Effects of Different Types of Heavy Metal Pollution on Functional Traits of Invasive Redroot Pigweed and Native Red Amaranth

  • Congyan WangEmail author
  • Bingde Wu
  • Kun Jiang
  • Jiawei Zhou
Research paper


The differences in functional traits between invasive plant species (invaders hereafter) and natives are believed to be closely associated with whether the former are successful invasion. Meanwhile, variability in the type of heavy metal pollution can alter the growth and physiological performance of invaders. Thus, determination of the potential effects of different types of heavy metal pollution on functional traits of invaders is vital for illuminating the mechanisms supporting the success of invaders. This study aims to address the effects of the separated treatment of Cu, Cd, and the combined treatments of Cu and Cd on functional traits of invasive redroot pigweed (Amaranthus retroflexus L.; pigweed hereafter) and native red amaranth (A. tricolor L.; amaranth hereafter). Pigweed was significantly taller than amaranth under most treatments. The greater height of pigweed may award greater competitive ability for resource acquisition (particularly sunlight). Leaf shape index of pigweed was significantly larger than that of amaranth under all treatments. The larger leaf shape index of pigweed can enhance the efficiency of resource capture (especially sunlight capture) via adjustments to leaf shape and size. Hence, the higher height and leaf shape index of pigweed may facilitate its further invasion process. Heavy metal pollution (especially Cd) poses significant adverse effects on the growth and physiological performance of the two Amaranthus species. This may be because heavy metal pollution, especially Cd, can mediate toxicity on plant species. The combined treatments of Cu and Cd can confer an antagonistic effect on functional traits of the two Amaranthus species compared with the separated treatment of Cu or Cd. The main reason may be the fact that Cd and Cu influence each other’s uptake for plants.

Graphical Abstract


Amaranthus retroflexus Heavy metal pollution Invasive plant species Leaf functional traits Resource capture 



This study was supported by National Key Research & Development Program of China (2016YFC0502002), Open Science Research Fund of State Key Laboratory of Pollution Control and Resource Reuse (Tongji University), China (PCRRF17015), National Natural Science Foundation of China (31300343), and Jiangsu Collaborative Innovation Center of Technology and Material of Water Treatment.


  1. Aan A, Hallik L, Kull O (2006) Photon flux partitioning among species along a productivity gradient of an herbaceous plant community. J Ecol 94:143–1155. CrossRefGoogle Scholar
  2. Abbaslou H, Bakhtiari S (2017) Phytoremediation potential of heavy metals by two native pasture plants (Eucalyptus grandis and ailanthus altissima) assisted with AMF and fibrous minerals in contaminated mining regions. Pollution 3:471–486. CrossRefGoogle Scholar
  3. An YJ, Kim YM, Kwon TI, Jeong SW (2004) Combined effect of copper, cadmium, and lead upon Cucumis sativus growth and bioaccumulation. Sci Total Environ 326:85–93. CrossRefGoogle Scholar
  4. Arredondo M, Martínez R, Núñez MT, Ruz M, Olivares M (2006) Inhibition of iron and copper uptake by iron, copper and zinc. Biol Res 39:95–102. CrossRefGoogle Scholar
  5. Chen HY, Teng YG, Lu SJ, Wang YY, Wang JS (2015) Contamination features and health risk of soil heavy metals in China. Sci Total Environ 512–513:143–153. CrossRefGoogle Scholar
  6. Cheng MM, Wu LH, Huang YJ, Luo YM, Christie P (2014) Total concentrations of heavy metals and occurrence of antibiotics in sewage sludges from cities throughout China. J Soil Sediment 14:1123–1135. CrossRefGoogle Scholar
  7. DeMalach N, Zaady E, Kadmon R (2017) Light asymmetry explains the effect of nutrient enrichment on grassland diversity. Ecol Lett 20:60–69. CrossRefGoogle Scholar
  8. Dwyer JM, Hobbs R, Mayfield MM (2014) Specific leaf area responses to environmental gradients through space and time. Ecology 95:399–410. CrossRefGoogle Scholar
  9. Funk JL, Standish RJ, Stock WD, Valladares F (2016) Plant functional traits of dominant native and invasive species in Mediterranean-climate ecosystems. Ecology 97:75–83. CrossRefGoogle Scholar
  10. Gallagher RV, Randall RP, Leishman MR (2015) Trait differences between naturalized and invasive plant species independent of residence time and phylogeny. Conserv Biol 29:360–369. CrossRefGoogle Scholar
  11. Gayomba SR, Jung H, Yan J, Danku J, Rutzke MA, Bernal M, Krämer U, Kochian LV, Salt DE, Vatamaniuk OK (2013) The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana. Metallomics 5:1262–1275. CrossRefGoogle Scholar
  12. Ge W, Jiao YQ, Sun BL, Qin R, Jiang WS, Liu DH (2012) Cadmium-mediated oxidative stress and ultrastructural changes in root cells of poplar cultivars. S Afr J Bot 83:98–108. CrossRefGoogle Scholar
  13. Gleason SM, Ares A (2004) Photosynthesis, carbohydrate storage and survival of a native and an introduced tree species in relation to light and defoliation. Tree Physiol 24:1087–1097. CrossRefGoogle Scholar
  14. Gouveia AC, Freitas H (2009) Modulation of leaf attributes and water use efficiency in Quercus suber along a rainfall gradient. Trees 23:267–275. CrossRefGoogle Scholar
  15. Gross N, Suding KN, Lavorel S, Roumet C (2007) Complementarity as a mechanism of coexistence between functional groups of grasses. J Ecol 95:1296–1305. CrossRefGoogle Scholar
  16. Gross N, Börger L, Duncan RP, Hulme PE (2013) Functional differences between alien and native species: do biotic interactions determine the functional structure of highly invaded grasslands? Funct Ecol 27:1262–1272. CrossRefGoogle Scholar
  17. Hang ZH, Wu HP (2016) Zhenjiang yearbook (The first edition). In: Chen J, Liu S (eds) Organized by Zhenjiang municipal people’s government and Writed by Zhenjiang local records office, vol 25. Publishing House of Local Records, Beijing, p 27Google Scholar
  18. Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Science 324:636–638. CrossRefGoogle Scholar
  19. Huang SS, Liao QL, Hua M, Wu XM, Bi KS, Yan CY, Chen B, Zhang XY (2007) Survey of heavy metal pollution and assessment of agricultural soil in Yangzhong District, Jiangsu Province, China. Chemosphere 67:2148–2155. CrossRefGoogle Scholar
  20. Ishii H, Asano S (2010) The role of crown architecture, leaf phenology and photosynthetic activity in promoting complementary use of light among coexisting species in temperate forests. Ecol Res 25:715–722. CrossRefGoogle Scholar
  21. Jeong N, Moon J, Kim H, Kim C, Jeong S (2011) Fine genetic mapping of the genomic region controlling leaflet shape and number of seeds per pod in the soybean. Theor Appl Genet 122:865–874. CrossRefGoogle Scholar
  22. Kardel F, Wuyts K, Babanezhad M, Vitharana UWA, Wuytack T, Potters G, Samson R (2010) Assessing urban habitat quality based on specific leaf area and stomatal characteristics of Plantago lanceolata L. Environ Pollut 158:788–794. CrossRefGoogle Scholar
  23. Kim AY, Kim JY, Ko MS, Kim KW (2010) Acid rain impact on phytoavailability of heavy metals in soils. Geosyst Eng 13:133–138. CrossRefGoogle Scholar
  24. LeBel P, Bradley RL, Thiffault N (2013) The relative importance of nitrogen vs. moisture stress may drive intraspecific variations in the SLA-RGR relationship: the case of Picea mariana seedlings. Am J Plant Sci 4:1278–1284. CrossRefGoogle Scholar
  25. 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. CrossRefGoogle Scholar
  26. Liu FD, Yang WJ, Wang ZS, Xu Z, Liu H, Zhang M, Liu YH, An SQ, Sun SC (2010) Plant size effects on the relationships among specific leaf area, leaf nutrient content, and photosynthetic capacity in tropical woody species. Acta Oecol 36:149–159. CrossRefGoogle Scholar
  27. Majsec K, Cvjetko P, Tolić S, Tkalec M, Balen B, Pavlica M (2016) Integrative approach gives new insights into combined Cd/Cu exposure in tobacco. Acta Physiol Plant 38:142. CrossRefGoogle Scholar
  28. Mandák B, Zákravský P, Dostál P, Plačková I (2011) Population genetic structure of the noxious weed Amaranthus retroflexus in Central Europe. Flora 206:697–703. CrossRefGoogle Scholar
  29. Marteinsdóttir B, Eriksson O (2014) Plant community assembly in semi-natural grasslands and ex-arable fields: a trait-based approach. J Veg Sci 25:77–87. CrossRefGoogle Scholar
  30. Mattina MJI, Lannucci-Berger W, Musante C, White JC (2003) Concurrent plant uptake of heavy metal and persistent organic pollutants from soil. Environ Pollut 124:375–378. CrossRefGoogle Scholar
  31. Meng FQ, Cao R, Yang DM, Niklas KJ, Sun SC (2014) Trade-offs between light interception and leaf water shedding: a comparison of shade- and sun-adapted species in a subtropical rainforest. Oecologia 174:13–22. CrossRefGoogle Scholar
  32. Moharami S, Jalali M (2015) Effect of acid rain on the fractionation of heavy metals and major elements in contaminated soils. Chem Ecol 31:160–172. CrossRefGoogle Scholar
  33. Motesharezadeh B, Kamal-poor S, Alikhani HA, Zarei M, Azimi S (2017) Investigating the effects of plant growth promoting bacteria and Glomus Mosseae on cadmium phytoremediation by Eucalyptus camaldulensis L. Pollution 3(4):575–588. CrossRefGoogle Scholar
  34. Murtaza G, Javed W, Hussain A, Qadir M, Aslam M (2017) Soil-applied zinc and copper suppress cadmium uptake and improve the performance of cereals and legumes. Int J Phytoremediat 19:199–206. CrossRefGoogle Scholar
  35. Powell KI, Chase JM, Knight TM (2013) Invasive plants have scale-dependent effects on diversity by altering species-area relationships. Science 339:316–318. CrossRefGoogle Scholar
  36. Scheepens JF, Frei ES, Stöcklin J (2010) Genotypic and environmental variation in specific leaf area in a widespread Alpine plant after transplantation to different altitudes. Oecologia 164:141–150. CrossRefGoogle Scholar
  37. Sheppard CS, Burns BR (2014) Effects of interspecific alien versus intraspecific native competition on growth of native woody plants. Plant Ecol 215:1527–1538. CrossRefGoogle Scholar
  38. Shi HP, Feng Y, Wang YL, Tsang PKE (2014) Effect of cadmium on cytogenetic toxicity in hairy roots of Wedelia trilobata L. and their alleviation by exogenous CaCl2. Environ Sci Poll Res 21:1436–1443. CrossRefGoogle Scholar
  39. Sun YB, Zhou QX, Liu WT, An J, Xu ZQ, Wang L (2009) Joint effects of arsenic and cadmium on plant growth and metal bioaccumulation: a potential Cd-hyperaccumulator and As-excluder Bidens pilosa L. J Hazard Mater 165:1023–1028. CrossRefGoogle Scholar
  40. Thomson FJ, Moles AT, Auld TD, Kingsford RT (2011) Seed dispersal distance is more strongly correlated with plant height than with seed mass. J Ecol 99:1299–1307. CrossRefGoogle Scholar
  41. Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892. CrossRefGoogle Scholar
  42. Wang Z, Zhang L (2012) Leaf shape alters the coefficients of leaf area estimation models for Saussurea stoliczkai in central Tibet. Photosynthetica 50:337–342. CrossRefGoogle Scholar
  43. Wang HT, Wang QJ, Cui ZQ, Sun Z, Sun C (2011) Analysis of correlation among heavy metals elements and background value of heavy metal elements in soil of nantong suburb. J Anhui Agric Sci 39:14062–14064 (In Chinese) Google Scholar
  44. Wang L, Zhang F, Wang CY, Xiao HG, Shi YC, Zhao LL, Du DL (2015) Insights into the ecotoxicological effects of leaf aqueous extract of Solidago canadensis on seed germination and growth of Lactuca sativa under Cu and Cd pollution. Asian J Ecotoxicol 10:203–209. (In Chinese) CrossRefGoogle Scholar
  45. Wang CY, Liu J, Xiao HG, Zhou JW (2016a) Differences in leaf functional traits between Rhus typhina and native species. Clean 44:1591–1597. CrossRefGoogle Scholar
  46. Wang CY, Xiao HG, Liu J, Zhou JW, Dun DL (2016b) Insights into the effects of simulated nitrogen deposition on leaf functional traits of Rhus typhina. Pol J Environ Stud 25:1279–1284. CrossRefGoogle Scholar
  47. Wang CY, Zhou JW, Xiao HG, Liu J, Wang L (2017a) Variations in leaf functional traits among plant species grouped by growth and leaf types in Zhenjiang, China. J For Res 28:241–248. CrossRefGoogle Scholar
  48. Wang CY, Liu J, Zhou JW, Xiao HG (2017b) Differences in leaf functional traits between exotic and native Compositae plant species. J Cent South Univ 24:2468–2474. CrossRefGoogle Scholar
  49. Wang CY, Zhou JW, Liu J, Jiang K (2017c) Differences in functional traits between invasive and native Amaranthus species under different forms of N deposition. Sci Nat 104:59. CrossRefGoogle Scholar
  50. Wang CY, Zhou JW, Liu J, Xiao HG, Wang L (2018a) Differences in functional traits and reproductive allocations between native and invasive plants. J Cent South Univ. CrossRefGoogle Scholar
  51. Wang CY, Jiang K, Liu J, Zhou JW, Wu BD (2018b) Moderate and heavy Solidago canadensis L. invasion are associated with decreased taxonomic diversity but increased functional diversity of plant communities in East China. Ecol Eng 112:55–64. CrossRefGoogle Scholar
  52. Wang CY, Jiang K, Zhou JW, Wu BD (2018c) Solidago canadensis invasion affects soil N-fixing bacterial communities in heterogeneous landscapes in urban ecosystems in East China. Sci Total Environ 631–632:702–713. CrossRefGoogle Scholar
  53. Yang Y, Zhao WJ, Li ZH, Zhu SF (2011) Molecular identification of a ‘Candidatus Phytoplasma ziziphi’-related strain infecting Amaranth (Amaranthus retroflexus L.) in China. J Phytopathol 159:635–637. CrossRefGoogle Scholar

Copyright information

© University of Tehran 2018

Authors and Affiliations

  1. 1.Institute of Environment and Ecology, Academy of Environmental Health and Ecological Security and School of the Environment and Safety EngineeringJiangsu UniversityZhenjiangPeople’s Republic of China
  2. 2.State Key Laboratory of Pollution Control and Resource ReuseTongji UniversityShanghaiPeople’s Republic of China

Personalised recommendations