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Simulated nitrogen deposition induces shifts in growth and resource-use strategies during range expansion of an invasive plant

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Abstract

An appropriate resource-use strategy contributes to the invasion success of exotic plants. During range expansion, population density and nitrogen availability are two important factors that exert significant influences on resource-use-associated traits. As population density decreases and resource availability increases, invasive species are likely driven to be increasingly quicker in resource-use return. By far, it remains unclear how resource-use-related traits shift in response to simultaneous changes in population density and N deposition, and how the shift in resource-use strategy is related to growth in invasive plants. Here we investigated the intraspecific variation in growth and leaf-level resource-use-related traits across invasive populations of different covers under contrasting N levels using a worldwide invasive perennial vine, Mikania micrantha. N addition greatly increased the growth and leaf physiological parameters of M. micrantha. At low N level, the resource-use strategy shifted to be more conservative with decreasing population cover, which was primarily correlated with increasing leaf investment; at high N level, on the contrary, the resource-use strategy shifted to be more acquisitive, which was primarily correlated with increasing carbon assimilation capacity. In addition, M. micrantha growth performance was less related to population cover, and it did not associate with leaf physiology. These results suggest that resource-use strategy shifts from conservative to acquisitive towards range edges during range expansion of M. micrantha. This work reveals the pattern of resource-use strategy in long-term plant invasion, and can provide insights into how invasive species will fare in the context of nitrogen deposition.

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References

  • Aerts R, Chapin FS III (1999) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67

    Article  Google Scholar 

  • Baruch Z, Goldstein G (1999) Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii. Oecologia 121:183–192

    Article  PubMed  CAS  Google Scholar 

  • Bauer GA, Bazzaz FA, Minocha R, Long S, Magill A, Aber J et al (2004) Effects of chronic N additions on tissue chemistry, photosynthetic capacity, and carbon sequestration potential of a red pine (Pinus resinosa Ait.) stand in the NE United States. Forest Ecol Manag 196:173–186

    Article  Google Scholar 

  • Brooks ML (2003) Effects of increased soil nitrogen on the dominance of alien annual plants in the Mojave Desert. J Appl Ecol 40:344–353

    Article  Google Scholar 

  • Burton OJ, Phillips BL, Travis JMJ (2010) Trade-offs and the evolution of life-histories during range expansion. Ecol Lett 13:1210–1220

    Article  PubMed  Google Scholar 

  • Daehler CC (2003) Performance comparisons of co-occurring native and invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol S 34:183–211

    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 

  • Díaz de León Guerrero SD, González-Rebeles Guerrero G, Ibarra-Montes TM, Rodríguez Bastarrachea A, Santos Cobos R, Bullock SH et al (2020) Functional traits indicate faster resource acquisition for alien herbs than native shrubs in an urban Mediterranean shrubland. Biol Invasions 22:2699–2712

    Article  Google Scholar 

  • Dietz H, Edwards PJ (2006) Recognition that causal processes change during plant invasion helps explain conflicts in evidence. Ecology 87:1359–1367

    Article  PubMed  Google Scholar 

  • Dukes JS, Chiariello NR, Loarie SR, Field CB (2011) Strong response of an invasive plant species (Centaurea solstitialis L.) to global environmental changes. Ecol Appl 21:1887–1894

    Article  PubMed  Google Scholar 

  • Feng YL, Fu GL, Zheng YL (2008) Specific leaf area relates to the differences in leaf construction cost, photosynthesis, nitrogen allocation, and use efficiencies between invasive and noninvasive alien congeners. Planta 228:383–390

    Article  PubMed  CAS  Google Scholar 

  • Feng YL, Li YP, Wang RF, Callaway RM, Valiente-Banuet A, Inderjit (2011) A quicker return energy-use strategy by populations of a subtropical invader in the non‐native range: a potential mechanism for the evolution of increased competitive ability. J Ecol 99:1116–1123

    Article  Google Scholar 

  • Funk JL (2013) The physiology of invasive plants in low-resource environments. Conserv Physiol 1:1–17

    Article  Google Scholar 

  • Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081

    Article  PubMed  CAS  Google Scholar 

  • Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226

    Article  CAS  Google Scholar 

  • González-Rodríguez V, Villar R, Navarro-Cerrillo RM (2011) Maternal influences on seed mass effect and initial seedling growth in four Quercus species. Acta Oecol 37:1–9

    Article  Google Scholar 

  • Hanski I, Saastamoinen M, Ovaskainen O (2006) Dispersal-related life-history trade-offs in a butterfly metapopulation. J Anim Ecol 75:91–100

    Article  PubMed  Google Scholar 

  • Heberling JM, Kichey T, Decocq G, Fridley JD (2016) Plant functional shifts in the invaded range: a test with reciprocal forest invaders of Europe and North America. Funct Ecol 30:875–884

    Article  Google Scholar 

  • Hikosaka K, Terashima I (1995) A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. Plant Cell Environ 18:605–618

    Article  CAS  Google Scholar 

  • Holm LG, Plucknett DL, Pancho JV, Herberger JP (1977) The world’s worst weeds. University Press, Hawaii

    Google Scholar 

  • Huang F, Peng S (2016) Intraspecific competitive ability declines towards the edge of the expanding range of the invasive vine Mikania micrantha. Oecologia 181:115–123

    Article  PubMed  Google Scholar 

  • Huang F, Peng S, Chen B, Liao H, Huang Q, Lin Z et al (2015) Rapid evolution of dispersal-related traits during range expansion of an invasive vine Mikania micrantha. Oikos 124:1023–1030

    Article  Google Scholar 

  • Hui C, Richardson DM, Landi P, Minoarivelo HO, Roy HE, Latombe G et al (2021) Trait positions for elevated invasiveness in adaptive ecological networks. Biol Invasions 23:1965–1985

    Article  Google Scholar 

  • Jia Y, Yu G, He N, Zhan X, Fang H, Sheng W et al (2014) Spatial and decadal variations in inorganic nitrogen wet deposition in China induced by human activity. Sci Rep 4:3763

    Article  PubMed  PubMed Central  Google Scholar 

  • Jifon JL, Wolfe DW (2002) Photosynthetic acclimation to elevated CO2 in Phaseolus vulgaris L. is altered by growth response to nitrogen supply. Glob Chang Biol 8:1018–1027

    Article  Google Scholar 

  • Kilkenny FF, Galloway LF (2013) Adaptive divergence at the margin of an invaded range. Evolution 67:722–731

    Article  PubMed  Google Scholar 

  • Kong G, Wu Q, Hu Q, Ye W (2000) Further supplementary data on Mikania micrantha H.B.K. (Asteraceae). J Trop Subtrop Bot 8:128-130 (in Chinese with an English abstract)

  • Lankau RA, Strauss SY (2011) Newly rare or newly common: evolutionary feedbacks through changes in population density and relative species abundance, and their management implications. Evol Appl 4:338–353

    Article  PubMed  PubMed Central  Google Scholar 

  • Lankau RA (2012) Coevolution between invasive and native plants driven by chemical competition and soil biota. PNAS 109:11240–11245

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leishman MR, Cooke J, Richardson DM (2014) Evidence for shifts to faster growth strategies in the new ranges of invasive alien plants. J Ecol 102:1451–1461

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu G, Yang YB, Zhu ZH (2018) Elevated nitrogen allows the weak invasive plant Galinsoga quadriradiata to become more vigorous with respect to inter-specific competition. Sci Rep 8:1–8

    Google Scholar 

  • Lowe S, Browne M, Boudjelas S, de Poorter M (2000) 100 of the world’s worst invasive alien species: a selection from the global invasive species database. Invasive Species Specialist Group Auckland, New Zealand

    Google Scholar 

  • Luo X, Xu X, Zheng Y, Guo H, Hu S (2019) The role of phenotypic plasticity and rapid adaptation in determining invasion success of Plantago virginica. Biol Invasions 21:2679–2692

    Article  Google Scholar 

  • Luo X, Zheng Y, Xu X, Xiao R, Guo H (2020) The impacts of warming and nitrogen addition on competitive ability of native and invasive populations of Plantago virginica. J Plant Ecol 13:676–682

    Article  Google Scholar 

  • Mattingly WB, Reynolds HL (2014) Soil fertility alters the nature of plant-resource interactions in invaded grassland communities. Biol Invasions 16:2465–2478

    Article  Google Scholar 

  • Monty A, Mahy G (2010) Evolution of dispersal traits along an invasion route in the wind-dispersed Senecio inaequidens (Asteraceae). Oikos 119:1563–1570

    Article  Google Scholar 

  • Morris TL, Esler KJ, Barger NN, Jacobs SM, Cramer MD (2011) Ecophysiological traits associated with the competitive ability of invasive Australian acacias. Divers Distrib 17:898–910

    Article  Google Scholar 

  • Mozdzer TJ, Megonigal JP (2012) Jack-and-master trait responses to elevated CO2 and N: a comparison of native and introduced Phragmites australis. PLoS ONE 7:e4279410

    Article  Google Scholar 

  • Nguyen MA, Ortega AE, Nguyen KQ, Kimball S, Goulden ML, Funk JL (2016) Evolutionary responses of invasive grass species to variation in precipitation and soil nitrogen. J Ecol 104:979–986

    Article  CAS  Google Scholar 

  • Ordonez A, Olff H (2013) Do alien plant species profit more from high resource supply than natives? A trait-based analysis. Glob Ecol Biogeogr 22:648–658

    Article  Google Scholar 

  • De Penning FWT, Brunsting AHM, van Laar HH (1974) Products, requirements and efficiency of biosynthesis a quantitative approach. J Theor Biol 45:339–377

    Article  Google Scholar 

  • Phillips BL (2009) The evolution of growth rates on an expanding range edge. Biol Lett 5:802–804

    Article  PubMed  PubMed Central  Google Scholar 

  • Phillips BL, Brown GP, Shine R (2010) Life-history evolution in range‐shifting populations. Ecology 91:1617–1627

    Article  PubMed  Google Scholar 

  • Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439:803

    Article  PubMed  CAS  Google Scholar 

  • Poorter H, Pepin S, Rijkers T, De Jong Y, Evans JR, Körner C (2006) Construction costs, chemical composition and payback time of high-and low-irradiance leaves. J Exp Bot 57:355–371

    Article  PubMed  CAS  Google Scholar 

  • Pyšek P, Jarošík V, Hulme PE, Pergl J, Hejda M, Schaffner U et al (2012) 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 18:1725–1737

    Article  PubMed Central  Google Scholar 

  • Ribeiro PCD, Menendez E, da Silva DL, Bonieck D, Ramírez-Bahena MH, Resende-Stoianoff MA et al (2017) Invasion of the Brazilian campo rupestre by the exotic grass Melinis minutiflora is driven by the high soil N availability and changes in the N cycle. Sci Total Environ 577:202–211

    Article  PubMed  CAS  Google Scholar 

  • Siemann E, Rogers WE, Dewalt SJ (2006) Rapid adaptation of insect herbivores to an invasive plant. P Roy Soc B-Biol Sci 273:2763–2769

    Google Scholar 

  • Tabassum S, Leishman MR (2020) Mixed evidence for shifts to faster carbon capture strategies towards range edges of two coastal invasive plants in eastern Australia. Biol Invasions 22:563–575

    Article  Google Scholar 

  • Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273

    Article  PubMed  Google Scholar 

  • Uddin MN, Robinson RW (2018) Can nutrient enrichment influence the invasion of Phragmites australis? Sci Total Environ 613–614:1449–1459

    Article  PubMed  Google Scholar 

  • Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, UK

    Google Scholar 

  • Vallano DM, Selmants PC, Zavaleta ES (2012) Simulated nitrogen deposition enhances the performance of an exotic grass relative to native serpentine grassland competitors. Plant Ecol 213:1015–1026

    Article  Google Scholar 

  • Van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245

    Article  PubMed  Google Scholar 

  • Van Kleunen M, Fischer M (2003) Effects of four generations of density-dependent selection on life history traits and their plasticity in a clonally propagated plant. J Evol Biol 16:474–484

    Article  PubMed  Google Scholar 

  • Vertregt N, Penning de Vries FWT (1987) A rapid method for determining the efficiency of biosynthesis of plant biomass. J Theor Biol 128:109–119

    Article  Google Scholar 

  • Wan J, Huang B, Yu H, Peng S (2019a) Reassociation of an invasive plant with its specialist herbivore provides a test of the shifting defence hypothesis. J Ecol 107:361–371

    Article  Google Scholar 

  • Wan L-Y, Qi S-S, Zou BC, Dai Z-C, Ren G-Q, Chen Q et al (2019b) Elevated nitrogen deposition may advance invasive weed Solidago canadensis in calcareous soils. J Plant Ecol 12:846–856

    Article  Google Scholar 

  • Wang BS, Liao WB, Zan QJ, Li MG, Zhou XY, Gao SH (2003) The spreads of Mikania micrantha in China. Acta Sci Nat Univ Sunyatseni 42:47–50. (in Chinese with an English abstract)

    Google Scholar 

  • Wang C, Zhou J, Liu J, Jiang K (2017) Differences in functional traits between invasive and native Amaranthus species under different forms of N deposition. Sci Nat 104:59

    Article  Google Scholar 

  • Wei C, Pan Y, Tang S, Lin C, Zhou C (2014) Distribution and damage of invasive plant Mikania micrantha in Guangxi. Guihaia 34:816–820

    Google Scholar 

  • Weiner J, Martinez S, Muller-Scharer H, Schmid PS (1997) How important are environmental maternal effects in plants? A study with Centaurea Maculosa. J Ecol 85:133–142

    Article  Google Scholar 

  • Williams K, Percival F, Merino J, Mooney HA (1987) Estimation of tissue construction cost from heat of combustion and organic nitrogen content. Plant Cell Environ 10:725–734

    CAS  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  PubMed  CAS  Google Scholar 

  • Zhang LY, Ye WH, Cao HL, Feng HL (2004) Mikania micrantha HBK in China-an overview. Weed Res 44:42–49

    Article  Google Scholar 

  • Zhang Y, Duan B, Qiao Y, Wang K, Korpelainen H, Li C (2008) Leaf photosynthesis of Betula albosinensis seedlings as affected by elevated CO2 and planting density. Forest Ecol Manag 255:1937–1944

    Article  Google Scholar 

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Funding

This study was supported by National Natural Science Foundation of China (31600330, 31971556), Guangdong Provincial Forestry Science and Technology Innovation Project (2021KJCX014) and Gaungdong Provincial Construction Project of Agricultural Science and Technology Innovation and Extension System (2020KJ264).

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Author notes

  1. Fang-Fang Huang

    Present address: Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou, 510520, China

  2. Fang-Fang Huang and Guo-Hao Zhou contributed equally to this work.

Authors and Affiliations

  1. School of Life Sciences, State Key Lab of Biocontrol, Guangdong Key Laboratory of Plant Resources, Sun Yat-Sen University, Guangzhou, 510275, China

    Fang-Fang Huang, Guo-Hao Zhou, Hui-Xuan Liao, Zhe-Xuan Fan & Bao-Ming Chen

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  1. Fang-Fang Huang
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  2. Guo-Hao Zhou
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  3. Hui-Xuan Liao
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Contributions

FFH, GHZ and BMC designed the research, GHZ and ZXF collected the data, FFH, HXL and BMC analyzed the data, FFH, GHZ and BMC wrote a draft of the manuscript, all authors contributed substantially to revisions.

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Correspondence to Bao-Ming Chen.

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Huang, FF., Zhou, GH., Liao, HX. et al. Simulated nitrogen deposition induces shifts in growth and resource-use strategies during range expansion of an invasive plant. Biol Invasions 24, 621–633 (2022). https://doi.org/10.1007/s10530-021-02668-4

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