Skip to main content
Log in

Invasive Rhus typhina invests more in height growth and traits associated with light acquisition than do native and non-invasive alien shrub species

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

The preferential investment in height growth and traits associated with light acquisition may provide insight into the invasiveness of Rhus typhina.

Abstract

Plant traits have been shown to be associated with invasiveness. Rhus typhina, a shrub or small tree native to North America, shows invasiveness in non-native habitats. Compared to the native shrub Vitex negundo var. heterophylla and the non-invasive alien shrub Amorpha fruticosa, R. typhina showed a high photosynthetic capacity and specific leaf area but a low-leaf nitrogen content, indicating that R. typhina gained high photosynthetic income with low-leaf constituent cost. The non-photochemical quenching of R. typhina was the highest among the three species, which can be linked to its capacity for photoprotection under high light conditions. Allometry analyses showed that R. typhina invested more in height growth than the other two species, pointing to its investment strategy in light acquisition. The low leaf nitrogen-to-phosphorus ratio may be associated with the fast growth of R. typhina. Additionally, R. typhina allocated more biomass to photosynthetic leaves than did the other two species. The preferential investment strategies and traits associated with light acquisition may help explain the invasiveness of R. typhina.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ackerly DD, Donoghue MJ (1998) Leaf size, sapling allometry, and Corner’s rules: phylogeny and correlated evolution in maples (Acer). Am Nat 152:767–791

    Article  PubMed  CAS  Google Scholar 

  • Atkin OK, Bloomfield KJ, Reich PB, Tjoelker MG, Asner GP, Bonal D, Bönisch G, Bradford MG, Cernusak LA, Cosio EG, Creek D, Crous KY, Domingues TF, Dukes JS, Egerton JJG, Evans JR, Farquhar GD, Fyllas NM, Gauthier PPG, Gloor E, Gimeno TE, Griffin KL, Guerrieri R, Heskel MA, Huntingford C, Ishida FY, Kattge J, Lambers H, Liddell MJ, Lloyd J, Lusk CH, Martin RE, Maksimov AP, Maximov TC, Malhi Y, Medlyn BE, Meir P, Mercado LM, Mirotchnick N, Ng D, Niinemets Ü, O’Sullivan OS, Phillips OL, Poorter L, Poot P, Prentice IC, Salinas N, Rowland LM, Ryan MG, Sitch S, Slot M, Smith NG, Turnbull MH, VanderWel MC, Valladares F, Veneklaas EJ, Weerasinghe LK, Wirth C, Wright IJ, Wythers KR, Xiang J, Xiang S, Zaragoza-Castells J (2015) Global variability in leaf respiration in relation to climate, plant functional types and leaf traits. New Phytol 206:614–636

    Article  PubMed  CAS  Google Scholar 

  • Bellard C, Thuiller W, Leroy B, Genovesi P, Bakkenes M, Courchamp F (2013) Will climate change promote future invasions? Glob Change Biol 19:3740–3748

    Article  Google Scholar 

  • Bentley LP, Stegen JC, Savage VM, Smith DD, von Allmen EI, Sperry JS, Reich PB, Enquist BJ (2013) An empirical assessment of tree branching networks and implications for plant allometric scaling models. Ecol Lett 16:1069–1078

    Article  PubMed  Google Scholar 

  • Broz AK, Manter DK, Callaway RM, Paschke MW, Vivanco JM (2008) A molecular approach to understanding plant–plant interactions in the context of invasion biology. Funct Plant Biol 35:1123–1134

    Article  CAS  PubMed  Google Scholar 

  • Burns JH, Winn AA (2006) A comparison of plastic responses to competition by invasive and non-invasive congeners in the Commelinaceae. Biol Invasions 8:797–807

    Article  Google Scholar 

  • Chazdon RL (1988) Sunflecks and their importance to forest understorey plants. Adv Ecol Res 18:1–63

    Article  Google Scholar 

  • Comin S, Ganis P, Poldini L, Vidali M (2011) A diachronic approach to assess alien plant invasion: the case study of Friuli Venezia Giulia (NE Italy). Plant Biosyst 145:50–59

    Article  Google Scholar 

  • Cripps G, Lindeque P, Flynn KJ (2014) Have we been underestimating the effects of ocean acidification in zooplankton? Glob Change Biol 20:3377–3385

    Article  Google Scholar 

  • Crous CJ, Jacobs SM, Esler KJ (2012) Wood anatomical traits as a measure of plant responses to water availability: invasive Acacia mearnsii De Wild. compared with native tree species in fynbos riparian ecotones, South Africa. Trees 26:1527–1536

    Article  Google Scholar 

  • D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass fire cycle, and global change. Annu Rev Ecol Syst 23:63–87

    Article  Google Scholar 

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

    Article  Google Scholar 

  • DeHaan LR, Ehlke NJ, Sheaffer CC, Wyse DL, DeHaan RL (2006) Evaluation of diversity among North American accessions of false indigo (Amorpha fruticosa L.) for forage and biomass. Genet Resour Crop Evol 53:1463–1476

    Article  Google Scholar 

  • Doust JL, Doust LL (1988) Modules of production and reproduction in a dioecious clonal shrub, Rhus typhina. Ecology 69:741–750

    Article  Google Scholar 

  • Du N, Guo W, Zhang X, Wang R (2010) Morphological and physiological responses of Vitex negundo L. var. heterophylla (Franch.) Rehd. to drought stress. Acta Physiol Plant 32:839–848

    Article  Google Scholar 

  • Du N, Wang R, Liu J, Zhang X, Tan X, Wang W, Chen H, Guo W (2013) Morphological response of Vitex negundo var. heterophylla and Ziziphus jujuba var. spinosa to the combined impact of drought and shade. Agrofor Syst 87:403–416

    Article  Google Scholar 

  • Du N, Tan X, Li Q, Liu X, Zhang W, Wang R, Liu J, Guo W (2017) Dominance of an alien shrub Rhus typhina over a native shrub Vitex negundo var. heterophylla under variable water supply patterns. PLoS One 12:e0176491

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Article  PubMed  Google Scholar 

  • Falster DS, Westoby M (2003) Plant height and evolutionary games. Trends Ecol Evol 18:337–343

    Article  Google Scholar 

  • Farquhara GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552

    Article  Google Scholar 

  • Fried G, Laitung B, Pierre C, Chagué N, Panetta FD (2014) Impact of invasive plants in Mediterranean habitats: disentangling the effects of characteristics of invaders and recipient communities. Biol Invasions 16:1639–1658

    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 

  • Galmés J, Abadía A, Medrano H, Flexas J (2007) Photosynthesis and photoprotection responses to water stress in the wild-extinct plant Lysimachia minoricensis. Environ Exp Bot 60:308–317

    Article  CAS  Google Scholar 

  • Glišić M, Lakušić D, Šinžar-Sekulić J, Jovanović S (2014) GIS analysis of spatial distribution of invasive tree species in the protected natural area of Mt. Avala (Serbia). Bot Serbica 38:131–138

    Google Scholar 

  • Goodwin BJ, McAllister AJ, Fahrig L (1999) Predicting invasiveness of plant species based on biological information. Conserv Biol 13:422–426

    Article  Google Scholar 

  • Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Article  PubMed  Google Scholar 

  • Kang S, Zhang L, Song X, Zhang S, Liu X, Liang Y, Zheng S (2001) Runoff and sediment loss responses to rainfall and land use in two agricultural catchments on the Loess Plateau of China. Hydrol Process 15:977–988

    Article  Google Scholar 

  • Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450

    Article  Google Scholar 

  • Küster EC, Kühn I, Bruelheide H, Klotz S (2008) Trait interactions help explain plant invasion success in the German flora. J Ecol 96:860–868

    Article  Google Scholar 

  • Leishman MR, Haslehurst T, Ares A, Baruch Z (2007) Leaf trait relationships of native and invasive plants: community- and global-scale comparisons. New Phytol 176:635–643

    Article  PubMed  CAS  Google Scholar 

  • Leishman MR, Thomson VP, Cooke J (2010) Native and exotic invasive plants have fundamentally similar carbon capture strategies. J Ecol 98:28–42

    Article  CAS  Google Scholar 

  • Lichtenthaler H, Wellburn A (1983) Determinations of total carotenoids and chlorophylls b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    Article  CAS  Google Scholar 

  • Liu J, Wang ET, Chen WX (2005) Diverse rhizobia associated with woody legumes Wisteria sinensis, Cercis racemosa and Amorpha fruticosa grown in the temperate zone of China. Syst Appl Microbiol 28:465–477

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Zhang W, Liu Z, Qu F, Tang X (2011) Changes in species diversity and above-ground biomass of shrubland over long-term natural restoration process in the Taihang Mountain in North China. Plant Soil Environ 57:505–512

    Article  Google Scholar 

  • Marchin RM, Bhandari RK, Wall WA, Hohmann MG, Gray JB, Hoffmann WA (2009) Are rare species less shade tolerant than common species in fire-prone environments? A test with seven Amorpha (Fabaceae) species. Plant Ecol 205:249–260

    Article  Google Scholar 

  • Mason JL (1963) Flame photometric determination of potassium in unashed plant leaves. Anal Chem 35:874–875

    Article  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185

    Article  PubMed  Google Scholar 

  • McJennet CL, Keddy PA, Pick FR (1995) Nitrogen and phosphorus tissue concentrations in 41 wetland plants: a comparison across habitats and functional groups. Funct Ecol 9:231–238

    Article  Google Scholar 

  • Medina AL (1986) Riparian plant communities of the Fort Bayard watershed in southwestern New Mexico. Southwest Assoc Nat 31:345–359

    Article  Google Scholar 

  • Michaletz ST, Cheng D, Kerkhoff AJ, Enquist BJ (2014) Convergence of terrestrial plant production across global climate gradients. Nature 512:39–43

    Article  PubMed  CAS  Google Scholar 

  • Möllerová J (2005) Notes on invasive and expansive trees and shrubs. J For Sci 51:19–23

    Google Scholar 

  • Mosseler A, Major JE, Labrecque M, Larocque GR (2014) Allometric relationships in coppice biomass production for two North American willows (Salix spp.) across three different sites. For Ecol Manag 320:190–196

    Article  Google Scholar 

  • Naeem S, Knops JMH, Tilman D, Howe KM, Kennedy T, Gale S (2000) Plant diversity increases resistance to invasion in the absence of covarying extrinsic factors. Oikos 91:97–108

    Article  Google Scholar 

  • Ordonez A, Wright IJ, Olff H (2010) Functional differences between native and alien species: a global-scale comparison. Funct Ecol 24:1353–1361

    Article  Google Scholar 

  • Packard GC (2014) On the use of log-transformation vs. nonlinear regression for analyzing biological power-laws. Biol J Linn Soc 113:1167–11178

    Article  Google Scholar 

  • Pattison RR, Goldstein G, Ares A (1998) International association for ecology growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. Oecologia 117:449–459

    Article  PubMed  CAS  Google Scholar 

  • Penuelas J, Sardans J, Llusià J, Owen SM, Carnicer J, Giambelluca TW, Rezende EL, Waite M, Niinemets Ü (2010) Faster returns on ‘leaf economics’ and different biogeochemical niche in invasive compared with native plant species. Glob Change Biol 16:2171–2185

    Article  Google Scholar 

  • Price CA, Enquist BJ, Savage VM (2007) A general model for allometric covariation in botanical form and function. Proc Natl Acad Sci USA 104:13204–13209

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Price CA, Ogle K, White EP, Weitz JS (2009) Evaluating scaling models in biology using hierarchical Bayesian approaches. Ecol Lett 12:641–651

    Article  PubMed  PubMed Central  Google Scholar 

  • Prieur-Richard A-H, Lavorel S, Linhart YB, Dos Santos A (2002) Plant diversity, herbivory and resistance of a plant community to invasion in Mediterranean annual communities. Oecologia 130:96–104

    Article  PubMed  Google Scholar 

  • Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? In: Nentwig W (ed) Biological invasions. Ecological studies (analysis and synthesis), vol 193. Springer, Berlin, 97–125

    Google Scholar 

  • Pyšek P, Richardson DM (2010) Invasive species, environmental change and management, and health. Annu Rev Environ Resour 35:25–55

    Article  Google Scholar 

  • Pyšek P, Jarošík V, Hulme PE, Pergl J, Hejda M, Schaffner U, Vilà M (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 Change Biol 18:1725–1737

    Article  Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS, Vose JM, John C, Gresham C, Bowman WD (1998) Relationships of leaf dark respiration to leaf nitrogen, specific leaf area and leaf life-span: a test across biomes and functional groups. Oecologia 114:471–482

    Article  PubMed  Google Scholar 

  • Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003) The evolution of plant functional variation: traits, spectra, and strategies. Int J Plant Sci 164:S143–S164

    Article  Google Scholar 

  • Rosati A, Dejong TM (2003) Estimating photosynthetic radiation use efficiency using incident light and photosynthesis of individual leaves. Ann Bot 91:869–877

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith MD, Knapp AK (2001) Physiological and morphological traits of exotic, invasive exotic, and native plant species in tallgrass prairie. Int J Plant Sci 162:785–792

    Article  Google Scholar 

  • USDA, NRCS (2018) The PLANTS Database. National Plant Data Team, Greensboro. http://plants.usda.gov. Accessed 10 Jan 2018

  • 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 

  • 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 

  • Vovides AG, Vogt J, Kollert A, Berger U, Grueters U, Peters R, Lara-Domínguez AL, López-Portillo J (2014) Morphological plasticity in mangrove trees: salinity-related changes in the allometry of Avicennia germinans. Trees 28:1413–1425

    Article  Google Scholar 

  • Wang G, Jiang G, Yu S, Li Y, Liu H (2008) Invasion possibility and potential effects of Rhus typhina on Beijing municipality. J Integr Plant Biol 50:522–530

    Article  PubMed  Google Scholar 

  • Warton DI, Duursma RA, Falster DS, Taskinen S (2012) smatr 3—an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259

    Article  Google Scholar 

  • Weber E, Sun SG, Li B (2008) Invasive alien plants in China: diversity and ecological insights. Biol Invasions 10:1411–1429

    Article  Google Scholar 

  • West GB, Brown JH, Enquist BJ (1999) A general model for the structure, and algometry of plant vascular systems. Nature 400:122–126

    Article  CAS  Google Scholar 

  • Westoby M, Wright IJ (2006) Land-plant ecology on the basis of functional traits. Trends Ecol Evol 21:261–268

    Article  PubMed  Google Scholar 

  • Whitman T, Aarssen LW (2010) The leaf size/number trade-off in herbaceous angiosperms. J Plant Ecol 3:49–58

    Article  Google Scholar 

  • Williamson MH, Fitter A (1996) The characters of successful invaders. Biol Conserv 78:163–170

    Article  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  PubMed  CAS  Google Scholar 

  • Xu F, Guo W, Wang R, Xu W, Du N, Wang Y (2009) Leaf movement and photosynthetic plasticity of black locust (Robinia pseudoacacia) alleviate stress under different light and water conditions. Acta Physiol Plant 31:553–563

    Article  CAS  Google Scholar 

  • Yuan Y, Guo W, Ding W, Du N, Luo Y, Liu J, Xu F, Wang R (2013) Competitive interaction between the exotic plant Rhus typhina L. and the native tree Quercus acutissima Carr. in Northern China under different soil N:P ratios. Plant Soil 372:389–400

    Article  CAS  Google Scholar 

  • Zhang J, Xi Y, Li J (2006) The relationships between environment and plant communities in the middle part of Taihang Mountain Range, North China. Commun Ecol 7:155–163

    Article  Google Scholar 

  • Zhang Z, Jiang C, Zhang J, Zhang H, Shi L (2009) Ecophysiological evaluation of the potential invasiveness of Rhus typhina in its non-native habitats. Tree Physiol 29:1307–1316

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Tan X, Wang R, Xu N, Guo W (2013) Effects of soil moisture and light intensity on ecophysiological characteristics of Amorpha fruticosa seedlings. J For Res 24:293–300

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the two anonymous reviewers for their thoughtful comments, which helped improve the manuscript. This work was financially supported by the National Natural Science Foundation of China (Nos. 31400173, 31470402, 31770361) and the Basic Work of the Ministry of Science and Technology, China (No. 2015FY1103003-02).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ning Du.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Communicated by E. van der Maaten.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tan, X., Guo, X., Guo, W. et al. Invasive Rhus typhina invests more in height growth and traits associated with light acquisition than do native and non-invasive alien shrub species. Trees 32, 1103–1112 (2018). https://doi.org/10.1007/s00468-018-1698-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-018-1698-8

Keywords

Navigation