Older populations of the invader Solidago canadensis exhibit stronger positive plant-soil feedbacks and competitive ability in China.
common-garden experiment
pathogens
plant invasion success
plant-soil feedback
soil microbial communities
soil microbiomes
Journal
American journal of botany
ISSN: 1537-2197
Titre abrégé: Am J Bot
Pays: United States
ID NLM: 0370467
Informations de publication
Date de publication:
08 2022
08 2022
Historique:
revised:
08
06
2022
received:
06
03
2022
accepted:
10
06
2022
pubmed:
13
7
2022
medline:
1
9
2022
entrez:
12
7
2022
Statut:
ppublish
Résumé
The enemy release hypothesis predicts that release from natural enemies, including soil-borne pathogens, liberates invasive plants from a negative regulating force. Nevertheless, invasive plants may acquire novel enemies and mutualists in the introduced range, which may cause variable effects on invader growth. However, how soil microorganisms may influence competitive ability of invasive plants along invasion chronosequences has been little explored. Using the invasive plant Solidago canadensis, we tested whether longer residence times are associated with stronger negative plant-soil feedbacks and thus weaker competitive abilities at the individual level. We grew S. canadensis individuals from 36 populations with different residence times across southeastern China in competition versus no competition and in three different types of soils: (1) conspecific rhizospheric soils; (2) soils from uninvaded patches; and (3) sterilized soil. For our competitor treatments, we constructed synthetic communities of four native species (Bidens parviflora, Solanum nigrum, Kalimeris indica, and Mosla scabra), which naturally co-occur with Solidago canadensis in the field. Solidago canadensis populations with longer residence times experienced stronger positive plant-soil feedbacks and had greater competitive responses (i.e., produced greater above-ground biomass and grew taller) in conspecific rhizospheric soils than in sterilized or uninvaded soils. Moreover, S. canadensis from older populations significantly suppressed above-ground biomass of the native communities in rhizospheric and uninvaded soils but not in sterilized soil. The present results suggest that older populations of S. canadensis experience stronger positive plant-soil feedbacks, which may enhance their competitive ability against native plant communities.
Substances chimiques
Soil
0
Banques de données
Dryad
['10.5061/dryad.z08kprrg2']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1230-1241Informations de copyright
© 2022 Botanical Society of America.
Références
Allen, W. J., A. E. DeVries, N. J. Bologna, W. A. Bickford, K. P. Kowalski, L. A. Meyerson, and J. T. Cronin. 2020. Intraspecific and biogeographical variation in foliar fungal communities and pathogen damage of native and invasive Phragmites australis. Global Ecology and Biogeography 29: 1199-1211.
Allen, W. J., L. A. Meyerson, D. Cummings, J. Anderson, G. P. Bhattarai, and J. T. Cronin. 2017. Biogeography of a plant invasion: drivers of latitudinal variation in enemy release. Global Ecology and Biogeography 26: 435-446.
Armas, C., R. Ordiales, and F. I. Pugnaire. 2004. Measuring plant interactions: a new comparative index. Ecology 85: 2682-2686.
Barton, N. H. 1999. Clines in polygenic traits. Genetics Research 74: 223-236.
Beckstead, J., and I. M. Parker. 2003. Invasiveness of Ammophila arenaria: Release from soil-borne pathogens? Ecology 84: 2824-2831.
Bever, J. D. 2003. Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytologist 157: 465-473.
Bezemer, T. M., J. Jing, J. M. T. Bakx-Schotman, and E.-J. Bijleveld. 2018. Plant competition alters the temporal dynamics of plant-soil feedbacks. Journal of Ecology 106: 2287-2300.
Blossey, B., and R. Nötzold. 1995. Evolution of increased competitive ability in invasive non-indigenous plants: a hypothesis. Journal of Ecology 83: 887-889.
Boheemen, L.van, D. Atwater, and K. Hodgins. 2019. Rapid and repeated local adaptation to climate in an invasive plant. New Phytologist 222: 614-627.
Buerdsell, S. L., B. G. Milligan, and E. A. Lehnhoff. 2021. Invasive plant benefits a native plant through plant-soil feedback but remains the superior competitor. NeoBiota 64: 119-136.
Casper, B. B., and J. P. Castelli. 2007. Evaluating plant-soil feedback together with competition in a serpentine grassland. Ecology Letters 10: 394-400.
Day, N. J., K. E. Dunfield, and P. M. Antunes. 2015. Temporal dynamics of plant-soil feedback and root-associated fungal communities over 100 years of invasion by a non-native plant. Journal of Ecology 103: 1557-1569.
De la Peña, E., N. de Clercq, D. Bonte, S. Roiloa, S. Rodríguez-Echeverría, and H. Freitas. 2010. Plant-soil feedback as a mechanism of invasion by Carpobrotus edulis. Biological Invasions 10: 3637-3648.
DeWalt, S. J., J. S. Denslow, and K. Ickes. 2004. Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology 85: 471-483.
Diagne, C., B. Leroy, A.-C. Vaissière, R. E. Gozlan, D. Roiz, I. Jarić, J.-M. Salles, et al. 2021. High and rising economic costs of biological invasions worldwide. Nature 592: 571-576.
Diez, J. M., I. A. Dickie, G. Edwards, P. E. Hulme, J. J. Sullivan, and R. P. Duncan. 2010. Negative soil feedbacks accumulate over time for non-native plant species. Ecology Letters 13: 803-809.
Dong, L.-J., Z.-K. Sun, Y. Gao, and W.-M. He. 2015. Two-year interactions between invasive Solidago canadensis and soil decrease its subsequent growth and competitive ability. Journal of Plant Ecology 8: 617-622.
Dong, L.-J., J.-X. Yang, H.-W. Yu, and W.-M. He. 2017. Dissecting Solidago canadensis-soil feedback in its real invasion. Ecology and Evolution 7: 2307-2315.
Dong, L.-J., H.-W. Yu, and W.-M. He. 2015. What determines positive, neutral, and negative impacts of Solidago canadensis invasion on native plant species richness? Scientific Reports 5: 16804.
Dostál, P., J. Müllerová, P. Pyšek, J. Pergl, and T. Klinerová. 2013. The impact of an invasive plant changes over time. Ecology Letters 16: 1277-1284.
Elton, C. S. 1958. The ecology of invasion by animals and plants. Chapman and Hall, London, UK.
Eppinga, M. B., M. Rietkerk, S. C. Dekker, P. C. De Ruiter, and W. H. Van der Putten. 2006. Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114: 168-176.
Evans, G. A., F. F. Kilkenny, and L. F. Galloway. 2013. Evolution of competitive ability within Lonicera japonica's invaded range. International Journal of Plant Sciences 174: 740-748.
Fang, K., L. Chen, J. Zhou, Z.-P. Yang, X.-F. Dong, and H.-B. Zhang. 2019. Plant-soil-foliage feedbacks on seed germination and seedling growth of the invasive plant Ageratina adenophora. Proceedings of the Royal Society, B, Biological Sciences 286: 20191520.
Felker-Quinn, E., J. A. Schweitzer, and J. K. Bailey. 2013. Meta-analysis reveals evolution in invasive plant species but little support for evolution of increased competitive ability (EICA). Ecology and Evolution 3: 739-751.
Flory, S. L., and K. Clay. 2013. Pathogen accumulation and long term dynamics of plant invasions. Journal of Ecology 101: 607-613.
Flory, S. L., N. Kleczewski, and K. Clay. 2011. Ecological consequences of pathogen accumulation on an invasive grass. Ecosphere 2: 1-12.
Gaudet, C. L., and P. A. Keddy. 1988. A comparative approach to predicting competitive ability from plant traits. Nature 334: 242-243.
Gibson, A., C. R. Nelson, and D. Z. Atwater. 2018. Response of bluebunch wheatgrass to invasion: differences in competitive ability among invader-experienced and invader-naïve populations. Functional Ecology 32: 1857-1866.
Goldberg, D. E., and K. Landa. 1991. Competitive effect and responses: hierarchies and correlated traits in the early stages of competition. Journal of Ecology 79: 1013-1030.
Gruntman, M., U. Segev, G. Glauser, and K. Tielbörger. 2017. Evolution of plant defences along an invasion chronosequence: defence is lost due to enemy release-but not forever. Journal of Ecology 105: 255-264.
Hawkes, C. V. 2007. Are invaders moving targets? The generality and persistence of advantages in size, reproduction, and enemy release in invasive plant species with time since introduction. American Naturalist 170: 832-843.
Hendriks, M., J. M. Ravenek, A. E. Smit-Tiekstra, J. W. van der Paauw, H. de Caluwe, W. H. Van der Putten, Hans de Kroon, and Liesje Mommer. 2015. Spatial heterogeneity of plant-soil feedback affects root interactions and interspecific competition. New Phytologist 207: 830-840.
Howard, M. M., T. H. Bell, and J. Kao-Kniffin. 2017. Soil microbiome transfer method affects microbiome composition, including dominant microorganisms, in a novel environment. FEMS Microbiol Letters 364: fnx092.
Huang, F., and S. Peng. 2016. Intraspecific competitive ability declines towards the edge of the expanding range of the invasive vine Mikania micrantha. Oecologia 181: 115-123.
Kaisermann, A., F. T. de Vries, R. I. Griffiths, and R. D. Bardgett. 2017. Legacy effects of drought on plant-soil feedbacks and plant-plant interactions. New Phytologist 215: 1413-1424.
Ke, P.-J., P. C. Zee, and T. Fukami. 2021. Dynamic plant-soil microbe interactions: the neglected effect of soil conditioning time. New Phytologist 231: 1546-1558.
Keane, R. M., and M. J. Crawley. 2002. Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution 17: 164-170.
Kilkenny, F. F., and L. F. Galloway. 2013. Adaptive divergence at the margin of an invaded range. Evolution 67: 722-731.
Klironomos, J. N. 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417: 67-70.
Kolar, C. S., and D. M. Lodge. 2001. Progress in invasion biology: predicting invaders. Trends in Ecology & Evolution 16: 199-204.
Kuznetsova, A., P. Brockhoff, and R. Christensen. 2017. lmerTest Package: tests in linear mixed effects models. Journal of Statistical Software 82: 1-26.
Lankau, R. A., and D. P. Keymer. 2018. Simultaneous adaptation and maladaptation of tree populations to local rhizosphere microbial communities at different taxonomic scales. New Phytologist 217: 1267-1278.
Lau, J. A., and T. Suwa. 2016. The changing nature of plant-microbe interactions during a biological invasion. Biological Invasions 18: 3527-3534.
Lekberg, Y., J. D. Bever, R. A. Bunn, R. M. Callaway, M. M. Hart, S. N. Kivlin, J. Klironomos, et al. 2018. Relative importance of competition and plant-soil feedback, their synergy, context dependency and implications for coexistence. Ecology Letters 21: 1268-1281.
Li, J., H. Liu, M. Yan, and L. Du. 2017. No evidence for local adaptation to salt stress in the existing populations of invasive Solidago canadensis in China. PLoS One 12: 1-13.
Li, J., A. M. O. Oduor, F. Yu, and M. Dong. 2019. A native parasitic plant and soil microorganisms facilitate a native plant co-occurrence with an invasive plant. Ecology and Evolution 9: 8652-8663.
Mack, R. N., D. Simberloff, M. W. Lonsdale, H. Evans, M. Clout, and F. A. Bazzaz. 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10: 689-710.
Mangla, S., and R. M. Callaway. 2008. Exotic invasive plant accumulates native soil pathogens which inhibit native plants. Journal of Ecology 96: 58-67.
McGinn, K. J., W. H. Van der Putten, P. E. Hulme, N. Shelby, C. Weser, and R. P. Duncan. 2018. The influence of residence time and geographic extent on the strength of plant-soil feedbacks for naturalised Trifolium. Journal of Ecology 106: 207-217.
Mitchell, C. E., A. A. Agrawal, J. D. Bever, G. S. Gilbert, R. A. Hufbauer, J. N. Klironomos, J. L. Maron, et al. 2006. Biotic interactions and plant invasions. Ecology Letters 9: 726-740.
Nijjer, S., W. E. Rogers, and E. Siemann. 2007. Negative plant-soil feedbacks may limit persistence of an invasive tree due to rapid accumulation of soil pathogens. Proceedings of the Royal Society, B, Biological Sciences 274: 2621-2627.
Oduor, A. M. O. 2022. Native plant species show evolutionary responses to invasion by Parthenium hysterophorus in an African savanna. New Phytologist 233: 983-994.
Oduor, A. M. O., R. Leimu, and M. van Kleunen. 2016. Invasive plant species are locally adapted just as frequently and at least as strongly as native plant species. Journal of Ecology 104: 957-968.
Oduor, A. M. O., M. van Kleunen, and M. Stift. 2017. In the presence of specialist root and shoot herbivory, invasive-range Brassica nigra populations have stronger competitive effects than native-range populations. Journal of Ecology 105: 1679-1686.
Ouborg, N. J., and R. van Treuren. 1995. Variation in fitness-related characters among small and large populations of Salvia pratensis. Journal of Ecology 83: 369-380.
R Development Core Team. 2021. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Website: http://www.r-project.org/index.html
Reinhart, K. O., T. Tytgat, W. H. Van der Putten, and K. Clay. 2010. Virulence of soil-borne pathogens and invasion by Prunus serotina. New Phytologist 186: 484-495.
Richardson, D., N. Allsopp, C. D'Antonio, S. Milton, and M. Rejmánek. 2000. Plant invasions the role of mutualisms. Biological Reviews 75: 65-93.
Rotter, M. C., and L. M. Holeski. 2018. A meta-analysis of the evolution of increased competitive ability hypothesis: genetic-based trait variation and herbivory resistance trade-offs. Biological Invasions 20: 2647-2660.
Samis, K. E., C. J. Murren, O. Bossdorf, K. Donohue, C. B. Fenster, R. L. Malmberg, M. D. Purugganan, and J. R. Stinchcombe. 2012. Longitudinal trends in climate drive flowering time clines in North American Arabidopsis thaliana. Ecology and Evolution 2: 1162-1180.
Schultheis, E. H., A. E. Berardi, and J. A. Lau. 2015. No release for the wicked: enemy release is dynamic and not associated with invasiveness. Ecology 96: 2446-2457.
Shipunov, A., G. Newcombe, A. K. H. Raghavendra, and C. L. Anderson. 2008. Hidden diversity of endophytic fungi in an invasive plant. American Journal of Botany 95: 1096-1108.
Speek, T., J. Schaminée, J. Stam, L. Lotz, W. Ozinga, and W. Van der Putten. 2015. Local dominance of exotic plants declines with residence time: a role for plant-soil feedback? AoB Plants 7: plv021.
Stricker, K., P. Harmon, E. Goss, K. Clay, and S. L. Flory. 2016. Emergence and accumulation of novel pathogens suppress an invasive species. Ecology Letters 19: 469-477.
Sun, Z.-K., and W.-M. He. 2010. Evidence for enhanced mutualism hypothesis: solidago canadensis plants from regular soils perform better. PLoS One 5: e15418.
Van der Putten, W., M. Bradford, E. P. Brinkman, T. Van de Voorde, and G. Veen. 2016. Where, when and how plant-soil feedback matters in a changing world. Functional Ecology 30: 1109-1121.
Vila, M., J. L. Espinar, M. Hejda, P. E. Hulme, V. Jarošík, J. L. Maron, J. Pergl, et al. 2011. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecology Letters 14: 702-708.
Wang, C., K. Jiang, J. Zhou, and B. Wu. 2018. Solidago canadensis invasion affects soil N-fixing bacterial communities in heterogeneous landscapes in urban ecosystems in East China. Science of The Total Environment 631-632: 702-713.
Xu, H., S. Qiang, P. Genovesi, H. Ding, J. Wu, L. Meng, Z. Han, et al. 2012. An inventory of invasive alien species in China. NeoBiota 15: 1-26.
Yang, R. Y., L. X. Mei, J. J. Tang, and X. Chen. 2007. Allelopathic effects of invasive Solidago canadensis L. on germination and growth of native Chinese plant species. Allelopathy Journal 19: 241-248.
Yang, R., G. Zhou, S. Zan, F. Guo, N. Su, and J. Li. 2014. Arbuscular mycorrhizal fungi facilitate the invasion of Solidago canadensis L. in southeastern China. Acta Oecologica 61: 71-77.
Yang, Y., M. Liu, Y. Pan, H. Huang, X. Pan, A. Sosa, Y. Hou, et al. 2021. Rapid evolution of latitudinal clines in growth and defence of an invasive weed. New Phytologist 230: 845-856.
Yuan, Y., J. Tang, D. Leng, S. Hu, J. W. H. Yong, and X. Chen. 2014. An invasive plant promotes its arbuscular mycorrhizal symbioses and competitiveness through its secondary metabolites: indirect evidence from activated carbon. PloS One 9: e97163.
Yuan, Y., B. Wang, S. Zhang, J. Tang, C. Tu, S. Hu, J. W. H. Yong, and X. Chen. 2013. Enhanced allelopathy and competitive ability of invasive plant Solidago canadensis in its introduced range. Journal of Plant Ecology 6: 253-263.
Zhang, Q., R. Yang, J. Tang, H. Yang, S. Hu, and X. Chen. 2010. Positive feedback between mycorrhizal fungi and plants influences plant invasion success and resistance to invasion. PloS One 5: e12380.
Zhang, Q., L. Yao, R. Yang, J. Tang, and X. Chen. 2007. Potential allelopathic effects of an invasive species Solidago canadensis in the mycorrhizae of native plant species. Allelopathy Journal 20: 71-78.
Zhang, S., Y. Jin, J. Tang, and X. Chen. 2009. The invasive plant Solidago canadensis L. suppresses local soil pathogens through allelopathy. Applied Soil Ecology 41: 215-222.
Zhang, S., W. Zhu, B. Wang, J. Tang, and X. Chen. 2011. Secondary metabolites from the invasive Solidago canadensis L. accumulation in soil and contribution to inhibition of soil pathogen Pythium ultimum. Applied Soil Ecology 48: 280-286.
Zhao, S. Y., S. G. Sun, C. Dai, R. W. Gituru, J. M. Chen, and Q. F. Wang. 2015. Genetic variation and structure in native and invasive Solidago canadensis populations. Weed Research 55: 163-172.