N. Rehabilitation of degraded rangeland in drylands by Prickly Pear (Opuntia ficus-indica L.) plantations: Effect on soil and spontaneous vegetation. Ecol. Balk.5, 63–76 (2013).
Garner W, Steinberger Y. A proposed mechanism for the formation of ‘Fertile Islands’ in the desert ecosystem. J. Arid Environ. 1989;16:257–262. doi: 10.1016/S0140-1963(18)30941-8. DOI
Marchante, H., Elizabete M, & Helena, F. Invasion of the Portuguese dune ecosystems by the exotic species Acacia longifolia (Andrews) Willd.: effects at the community level. Plant invasions: ecological threats and management solutions. pp. 75–85 (2003).
Marchante E, et al. Short-and long-term impacts of Acacia longifolia invasion on the belowground processes of a Mediterranean coastal dune ecosystem. Appl. Soil Ecol. 2008;40(2):210–217. doi: 10.1016/j.apsoil.2008.04.004. DOI
Yelenik SG, Stock WD, Richardson DM. Ecosystem level impacts of invasive Acacia saligna in the South African fynbos. Restor. Ecol. 2004;12(1):44–51. doi: 10.1111/j.1061-2971.2004.00289.x. DOI
Werner C, et al. High competitiveness of a resource demanding invasive acacia under low resource supply. Plant. Ecol. 2010;206(1):83–96. doi: 10.1007/s11258-009-9625-0. DOI
Le Maitre DC, et al. Impacts of invasive Australian acacias: implications for management and restoration. Divers. Distrib. 2011;17(5):1015–1029. doi: 10.1111/j.1472-4642.2011.00816.x. DOI
Bargali K, Bargali SS. Acacia nilotica: a multipurpose leguminous plant. Nat. Sci. 2009;7:11–19.
Rughöft S, et al. Community composition and abundance of bacterial, archaeal and nitrifying populations in savanna soils on contrasting bedrock material in Kruger National Park, South Africa. Front. Microbiol. 2016;7:1638. PubMed PMC
Neilson JW, et al. Life at the hyperarid margin: Novel bacterial diversity in arid soils of the Atacama Desert, Chile. Extremophiles. 2012;16:553–566. doi: 10.1007/s00792-012-0454-z. PubMed DOI
de Vos, P. et al. The Firmicutes. Bergey’s Manual of Systematic Bacteriology. (Springer, 2009).
Brockett BFT, Prescott CE, Grayston SJ. Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol. Biochem. 2012;44:9–20. doi: 10.1016/j.soilbio.2011.09.003. DOI
Yang Y, Dou Y, An S. Testing association between soil bacterial diversity and soil carbon storage on the Loess Plateau. Sci. Total Environ. 2018;626:48–58. doi: 10.1016/j.scitotenv.2018.01.081. PubMed DOI
Rajaniemi TK, Allison VJ. Abiotic conditions and plant cover differentially affect microbial biomass and community composition on dune gradients. Soil Biol. Biochem. 2009;41:102–109. doi: 10.1016/j.soilbio.2008.10.001. DOI
Novoa, A., Rodríguez, R., Richardson, D. & González, L. Soil quality: A key factor in understanding plant invasion? The case of Carpobrotus edulis (L.) N.E.Br. Biol. Invasions16, 429–443 (2014).
Penfield S. Seed dormancy and germination. Curr. Biol. 2017;27:R874–R878. doi: 10.1016/j.cub.2017.05.050. PubMed DOI
Tielbörger K, Prasse R. Do seeds sense each other? Testing for density-dependent germination in desert perennial plants. Oikos. 2009;118:792–800. doi: 10.1111/j.1600-0706.2008.17175.x. DOI
Renne IJ, et al. Eavesdropping in plants: delayed germination via biochemical recognition. J. Ecol. 2014;102:86–94. doi: 10.1111/1365-2745.12189. DOI
Yannelli FA, Novoa A, Lorenzo P, Rodríguez J, Le Roux JJ. No evidence for novel weapons: biochemical recognition modulates early ontogenetic processes in native species and invasive acacias. Biol. Invasions. 2020;22:549–562. doi: 10.1007/s10530-019-02110-w. DOI
Al-Wakeel SAM, Gabr MA, Hamid AA, Abu-El-Soud WM. Allelopathic effects of Acacia nilotica leaf residue on Pisum sativum L. Allelopath. J. 2007;19:411.
Scholes, M. C., Scholes, R. J., Otter, L. B. & Woghiren, A. J. Biogeochemistry: The cycling of elements. in The Kruger Experience: Ecology and Management of Savanna Heterogeneity (eds. du Toit, J. T., Rogers, K. H. & Biggs, H. C.) 130–148 (Island Press, 2003).
Kyalangalilwa B, Boatwright JS, Daru BH, Maurin O, van der Bank M. Phylogenetic position and revised classification of Acacia s.l. (Fabaceae: Mimosoideae) in Africa, including new combinations in Vachellia and Senegalia. Bot. J. Linn. Soc. 2013;172:500–523. doi: 10.1111/boj.12047. DOI
van Wyk, B. & van Wyk, P. Field Guide to Trees of Southern Africa. (Struik Nature, 2013).
Coates Palgrave, K. & Coates Palgrave, M. Palgrave’s Trees of Southern Africa. (Struik Publishers, 2002).
Novoa A, Kumschick S, Richardson DM, Rouget M, Wilson JRU. Native range size and growth form in Cactaceae predict invasiveness and impact. NeoBiota. 2016;30:75–90. doi: 10.3897/neobiota.30.7253. DOI
Allen, S. E. Chemical Analysis of Ecological Materials. (Blackwell Scientific Publications, 1989).
Tabatabai MA, Bremner JM. Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol. Biochem. 1969;1:301–307. doi: 10.1016/0038-0717(69)90012-1. DOI
Kandeler E, Gerber H. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol. Fertil. Soils. 1988;6:68–72. doi: 10.1007/BF00257924. DOI
Allison SD, Vitousek PM. Extracellular enzyme activities and carbon chemistry as drivers of tropical plant litter decomposition. Biotropica. 2004;36:285–296.
German DP, Chacon SS, Allison SD. Substrate concentration and enzyme allocation can affect rates of microbial decomposition. Ecology. 2011;92:1471–1480. doi: 10.1890/10-2028.1. PubMed DOI
Lane DJ, et al. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc. Natl. Acad. Sci. 1985;82:6955–6959. doi: 10.1073/pnas.82.20.6955. PubMed DOI PMC
Tringe SG, Hugenholtz P. A renaissance for the pioneering 16S rRNA gene. Curr. Opin. Microbiol. 2008;11:442–446. doi: 10.1016/j.mib.2008.09.011. PubMed DOI
Bukin YS, et al. The effect of 16s rRNA region choice on bacterial community metabarcoding results. Sci. Data. 2019;6:1–14. doi: 10.1038/sdata.2019.7. PubMed DOI PMC
Chakravorty S, Helb D, Burday M, Connell N, Alland D. A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J. Microbiol. Methods. 2007;69:330–339. doi: 10.1016/j.mimet.2007.02.005. PubMed DOI PMC
Beckers B, et al. Performance of 16s rDNA primer pairs in the study of rhizosphere and endosphere bacterial microbiomes in metabarcoding studies. Front. Microbiol. 2016;7:1–15. doi: 10.3389/fmicb.2016.00650. PubMed DOI PMC
Thijs S, et al. Comparative evaluation of four bacteria-specific primer pairs for 16S rRNA gene surveys. Front. Microbiol. 2017;8:1–15. doi: 10.3389/fmicb.2017.00494. PubMed DOI PMC
Schloss PD, Westcott SL. Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl. Environ. Microbiol. 2011;77(10):3219–3226. doi: 10.1128/AEM.02810-10. PubMed DOI PMC
Schloss PD, et al. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 2009;75:7537–7541. doi: 10.1128/AEM.01541-09. PubMed DOI PMC
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–2200. doi: 10.1093/bioinformatics/btr381. PubMed DOI PMC
Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007;73:5261–5267. doi: 10.1128/AEM.00062-07. PubMed DOI PMC
McMurdie PJ, Holmes S. Waste not, want not: Why rarefying microbiome data is inadmissible. PLoS Comput. Biol. 2014;10:e1003531. doi: 10.1371/journal.pcbi.1003531. PubMed DOI PMC
Weiss S, et al. Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome. 2017;5:1–18. doi: 10.1186/s40168-017-0237-y. PubMed DOI PMC
de Cárcer DA, Denman SE, McSweeney C, Morrison M. Evaluation of subsampling-based normalization strategies for tagged high-throughput sequencing data sets from gut microbiomes. Appl. Environ. Microbiol. 2011;77:8795–8798. doi: 10.1128/AEM.05491-11. PubMed DOI PMC
Chiapusio G, Sánchez AM, Reigosa MJ, González L, Pellissier F. Do germination indices adequately reflect allelochemical effects on the germination process? J. Chem. Ecol. 1997;23:2445–2453. doi: 10.1023/B:JOEC.0000006658.27633.15. DOI
Oksanen, J. F. et al.vegan: Community Ecology Package. R package version 2.3-3. (2016).
Jost L. Entropy and diversity. Oikos. 2006;113:363–375. doi: 10.1111/j.2006.0030-1299.14714.x. DOI
Jost L. The relation between evenness and diversity. Diversity. 2010;2:207–232. doi: 10.3390/d2020207. DOI
Jost L. Partitioning diversity into independent alpha and beta components. Ecology. 2007;88:2427–2439. doi: 10.1890/06-1736.1. PubMed DOI
Charney, N. & Record, S. vegetarian: Jost Diversity Measures for Community Data. R package version 1.2. (2012).
Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 2001;26:32–46.
Segata N, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:1–18. doi: 10.1186/1465-6906-12-S1-P1. PubMed DOI PMC
Clarke KR. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 1993;18:117–143. doi: 10.1111/j.1442-9993.1993.tb00438.x. DOI