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Interactive effects of nutrient availability, fluctuating supply, and plant parasitism on the post-invasion success of Bidens pilosa

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Abstract

The post-invasion success of alien plant species is determined by many biotic and abiotic factors, but no study has tested the interactive effect of nutrient availability, fluctuating nutrient supply and parasitic plants. Testing this effect is important because parasitic plants are proposed as a promising agent for biocontrol of alien plant invasions. We constructed an experimental native community under constant or fluctuating conditions as well as high or low nutrient availability and let them be invaded by an alien annual plant Bidens pilosa or not and parasitized by Cuscuta australis or not. High nutrient availability significantly increased the invasion success of B. pilosa (as indicated by its increased biomass fraction, i.e., invader biomass divided by total biomass of all plants) by benefiting the invader more than the native plant community. Fluctuating nutrient supply also significantly enhanced the invasion success of B. pilosa by suppressing the growth of the natives while improving that of the invader. Parasitism by C. australis decreased the growth of the invader and thus its invasion success in the native community when nutrient availability was low and fluctuating, but parasitism had little impact under other nutrient conditions. Our study offers further evidence that high and fluctuating nutrient availability can increase the invasion success of alien plant species in native plant communities, but also demonstrates that the impact of parasitic plants depends on environmental conditions. Thus, reducing nutrient loading and the extent of fluctuating nutrient supply can help native plant communities resist alien plant invasions, but introducing parasitic plants may only be successful if reduced loads are also fluctuating.

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References

  • Allington GR, Koons DN, Morgan Ernest SK, Schutzenhofer MR, Valone TJ (2013) Niche opportunities and invasion dynamics in a desert annual community. Ecol Lett 16:158–166

    Article  PubMed  Google Scholar 

  • Blumenthal D, Mitchell CE, Pyšek P, Jarošík V (2009) Synergy between pathogen release and resource availability in plant invasion. P Natl Acad Sci USA 106:7899–7904

    Article  CAS  Google Scholar 

  • Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443

    Article  Google Scholar 

  • Cirocco RM, Facelli JM, Watling JR (2017) Does nitrogen affect the interaction between a native hemiparasite and its native or introduced leguminous hosts? New Phytol 213:812–821

    Article  CAS  PubMed  Google Scholar 

  • Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis. Ecol Lett 14:419–431

    Article  PubMed  Google Scholar 

  • Davis MA, Pelsor M (2001) Experimental support for a resource-based mechanistic model of invasibility. Ecol Lett 4:421–428

    Article  Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534

    Article  Google Scholar 

  • Dawson W, Rohr RP, van Kleunen M, Fischer M (2012) Alien plant species with a wider global distribution are better able to capitalize on increased resource availability. New Phytol 194:859–867

    Article  PubMed  Google Scholar 

  • Drenovsky RE, Martin CE, Falasco MR, Falasco MR, James JJ (2008) Variation in resource acquisition and utilization traits between native and invasive perennial forbs. Am J Bot 95:681–687

    Article  PubMed  Google Scholar 

  • Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079

    Article  CAS  PubMed  Google Scholar 

  • Gallien L, Altermatt F, Wiemers M, Schweiger O, Zimmermann NE (2017) Invasive plants threaten the least mobile butterflies in Switzerland. Divers Distrib 23:185–195

    Article  Google Scholar 

  • Gao F-L, Alpert P, Yu F-H (2021) Parasitism induces negative effects of physiological integration in a clonal plant. New Phytol 229:585–592

    Article  CAS  PubMed  Google Scholar 

  • Grewell BJ (2008) Parasite facilitates plant species coexistence in a coastal wetland. Ecology 89:1481–1488

    Article  PubMed  Google Scholar 

  • Hautier Y, Hector A, Vojtech E, Purves D, Turnbull LA (2010) Modelling the growth of parasitic plants. J Ecol 98:857–866

    Article  Google Scholar 

  • Heckman RW, Wright JP, Mitchell CE (2016) Joint effects of nutrient addition and enemy exclusion on exotic plant success. Ecology 97:3337–3345

    Article  PubMed  Google Scholar 

  • Huang QQ, Shen YD, Li XX, Li SL, Fan ZW (2016) Invasive Eupatorium catarium and Ageratum conyzoides benefit more than does a common native plant from nutrient addition in both competitive and non-competitive environments. Ecol Res 31:145–152

    Article  Google Scholar 

  • James JJ, Richards JH (2006) Plant nitrogen capture in pulse-driven systems: interactions between root responses and soil processes. J Ecol 94:765–777

    Article  CAS  Google Scholar 

  • James JJ, Richards JH (2007) Influence of temporal heterogeneity in nitrogen supply on competitive interactions in a desert shrub community. Oecologia 152:721–727

    Article  CAS  PubMed  Google Scholar 

  • James SE, Partel M, Wilson SD, Peltzer DA (2003) Temporal heterogeneity of soil moisture in grassland and forest. J Ecol 91:234–239

    Article  Google Scholar 

  • Jauni M, Gripenberg S, Ramula S (2015) Non-native plant species benefit from disturbance: a meta-analysis. Oikos 124:122–129

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Kennedy TA, Naeem S, Howe KM, Knops JMH, Tilman D, Reich P (2002) Biodiversity as a barrier to ecological invasion. Nature 417:636–638

    Article  CAS  PubMed  Google Scholar 

  • Koch AM, Binder C, Sanders IR (2004) Does the generalist parasitic plant Cuscuta campestris selectively forage in heterogeneous plant communities? New Phytol 162:147–155

    Article  Google Scholar 

  • Koerner SE, Avolio ML, Chang CC, Gray J, Hoover DL, Smith MD (2015) Invasibility of a mesic grassland depends on the time-scale of fluctuating resources. J Ecol 103:1538–1546

    Article  Google Scholar 

  • Lepš J, Tešitel J (2015) Root hemiparasites in productive communities should attack competitive host, and harm them to make regeneration gaps. J Veg Sci 26:407–408

    Article  Google Scholar 

  • Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989

    Article  Google Scholar 

  • Li JM, Jin ZX, Song WJ (2012) Do native parasitic plants cause more damage to exotic invasive hosts than native non-invasive hosts? an implication for biocontrol. PLoS ONE 7:e34577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li JM, Yang BF, Yan QD, Zhang J, Yan M, Li MH (2015) Effects of a native parasitic plant on an exotic invader decrease with increasing host age. AoB PLANTS 7:plv031

  • Liu YJ, van Kleunen M (2017) Responses of common and rare aliens and natives to nutrient availability and fluctuations. J Ecol 105:1111–1122

    Article  CAS  Google Scholar 

  • Liu YJ, Oduor AMO, Zhang Z, Manea A, Tooth IM, Leishman MR, Xu XL, van Kleunen M (2017a) Do invasive alien plants benefit more from global environmental change than native plants? Glob Chang Biol 23:3363–3370

    Article  PubMed  Google Scholar 

  • Liu YY, Taxipulati T, Gong YM, Sui XL, Wang XZ, Parent S-É, Hu YK, Guan KY, Li AR (2017b) N-P Fertilization Inhibits Growth of Root Hemiparasite Pedicularis kansuensis in Natural Grassland. Front Plant Sci 8:2088

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu YJ, Zhang XQ, van Kleunen M (2018) Increases and fluctuations in nutrient availability do not promote dominance of alien plants in synthetic communities of common natives. Funct Ecol 32:2594–2604

    Article  Google Scholar 

  • Lü C, Tian H (2007) Spatial and temporal patterns of nitrogen deposition in China: synthesis of observational data. J Gecophys Res 112:D22S05

    Google Scholar 

  • Lundholm JT, Larson DW (2003) Temporal variability in water supply controls seedling diversity in limestone pavement microcosms. J Ecol 91:966–975

    Article  Google Scholar 

  • Maron J, Marler M (2007) Native plant diversity resists invasion at both low and high resource levels. Ecology 88:2651–2661

    Article  PubMed  Google Scholar 

  • Mata TM, Haddad NM, Holyoak M (2013) How invader traits interact with resident communities and resource availability to determine invasion success. Oikos 122:149–160

    Article  Google Scholar 

  • Parepa M, Fischer M, Bossdorf O (2013) Environmental variability promotes plant invasion. Nat Commun 4:1604

    Article  PubMed  CAS  Google Scholar 

  • Parepa M, Kahmen A, Werner RA, Fischer M, Bossdorf O (2019) Invasive knotweed has greater nitrogen-use efficiency than native plants: evidence from a N-15 pulse-chasing experiment. Oecologia 191:389–396

    Article  PubMed  Google Scholar 

  • Pennings S, Callaway R (2002) Parasitic plants: parallels and contrasts with herbivores. Oecologia 131:479–489

    Article  PubMed  Google Scholar 

  • Pennings SC, Simpson JC (2008) Like herbivores, parasitic plants are limited by host nitrogen content. Plant Ecol 196:245–250

    Article  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytol 166:737–751

    Article  PubMed  Google Scholar 

  • Renne IJ, Tracy BF, Colonna IA (2006) Shifts in grassland invasibility: Effects of soil resources, disturbance, composition, and invader size. Ecology 87:2264–2277

    Article  PubMed  Google Scholar 

  • Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993

    Article  PubMed  Google Scholar 

  • Schrama M, Bardgett RD, Austin A (2016) Grassland invasibility varies with drought effects on soil functioning. J Ecol 104:1250–1258

    Article  Google Scholar 

  • Selmants PC, Zavaleta ES, Pasari JR, Hernandez DL (2012) Realistic plant species losses reduce invasion resistance in a California serpentine grassland. J Ecol 100:723–731

    Article  Google Scholar 

  • Shen XY, Peng SL, Chen BM, Pang JX, Chen LY, Xu HM, Hou YP (2011) Do higher resource capture ability and utilization efficiency facilitate the successful invasion of native plants? Biol Invasions 13:869–881

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H. Freeman, New York

    Google Scholar 

  • Tarasi DD, Peet RK (2017) The native-exotic species richness relationship varies with spatial grain of measurement and environmental conditions. Ecology 98:3086–3095

    Article  PubMed  Google Scholar 

  • Těšitel J, Těšitelova T, Fisher JP, Lepš J, Cameron DD (2015) Integrating ecology and physiology of root-hemiparasitic interaction: interactive effects of abiotic resources shape the interplay between parasitism and autotrophy. New Phytol 205:350–360

    Article  PubMed  Google Scholar 

  • Těšitel J, Mládek J, Horník J, Těšitelová T, Adamec V, Tichý L (2017) Suppressing competitive dominants and community restoration with native parasitic plants using the hemiparasitic Rhinanthus alectorolophus and the dominant grass Calamagrostis epigejos. J Appl Ecol 54:1487–1495

    Article  Google Scholar 

  • Těšitel J, Cirocco RM, Facelli JM, Watling JR (2020) Native parasitic plants: biological control for plant invasions? Appl Veg Sci 23:464–469

    Article  Google Scholar 

  • Tognetti PM, Chaneton EJ (2015) Community disassembly and invasion of remnant native grasslands under fluctuating resource supply. J Appl Ecol 52:119–128

    Article  Google Scholar 

  • Underwood AJ (1996) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge, UK

    Book  Google Scholar 

  • van Kleunen M, Essl F, Pergl J, Brundu G, Carboni M, Dullinger S, Early R, González-Moreno P, Groom QJ, Hulme PE et al (2018a) The changing role of ornamental horticulture in alien plant invasions. Biol Rev 93:1421–1437

    Article  PubMed  Google Scholar 

  • van Kleunen M, Bossdorf O, Dawson W (2018b) The ecology and evolution of alien plants. Annu Rev of Ecol Evol S 49:25–47

    Article  Google Scholar 

  • Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708

    Article  PubMed  Google Scholar 

  • Wang YJ, Müller-Schärer H, van Kleunen M, Cai AM, Zhang P, Yan R, Dong BC, Yu FH (2017) Invasive alien plants benefit more from clonal integration in heterogeneous environments than natives. New Phytol 216:1072–1078

    Article  PubMed  Google Scholar 

  • Wang YJ, Chen D, Yan R, Yu FH, van Kleunen M (2019) Invasive alien clonal plants are competitively superior over co-occurring native clonal plants. Perspect Plant Ecol 40:125484

    Article  Google Scholar 

  • Xu HG, Qiang S, Genovesi P, Ding H, Wu J, Meng L, Han ZM, Miao JL, Hu BS, Guo JY, Sun HY, Huang C, Lei JC, Zf Le, Zhang XP, He SP, Wu Y, Zheng Z, Chen L, Jarošík V, Pyšek P (2012) An inventory of invasive alien species in China. NeoBiota 15:1–26

    Article  Google Scholar 

  • Yang LH, Bastow JL, Spence KO, Wright AN (2008) What can we learn from resource pulses? Ecology 89:621–634

    Article  PubMed  Google Scholar 

  • Yu H, Yu FH, Miao SL, Dong M (2008) Holoparasitic Cuscuta campestris suppresses invasive Mikania micrantha and contributes to native community recovery. Biol Conserv 141:2653–2661

    Article  Google Scholar 

  • Yu H, He WM, Liu J, Miao SL, Dong M (2009) Native Cuscuta campestris restrains exotic Mikania micrantha and enhances soil resources beneficial to natives in the invaded communities. Biol Invasions 11:835–844

    Article  Google Scholar 

  • Yu H, Liu JA, He WM, Miao SL, Dong M (2011) Cuscuta australis restrains three exotic invasive plants and benefits native species. Biol Invasions 13:747–756

    Article  Google Scholar 

  • Zhang P, Li B, Wu JH et al (2019) Invasive plants differentially affect soil biota through litter and rhizosphere pathways: a meta-analysis. Ecol Lett 22:200–210

    Article  PubMed  Google Scholar 

  • Zheng YL, Burns JH, Liao ZY, Li YP, Yang J, Chen YJ, Zhang JL, Zheng YG (2018) Species composition, functional and phylogenetic distances correlate with success of invasive Chromolaena odorata in an experimental test. Ecol Lett 21:1211–1220

    Article  PubMed  Google Scholar 

  • Zhou Y, Staver AC (2019) Enhanced activity of soil nutrient-releasing enzymes after plant invasion: a meta-analysis. Ecology 100:e02830

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Prof. Yanjie Liu for help with the experimental design, and the associate editor (Dr. Josh Caplan) and two anonymous reviewers for their comments. This study was supported by the Ten-Thousand-Talent Program of Zhejiang Province (2018R52016), the Joint Fund of Zhejiang Provincial Natural Science Foundation (LTZ20C030001), the National Natural Science Foundation of China (31761123001; 32001302) and a Startup Project for Doctor’s Scientific Research of Binzhou University (2019Y35). We declare that there is no conflict of interest and our data are available on request.

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Authors and Affiliations

  1. Shandong Key Laboratory of Eco-Environmental Science for the Yellow River Delta, Binzhou University, Binzhou, 256603, China

    Fang-Lei Gao

  2. Institute of Wetland Ecology & Clone Ecology, Taizhou University, Taizhou, 318000, China

    Fang-Lei Gao, Qiao-Sheng He, Ru-Qian Xie, Jia-Hui Hou, Chen-Lu Shi & Fei-Hai Yu

  3. Zhejiang Province Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, Taizhou, 318000, China

    Fang-Lei Gao, Jun-Min Li & Fei-Hai Yu

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  1. Fang-Lei Gao
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Gao, FL., He, QS., Xie, RQ. et al. Interactive effects of nutrient availability, fluctuating supply, and plant parasitism on the post-invasion success of Bidens pilosa. Biol Invasions 23, 3035–3046 (2021). https://doi.org/10.1007/s10530-021-02555-y

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