Biological Invasions

, Volume 21, Issue 1, pp 189–201 | Cite as

Latitudinal trends in growth, reproduction and defense of an invasive plant

  • Li Xiao
  • Maxime R. Hervé
  • Juli Carrillo
  • Jianqing DingEmail author
  • Wei HuangEmail author
Original Paper


Invasive plants often occupy an array of habitats along wide latitudinal scales which differ considerably in climatic conditions and herbivory. Variation in plant traits across latitude may play an important role in invasion success, yet few studies have tested whether there is a latitudinal pattern in invasive plant traits. Here, we sampled individuals of the invasive plant Phytolacca americana at 15 field sites spanning 10° of latitude from 25.72° to 36.15°N in central and southern China. We measured traits related to growth (plant height, canopy width, number of branches and stem diameter), reproduction (fruits per raceme and racemes per plant) and anti-herbivory defense (leaf, stem, root and fruit saponin). Overall, we found no latitudinal patterns for plant size, reproductive output or defense in growth tissues. However, growth architecture was significantly related to latitude: number of stems increased, while stem diameter decreased with increasing latitude. Reproductive architecture was also significantly related to latitude: with increasing latitude, plants produced fewer fruits per raceme, but more racemes per plant. We also found defense in reproductive tissue (fruit saponin) increased with increasing latitude. These findings provide an important latitudinal perspective for resource allocation and adaptive strategy in invasive P. americana that may aid in management recommendations at regional scales.


Environmental heterogeneity Latitudinal gradient Biotic pressures Phytolacca americana Plant invasion Temperature and Precipitation 



We thank Jian Zhang for her assistance in the field. We also thank Van Driesche Scientific Editing for revising the manuscript and providing helpful scientific input. This work was supported by the National Key Research and Development Program (2017YFC1200100, to J. Ding), the National Natural Science Foundation of China (31470447 to W. Huang) and the Youth Innovation Promotion Association of the Chinese Academy of Sciences (Y329351H03 to W. Huang).

Author contributions

JD and WH conceived the project and designed experiments. LX and WH carried out field survey. WH and MRH analyzed data with interpretation from all authors. All authors wrote the first draft of the manuscript and revised subsequent versions.

Supplementary material

10530_2018_1816_MOESM1_ESM.docx (87 kb)
Supplementary material 1 (DOCX 86 kb)


  1. Alexander JM, Edwards PJ, Poll M, Parks CG, Dietz H (2009) Establishment of parallel altitudinal clines in traits of native and introduced forbs. Ecology 90:612–622CrossRefGoogle Scholar
  2. Allen WJ, Meyerson LA, Cummings D, Anderson J, Bhattarai GP, Cronin JT (2017) Biogeography of a plant invasion: drivers of latitudinal variation in enemy release. Global Ecol Biogeogr 26:435–446CrossRefGoogle Scholar
  3. Augustin JM, Kuzina V, Andersen SB, Bak S (2011) Molecular activities, biosynthesis and evolution of triterpenoid saponins. Phytochem Rev 72:435–457CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  5. Bezemer TM, Harvey JA, Cronin JT (2014) Response of native insect communities to invasive plants. Annu Rev Entomol 59:119–141CrossRefGoogle Scholar
  6. Bhattarai GP, Meyerson LA, Anderson J, Cummings D, Allen WJ, Cronin JT (2017) Biogeography of a plant invasion: genetic variation and plasticity in latitudinal clines for traits related to herbivory. Ecol Monogr 87:57–75CrossRefGoogle Scholar
  7. Burnhan KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, BerlinGoogle Scholar
  8. Burns JH, Pardini EA, Schutzenhofer MR, Chung YA, Seidler KJ, Knight TM (2013) Greater sexual reproduction contributes to differences in demography of invasive plants and their noninvasive relatives. Ecology 94:995–1004CrossRefGoogle Scholar
  9. Chaturvedi GS, Aggarwal PK, Singh AK, Joshi MG, Sinha SK (1981) Effect of irrigation on tillering in wheat, triticale and barley in a water-limited environment. Irrig Sci 2:225–235CrossRefGoogle Scholar
  10. Colautti RI, Barrett SCH (2013) Rapid adaptation to climate facilitates range expansion of an invasive plant. Science 342:364–366CrossRefGoogle Scholar
  11. Colautti RI, Eckert CG, Barrett SCH (2010) Evolutionary constraints on adaptive evolution during range expansion in an invasive plant. Proc R Soc B Biol Sci 277:1799–1806CrossRefGoogle Scholar
  12. Coley PD, Aide T (1991) Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant-animal interaction: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 25–49Google Scholar
  13. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335CrossRefGoogle Scholar
  14. Cronin JT, Bhattarai GP, Allen WJ, Meyerson LA (2015) Biogeography of a plant invasion: plant-herbivore interactions. Ecology 96:1115–1127CrossRefGoogle Scholar
  15. Dobzhansky T (1950) Evolution in the tropics. Am Sci 38:209–221Google Scholar
  16. Elton C (1958) The ecology of invasions by animals and plants. Methuem, LondonCrossRefGoogle Scholar
  17. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. SAGE Publications, Thousand OaksGoogle Scholar
  18. Fraser J (1991) Flowering in native white clover (Trifolium repens) populations and cultivars in Nova Scotia. Can J Plant Sci 71:1173–1177CrossRefGoogle Scholar
  19. Friend DJC (1965) Tillering and leaf production in wheat as affected by temperature and light intensities. Can J Bot 43:1063–1076CrossRefGoogle Scholar
  20. Fu J, Li C, Xu J, Cheng W, Song R, Liu Y (2012) Prevention and control of invaded plant Phytolacca americana in sandy coastal shelter forests. Chin J Appl Ecol 23:991–997Google Scholar
  21. Hejda M, Pyšek P, Pergl J, Sádlo J, Chytrý M, Jarošík V (2009) Invasion success of alien plants: do habitat affinities in the native distribution range matter? Global Ecol Biogeogr 18:372–382CrossRefGoogle Scholar
  22. Hervé M (2018) RVAideMemoire: diverse basic statistical and graphical functions. R package v 0.9-55. Available at:
  23. Huang W, Ding J (2016) Effects of generalist herbivory on resistance and resource allocation by the invasive plant, Phytolacca americana. Insect Sci 23:191–199CrossRefGoogle Scholar
  24. Huang H, Fan Z (2010) Measure content of total saponins in selfheal with spectrophotometry. J Zhejiang Univ Med Sci 34:420–421Google Scholar
  25. Huang W, Siemann E, Wheeler GS, Zou J, Carrillo J, Ding J (2010) Resource allocation to defence and growth are driven by different responses to generalist and specialist herbivory in an invasive plant. J Ecol 98:1157–1167CrossRefGoogle Scholar
  26. Hughes AR, Schenck FR, Bloomberg J, Hanley TC, Feng D, Gouhier TC, Beighley RE, Kimbro DL (2016) Biogeographic gradients in ecosystem processes of the invasive ecosystem engineer Phragmites australis. Biol Invasions 18:2577–2595CrossRefGoogle Scholar
  27. Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108CrossRefGoogle Scholar
  28. Kambo D, Kotanen PM (2014) Latitudinal trends in herbivory and performance of an invasive species, common burdock (Arctium minus). Biol Invasions 16:101–112CrossRefGoogle Scholar
  29. Kim YO, Johnson JD, Lee EJ (2005) Phytotoxic effects and chemical analysis of leaf extracts from three Phytolaccaceae species in South Korea. J Chem Ecol 31:1175–1186CrossRefGoogle Scholar
  30. Kollmann J, Bañuelos MJ (2004) Latitudinal trends in growth and phenology of the invasive alien plant Impatiens glandulifera (Balsaminaceae). Divers Distrib 10:377–385CrossRefGoogle Scholar
  31. Kuebbing SE, Nuñez MA (2015) Negative, neutral, and positive interactions among nonnative plants: patterns, processes, and management implications. Global Change Biol 21:926–934CrossRefGoogle Scholar
  32. Leiblein-Wild MC, Tackenberg O (2014) Phenotypic variation of 38 European Ambrosia artemisiifolia populations measured in a common garden experiment. Biol Invasions 16:2003–2015CrossRefGoogle Scholar
  33. Li X, She D, Zhang D, Liao W (2015) Life history trait differentiation and local adaptation in invasive populations of Ambrosia artemisiifolia in China. Oecologia 177:669–677CrossRefGoogle Scholar
  34. Liu W, Maung-Douglass K, Strong DR, Pennings SC, Zhang Y (2016) Geographical variation in vegetative growth and sexual reproduction of the invasive Spartina alterniflora in China. J Ecol 104:173–181CrossRefGoogle Scholar
  35. Ma J (2013) The checklist of the Chinese invasive plants. China Higher Education Press, BeijingGoogle Scholar
  36. Maron JL, Vila M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280CrossRefGoogle Scholar
  37. Maron JL, Baer KC, Angert AL (2014) Disentangling the drivers of context-dependent plant–animal interactions. J Ecol 102:1485–1496CrossRefGoogle Scholar
  38. Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WF, Parker IM, Power AG, Seabloom EW, Torchin ME, Vazquez DP (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740CrossRefGoogle Scholar
  39. Mitich LW (1994) Common pokeweed. Weed Technol 8:887–890CrossRefGoogle Scholar
  40. Moles AT, Warton DI, Warman L, Swenson NG, Laffan SW, Zanne AE, Pitman A, Hemmings FA, Leishman MR (2009) Global patterns in plant height. J Ecol 97:923–932CrossRefGoogle Scholar
  41. Moles AT, Bonser SP, Poore AGB, Wallis IR, Foley WJ (2011) Assessing the evidence for latitudinal gradients in plant defence and herbivory. Funct Ecol 25:380–388CrossRefGoogle Scholar
  42. Moles AT, Perkins SE, Laffan SW, Flores-Moreno H, Awasthy M, Tindall ML, Sack L, Pitman A, Kattge J, Aarssen LW, Anand M, Bahn M, Blonder B, Cavender-Bares J, Cornelissen JHC, Cornwell WK, Díaz S, Dickie JB, Freschet GT, Griffiths JG, Gutierrez AG, Hemmings FA, Hickler T, Hitchcock TD, Keighery M, Kleyer M, Kurokawa H, Leishman MR, Liu K, Niinemets Ü, Onipchenko V, Onoda Y, Penuelas J, Pillar VD, Reich PB, Shiodera S, Siefert A, Sosinski EE, Soudzilovskaia NA, Swaine EK, Swenson NG, van Bodegom PM, Warman L, Weiher E, Wright IJ, Zhang H, Zobel M, Bonser SP (2014) Which is a better predictor of plant traits: temperature or precipitation? J Veg Sci 25:1167–1180CrossRefGoogle Scholar
  43. Montague JL, Barrett SCH, Eckert CG (2008) Re-establishment of clinal variation in flowering time among introduced populations of purple loosestrife (Lythrum salicaria, Lythraceae). J Evol Biol 21:234–245CrossRefGoogle Scholar
  44. Moravcová L, Pyšek P, Jarošík V, Pergl J (2015) Getting the right traits: reproductive and dispersal characteristics predict the invasiveness of herbaceous plant species. PLoS ONE 10:e0123634CrossRefGoogle Scholar
  45. Oduor AMO, Lankau RA, Strauss SY, Gómez JM (2011) Introduced Brassica nigra populations exhibit greater growth and herbivore resistance but less tolerance than native populations in the native range. New Phytol 191:536–544CrossRefGoogle Scholar
  46. Oksanen J, Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin P, O’Hara R, Simpson G, Solymos P, Stevens M, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2.4-5. Available at:
  47. Pennings SC, Siska EL, Bertness MD (2001) Latitudinal differences in plant palatability in Atlantic coast salt marshes. Ecology 82:1344–1359CrossRefGoogle Scholar
  48. Pennings SC, Ho C-K, Salgado CS, Wieski K, Dave N, Kunza AE, Wason EL (2009) Latitudinal variation in herbivore pressure in Atlantic Coast salt marshes. Ecology 90:183–195CrossRefGoogle Scholar
  49. Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294CrossRefGoogle Scholar
  50. Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecol Lett 14:476–483CrossRefGoogle Scholar
  51. Richardson DM, Pyšek P (2012) Naturalization of introduced plants: ecological drivers of biogeographical patterns. New Phytol 196:383–396CrossRefGoogle Scholar
  52. Rondanini DP, del Pilar Vilariño M, Roberts ME, Polosa MA, Botto JF (2014) Physiological responses of spring rapeseed (Brassica napus) to red/far-red ratios and irradiance during pre-and post-flowering stages. Physiol Plant 152:784–794CrossRefGoogle Scholar
  53. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Evol S 32:305–332CrossRefGoogle Scholar
  54. Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K (2009) Is there a latitudinal gradient in the importance of biotic interactions? Annu Rev Ecol Evol S 40:245–269CrossRefGoogle Scholar
  55. Stephenson RA, Gallagher EC (1986) Effects of night temperature on floral initiation and raceme development in macadamia. Sci Hortic Amst 30:213–218CrossRefGoogle Scholar
  56. Stützel H, Kahlen K (2016) Virtual plants: modeling plant architecture in changing environments. Front Plant Sci 7:1734CrossRefGoogle Scholar
  57. Szakiel A, Pączkowski C, Henry M (2011) Influence of environmental abiotic factors on the content of saponins in plants. Phytochem Rev 10:471–491CrossRefGoogle Scholar
  58. Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273CrossRefGoogle Scholar
  59. Van Pelt R (2008) Identifying old trees and forests in eastern Washington. Washington State Department of Natural Resources, OlympiaGoogle Scholar
  60. Weber E, Schmid B (1998) Latitudinal population differentiation in two species of Solidago (Asteraceae) introduced into Europe. Am J Bot 85:1110–1121CrossRefGoogle Scholar
  61. Xu H, Qiang S, Han Z, Guo J, Huang Z, Sun H, He S, Ding H, Wu H, Wan F (2006) The status and causes of alien species invasion in China. Biodivers Conserv 15:2893–2904CrossRefGoogle Scholar
  62. Xu H, Qiang S, Genovesi P, Ding H, Wu J, Meng L, Han Z, Miao J, Hu B, Guo J, Sun H, Huang C, Lei J, Le Z, Zhang X, He S, Wu Y, Zheng Z, Chen L, Jarošik V, Pyšek P (2012) An inventory of invasive alien species in China. NeoBiota 15:1–26CrossRefGoogle Scholar
  63. Yang X, Huang W, Tian B, Ding J (2014) Differences in growth and herbivory damage of native and invasive kudzu (Peuraria montana var. lobata) populations grown in the native range. Plant Ecol 215:339–346CrossRefGoogle Scholar
  64. Zhai S, Li C, Xu J, Liu L, Zhang D, Zhou Z (2010) Spatial and temporal dynamics of Phytolacca americana seed rain under Robinia pseudoacacia forest in Lingshan Bay National Forest Park, Shandong, China. Chin J Plant Ecol 34:1236–1242Google Scholar
  65. Zhang B, Chen H, Hou X, Fang Q, Jiang J, Pei C, Xu D, Ji L, Yun X, Han W (2015) Ecological response of reproductive performance of Stipa baicalensis in Xilingol steppe of Inner Mongolia. J Gansu Agric Univ 50:103–108Google Scholar
  66. Zhao C, Sun Y, Chen Z, Wei F, Wen G, Tang X, Xiao X, Li S (2016) Responses of the anthocyanin and saponin contents of the vegetative organs of one-year—old purple and green aerial stemmed Panax notoginseng plants to the low temperature stress simulated by icy water. Lishizhen Med Mater Medica Res 27:2492–2496Google Scholar
  67. Zheng Y, Feng Y, Zhang L, Callaway RM, Valiente-Banuet A, Luo D, Liao Z, Lei Y, Barclay GF, Silva-Pereyra C (2015) Integrating novel chemical weapons and evolutionarily increased competitive ability in success of a tropical invader. New Phytol 205:1350–1359CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical GardenChinese Academy of SciencesWuhanChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.INRA, UMR1349 IGEPPLe RheuFrance
  4. 4.Faculty of Land and Food Systems, Biodiversity Research CentreThe University of British ColumbiaVancouverCanada
  5. 5.College of Life SciencesHenan UniversityKaifengChina
  6. 6.Institute of Plant SciencesUniversity of BernBernSwitzerland

Personalised recommendations