Abstract
Leaf resource allocation plays a significant role in the evolution of plant functional strategies, where tradeoffs between defense, structure, and different components of photosynthesis drive the partitioning of carbon and nitrogen. One hypothesized but underexplored mechanism of the success of many invasive species in competition with natives is reallocation of resources toward higher photosynthetic capacity, assuming they experience reduced pest consumption in their invaded (‘away’) range. We examined leaf function and chemistry in the context of carbon and nitrogen (N) budgets in home- (Japan) and away-range (France and USA) populations of the global invader, Japanese knotweed (Reynoutria japonica (Houtt.) var. japonica). In 38 field populations, we measured photosynthetic CO2 (A-Ci) response curves and quantified the proportion of leaf N allocated to separate photosynthetic processes, including carboxylation (Rubisco content), light harvesting, and the electron transport chain, plus the amount of N allocated to cell structure (cell wall protein) and defense (total alkaloids, cyanogenic glycosides). Consistent with our hypothesis, we found significantly higher leaf N allocation to photosynthesis in both away range populations, particularly Rubisco content, along with higher total leaf N in USA populations. However, neither maximum carboxylation capacity nor light-saturated photosynthetic rates were greater in the away ranges, nor did we find reduced allocation to leaf structure (cell wall protein). Further, USA populations had significantly greater concentrations of defensive cyanogenic glycosides, where some native-range herbivores have unintentionally been introduced. Our study suggests that away-range changes in invader leaf function may be more complex than a simple expectation based on photosynthetic capacity.
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References
Aguilera AG, Alpert P, Dukes JS, Harrington R (2010) Impacts of the invasive plant Fallopia japonica (Houtt.) on plant communities and ecosystem processes. Biol Invasions 12:1243–1252
Bahar NHA, Ishida FY, Weerasinghe LK, Guerrieri R, O’Sullivan OS, Bloomfield KJ, Asner GP, Martin RE, Lloyd J, Malhi Y, Phillips OL, Meir P, Salinas N, Cosio EG, Domingues TF, Quesada CA, Sinca F, Escudero Vega A, Zuloaga Ccorimanya PP, Atkin OK (2017) Leaf-level photosynthetic capacity in lowland Amazonian and high-elevation Andean tropical moist forests of Peru. New Phytol 214(3):1002–1018. https://doi.org/10.1111/nph.14079
Barney JN, Tharayil N, DiTommaso A, Bhowmik PC (2006) The biology of invasive alien plants in Canada. 5. Polygonum cuspidatum Sieb. & Zucc. [= Fallopia japonica (Houtt.) Ronse Decr.]. Can J Plant Sci 86(3):887–906. https://doi.org/10.4141/P05-170
Beerling DJ, Huntley B, Bailey JP (1995) Climate and the distribution of Fallopia japonica: use of an introduced species to test the predictive capacity of response surfaces. J Veg Sci 6(2):269–282
Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83(5):887–889
Brandenburger CR, Cooke J, Sherwin WB, Moles AT (2019) Rapid evolution of leaf physiology in an introduced beach daisy. Proc R Soc b: Biol Sci 286(1909):20191103. https://doi.org/10.1098/rspb.2019.1103
Brinker AM, Seigler DS (1989) Methods for the detection and quantitative determination of cyanide in plant materials. Phytochem Bull 21(2):24
Cui G, Ji G, Liu S, Li B, Lian L, He W, Zhang P (2019) Physiological adaptations of Elymus dahuricus to high altitude on the Qinghai-Tibetan Plateau. Acta Physiol Plant 41(7):115. https://doi.org/10.1007/s11738-019-2904-z
Desjardins SD, Pashley CH, Bailey JP (2023) A taxonomic, cytological and genetic survey of Japanese knotweed sl in New Zealand indicates multiple secondary introductions from Europe and a direct introduction from Japan. New Zealand J Botany 61(1):49–66
Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78(1):9–19
Evans JR, Clarke VC (2019) The nitrogen cost of photosynthesis. J Exp Bot 70(1):7–15
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Biol 40(1):503–537
Feng Y-L, Fu G-L (2008) Nitrogen allocation, partitioning and use efficiency in three invasive plant species in comparison with their native congeners. Biol Invasions 10:891–902
Feng Y-L et al (2009) Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant. Proc Natl Acad Sci 106(6):1853–1856. https://doi.org/10.1073/pnas.0808434106
Forman J, Kesseli RV (2003) Sexual reproduction in the invasive species Fallopia japonica (Polygonaceae). Am J Bot 90(4):586–592
Fridley JD (2013) Plant invasions across the Northern Hemisphere: a deep-time perspective. Ann N Y Acad Sci 1293(1):8–17
Fridley JD, Sax DF (2014) The imbalance of nature: Revisiting a D arwinian framework for invasion biology. Glob Ecol Biogeogr 23(11):1157–1166
Fridley JD, Bauerle TL, Craddock A, Ebert AR, Frank DA, Heberling JM, Hinman ED, Jo I, Martinez KA, Smith MS (2022) Fast but steady: an integrated leaf-stem-root trait syndrome for woody forest invaders. Ecol Lett 25(4):900–912
Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446(7139):1079–1081
Funk JL, Glenwinkel LA, Sack L (2013) Differential allocation to photosynthetic and non-photosynthetic nitrogen fractions among native and invasive species. PLoS ONE 8(5):e64502
Gammon MA, Kesseli R (2010) Haplotypes of Fallopia introduced into the US. Biol Invasions 12:421–427
Gammon MA, Grimsby JL, Tsirelson D, Kesseli R (2007) Molecular and morphological evidence reveals introgression in swarms of the invasive taxa Fallopia japonica, F. sachalinensis, and F.× bohemica (Polygonaceae) in the United States. Am J Bot 94(6):948–956
Gerber E, Krebs C, Murrell C, Moretti M, Rocklin R, Schaffner U (2008) Exotic invasive knotweeds (Fallopia spp.) negatively affect native plant and invertebrate assemblages in European riparian habitats. Biol Conserv 141(3):646–654. https://doi.org/10.1016/j.biocon.2007.12.009
Gleadow RM, Møller BL (2014) Cyanogenic glycosides: synthesis, physiology, and phenotypic plasticity. Annu Rev Plant Biol 65:155–185
Hari V, Rakovec O, Markonis Y, Hanel M, Kumar R (2020) Increased future occurrences of the exceptional 2018–2019 central European drought under global warming. Sci Rep 10(1):12207
Heberling JM, Fridley JD (2013) Resource-use strategies of native and invasive plants in Eastern North American forests. New Phytol 200(2):523–533
Heberling JM, Fridley JD (2016) Invaders do not require high resource levels to maintain physiological advantages in a temperate deciduous forest. Ecology 97(4):874–884
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(6):875–884
Hikosaka K (2004) Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance. J Plant Res 117:481–494
Hikosaka K, Shigeno A (2009) The role of Rubisco and cell walls in the interspecific variation in photosynthetic capacity. Oecologia 160:443–451
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(6):605–618
Hinman ED, Fridley JD, Parry D (2019) Plant defense against generalist herbivores in the forest understory: a phylogenetic comparison of native and invasive species. Biol Invasions 21:1269–1281
Hirose T (1984) Nitrogen use efficiency in growth of Polygonum cuspidatum Sieb. Et Zucc. Ann Bot 54(5):695–704
Hollingsworth ML, Bailey JP (2000) Evidence for massive clonal growth in the invasive weed Fallopia japonica (Japanese Knotweed). Bot J Linnean Soc 133(4):463–472
Howard Bradbury J, Bradbury MG, Egan SV (1994) Comparison of methods of analysis of cyanogens in cassava. Int Workshop Cassava Saf 375:87–96
Jo I, Fridley JD, Frank DA (2017) Invasive plants accelerate nitrogen cycling: evidence from experimental woody monocultures. J Ecol 105(4): 1105–1110
John B, Sulaiman CT, George S, Reddy VRK (2014) Spectrophotometric estimation of total alkaloids in selected Justicia species. Int J Pharm Pharm Sci 6(5):647–648
Johnson LR, Breger B, Drummond F (2019) Novel plant–insect interactions in an urban environment: enemies, protectors, and pollinators of invasive knotweeds. Ecosphere 10(11):e02885
Liu W, Zhang Y, Chen X, Maung-Douglass K, Strong DR, Pennings SC (2020) Contrasting plant adaptation strategies to latitude in the native and invasive range of Spartina alterniflora. New Phytol 226(2):623–634. https://doi.org/10.1111/nph.16371
Luo X, Keenan TF, Chen JM, Croft H, Colin Prentice I, Smith NG, Walker AP, Wang H, Wang R, Xu C (2021) Global variation in the fraction of leaf nitrogen allocated to photosynthesis. Nat Commun 12(1):4866
Machino S, Nagano S, Hikosaka K (2021) The latitudinal and altitudinal variations in the biochemical mechanisms of temperature dependence of photosynthesis within Fallopia japonica. Environ Exp Bot 181:104248
Makino A, Mae T, Ohira K (1986) Colorimetric measurement of protein stained with Coomassie Brilliant Blue R on sodium dodecyl sulfate-polyacrylamide gel electrophoresis by eluting with formamide. Agric Biol Chem 50(7):1911–1912
Makkar HPS, Siddhuraju P, Becker K (2007) Plant secondary metabolites. Methods Mol Biol 393:1–122. https://doi.org/10.1007/978-1-59745-425-4_1
Maranna MC, Saikrishnan LM, Dinesh TK, Tyagi KK (2018) Determination of hydrogen cyanide in cigarette smoke by continuous flow analysis method using safer chemistry. Contrib Tob Nicotine Res 28(4):191–202
Martinez KA, Fridley JD, Oguchi R, Aiba M, Hikosaka K (2019) Functional shifts in leaves of woody invaders of deciduous forests between their home and away ranges. Tree Physiol 39(9):1551–1560. https://doi.org/10.1093/treephys/tpz065
Matzek V (2011) Superior performance and nutrient-use efficiency of invasive plants over non-invasive congeners in a resource-limited environment. Biol Invasions 13(12):3005–3014. https://doi.org/10.1007/s10530-011-9985-y
Maurel N, Fujiyoshi M, Muratet A, Porcher E, Motard E, Gargominy O, Machon N (2013) Biogeographic comparisons of herbivore attack, growth and impact of J apanese knotweed between J apan and F rance. J Ecol 101(1):118–127
McDowell SC (2002) Photosynthetic characteristics of invasive and noninvasive species of Rubus (Rosaceae). Am J Bot 89(9):1431–1438
Ness JH, Morales MA, Kenison E, Leduc E, Leipzig-Scott P, Rollinson E, Swimm BJ, Von Allmen DR (2013) Reciprocally beneficial interactions between introduced plants and ants are induced by the presence of a third introduced species. Oikos 122(5):695-704
Niinemets Ü, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant, Cell Environ 20(7):845–866
Niinemets Ü, Valladares F, Ceulemans R (2003) Leaf-level phenotypic variability and plasticity of invasive Rhododendron ponticum and non-invasive Ilex aquifolium co-occurring at two contrasting European sites. Plant, Cell Environ 26(6):941–956. https://doi.org/10.1046/j.1365-3040.2003.01027.x
Oduor AMO (2022) Invasive plant species that experience lower herbivory pressure may evolve lower diversities of chemical defense compounds in the exotic range. Am J Bot 109(9):1382–1393. https://doi.org/10.1002/ajb2.16053
Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Funct Ecol 18(3):419–425
Onoda Y, Wright IJ, Evans JR, Hikosaka K, Kitajima K, Niinemets Ü, Poorter H, Tosens T, Westoby M (2017) Physiological and structural tradeoffs underlying the leaf economics spectrum. New Phytol 214(4):1447–1463
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(6):648–658
Osone Y, Tateno M (2003) Effects of stem fraction on the optimization of biomass allocation and maximum photosynthetic capacity. Funct Ecol 17(5):627–636
Patton CA, Ranney TG, Burton JD, Walgenbach JF (1997) Natural pest resistance of Prunus taxa to feeding by adult Japanese beetles: Role of endogenous allelochemicals in host plant resistance. J Am Soc Hortic Sci 122(5):668–672
Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24(9):497–504
Porra RJ, Thompson WAA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta (BBA) Bioenerg 975(3):384–394
Qing H, Cai Y, Xiao Y, Yao Y, An S (2012) Leaf nitrogen partition between photosynthesis and structural defense in invasive and native tall form Spartina alterniflora populations: effects of nitrogen treatments. Biol Invasions 14(10):2039–2048. https://doi.org/10.1007/s10530-012-0210-4
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Raven PH, Evert RF, Eichhorn SE (2005) Biology of plants: biology of plants. Peter Marshall, New York, NY
Stacklies W, Redestig H, Scholz M, Walther D, Selbig J (2007) pcaMethods—a bioconductor package providing PCA methods for incomplete data. Bioinformatics 23(9):1164–1167
Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant, Cell Environ 27(8):1047–1054
Teulier L, Puijalon S, Boisselet C, Piola F (2022) The clone wars: the Japanese knotweed (Fallopia japonica) vs the black vine weevil (Otiorhynchus sulcatus), characterization of a potential herbivory. bioRxiv 23:93
Townsend A (1997) Japanese knotweed: a reputation lost. Arnoldia 57(3):13–19
Xing K, Zhao M, Niinemets Ü, Niu S, Tian J, Jiang Y, Chen HYH, White PJ, Guo D, Ma Z (2021) Relationships between leaf carbon and macronutrients across woody species and forest ecosystems highlight how carbon is allocated to leaf structural function. Front Plant Sci 12:674932
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(7):702-708
Wagner H, Bladt S (1996) Plant drug analysis: a thin layer chromatography atlas. Springer, Berlin
Warren CR, Adams MA (2001) Distribution of N, Rubisco and photosynthesis in Pinus pinaster and acclimation to light. Plant, Cell Environ 24(6):597–609
Warren CR, Adams MA, Chen Z (2000) Is photosynthesis related to concentrations of nitrogen and Rubisco in leaves of Australian native plants? Funct Plant Biol 27(5):407–416
Warren CR, Dreyer E, Adams MA (2003) Photosynthesis-Rubisco relationships in foliage of Pinus sylvestris in response to nitrogen supply and the proposed role of Rubisco and amino acids as nitrogen stores. Trees 17:359–366
Williams V-RJ, Sahli HF (2016) A comparison of herbivore damage on three invasive plants and their native congeners: Implications for the enemy release hypothesis. Castanea 81:128–137
Zhang YY, Parepa M, Fischer M, Bossdorf O (2016) Epigenetics of colonizing species? A study of Japanese knotweed in central Europe. In: Barrett SCH et al (eds) Invasion genetics: the Baker and Stebbins legacy. Wiley, New Jersey, pp 328–340
Acknowledgements
This project was supported by grant IOS-1754273 from the U.S. National Science Foundation. We thank research assistants Morgane Dauvé, Morgan Bault, Jeremy Delamare, Tiphaine Mroczek, Océane Raymond, Noémie Pernes, Noelle Stevens, and Ilknur Yakilkan, and two anonymous reviewers.
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Funding was provided by National Science Foundation (Grant no: IOS-1754273).
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This study was conceived by JF with input from co-PIs KH, TK, and GD. All authors contributed to the design of the study. Data collection was performed by RJG-N, LB, TK, JL, and MM. Data curation and formal analysis were performed by RJG-N and J Fridley. The initial draft of the manuscript from written by RJG-N and JF. All authors read and approved the final manuscript.
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Griffin-Nolan, R.J., Bensaddek, L., Decocq, G. et al. Away-range shifts in leaf function of a global invader: a case of resource reallocation?. Biol Invasions (2024). https://doi.org/10.1007/s10530-024-03262-0
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DOI: https://doi.org/10.1007/s10530-024-03262-0