Abstract
Invasive plant species are often found to have advantages over native species in growth-related traits, such as photosynthetic rate, in disturbed or resource-rich environments. However, resource-use efficiency, rather than opportunistic resource capture, may confer more advantages when resources are scarce. In this study, performance and functional traits of invasive and non-invasive members of the genus Pinus were contrasted under the condition of nutrient limitations. Invasive species outperformed non-invasive congeners by growing 28% faster, on average. Invasives and non-invasives did not differ in biomass allocation traits (root-weight ratio, stem-weight ratio, leaf-weight ratio, leaf area ratio, root: shoot coefficient), but invaders had thinner and/or less dense leaves, as shown by a significantly lower leaf mass per area and leaf dry mass fraction. No differences between invasives and non-invasives were apparent in area-based leaf content of nitrogen, chlorophyll, or total protein, nor did the two groups differ in how efficiently they took up nutrients (specific absorption rate per unit root mass). The trait most strongly associated with invasives’ superior performance was photosynthetic nitrogen-use efficiency. Non-invaders were more water-use efficient. The results suggests that the relative performance of invasive and non-invasive species is context-dependent. Invaders may allocate leaf nitrogen more efficiently to maximize photosynthesis and growth in nitrogen-poor soils, while non-invaders with more heavily defended leaves may have an advantage in drier areas. Rather than searching for a suite of traits that constitutes “invasiveness”, it may be necessary to identify potential invaders by traits that are most adaptive to the local resource context.
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References
Alpert P, Bone E, Holzapfel C (2000) Invasiveness, invasibility, and the role of environmental stress in the spread of non-native plants. Perspect Plant Eco Evol Syst 3:52–66
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
Blicker PS, Olson BE, Engel R (2002) Traits of the invasive C. maculosa and two native grasses: effect of N supply. Plant Soil 247:261–269
Blumenthal DM, Jordan NR, Russelle MP (2003) Soil carbon addition controls weeds and facilitates prairie restoration. Ecol Appl 13:605–615
Blumenthal D (2009) Carbon addition interacts with water availability to reduce invasive forb establishment in a semi-arid grassland. Biol Invasions 11:1281–1290
Brooks ML, D’Antonio CM, Richardson DM, Grace JB, Keeley JE, DiTomaso JM, Hobbs RJ, Pellant M, Pyke D (2004) Effects of invasive alien plants on fire regimes. Bioscience 54:677–688
Burke MJW, Grime JP (1996) An experimental study of plant community invasibility. Ecology 77:776–790
Burns JH (2004) A comparison of invasive and non-invasive dayflowers (Commelinaceae) across experimental nutrient and water gradients. Divers Distrib 10:387–397
Burns JH (2006) Relatedness and environment affect traits associated with invasive and noninvasive introduced Commelinaceae. Ecol Appl 16:1367–1376
Causton DR, Venus JC (1981) The biometry of plant growth. Edward Arnold, London
Corbin JD, D’Antonio CM (2004) Can carbon addition increase competitiveness of native grasses? A case study from California. Rest Ecol 12:36–43
Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Ann Rev Ecol Evol Syst 34:183–211
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534
Deng X, Ye WH, Feng HL, Yang QH, Cao HL, Hui KY, Zhang Y (2004) Gas exchange characteristics of the invasive species Mikania micrantha and its indigenous congener M. cordata (Asteraceae) in south China. Bot Bull Acad Sin 45:213–220
Durand LZ, Goldstein G (2001a) Growth, leaf characteristics, and spore production in native and invasive tree ferns in Hawaii. Am Fern J 91:25–35
Durand LZ, Goldstein G (2001b) Photosynthesis, photoinhibition and nitrogen use efficiency in native and invasive tree ferns in Hawaii. Oecologia 126:345–354
Ekramoddoullah AKM (1993) Analysis of needle proteins and N-terminal amino-acid-sequences of 2 photosystem-II proteins of western white-pine (P. monticola D. Don). Tree Physiol 12:101–106
Feng YL, Fu GL (2008) Nitrogen allocation, partitioning and use efficiency in three invasive plant species in comparison with their native congeners. Biol Invasions 10:891–902
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
Field C, Merino J, Mooney HA (1983) Compromises between water-use efficiency and nitrogen-use efficiency in five species of California evergreens. Oecologia 60:384–389
Forcella F, Wood JT, Dillon SP (1986) Characteristics distinguishing invasive weeds within Echium (bugloss). Weed Res 26:351–364
Funk JL (2008) Differences in plasticity between invasive and native plants from a low resource environment. J Ecol 96:1162–1173
Funk JL, McDaniel S (2010) Altering light availability to restore invaded forest: the predictive role of plant traits. Rest Ecol 18:865–872
Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081
Garcia-Serrano H, Escarre J, Garnier E, Sans XF (2005) A comparative growth analysis between alien invader and native senecio species with distinct distribution ranges. Ecoscience 12:35–43
Gerlach JD Jr, Rice KJ (2003) Testing life history correlates of invasiveness using congeneric plant species. Ecol Appl 13:167–179
Grotkopp E, Rejmánek M (2007) High seedling relative growth rate and specific leaf area are traits of invasive species: phylogenetically independent contrasts of woody angiosperms. Am J Bot 94:526–532
Grotkopp E, Rejmánek M, Rost TL (2002) Toward a causal explanation of plant invasiveness: seedling growth and life-history strategies of 29 pine (pinus) species. Am Nat 159:396–419
Gurevitch J, Howard TG, Ashton IW, Leger EA, Howe KM, Woo E, Lerdau M (2008) Effects of experimental manipulation of light and nutrients on establishment of seedlings of native and invasive woody species in long Island, NY forests. Biol Invasions 10:821–831
Hamilton MA, Murray BR, Cadotte MW, Hose GC, Baker AC, Harris CJ, Licari D (2005) Life-history correlates of plant invasiveness at regional and continental scales. Ecol Lett 8:1066–1074
Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15
Hikosaka K (2004) Interspecific difference in the photosynthesis-nitrogen relationship: patterns, physiological causes, and ecological importance. J Plant Res 117:481–494
Hikosaka K, Hanba YT, Hirose T, Terashima I (1998) Photosynthetic nitrogen-use efficiency in leaves of woody and herbaceous species. Func Ecol 12:896–905
Kloeppel BD, Abrams MD (1995) Ecophysiological attributes of the native Acer saccharum and the exotic Acer platanoides in urban oak forests in PA, USA. Tree Physiol 15:739–746
Leicht-Young SA, Silander JA, Latimer AM (2007) Comparative performance of invasive and native Celastrus species across environmental gradients. Oecologia 154:273–282
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
Leishman MR, Thomson VP, Cooke J (2010) Native and exotic invasive plants have fundamentally similar carbon capture strategies. J Ecol 98:28–42
Lichtenthaler HK, Wellburn A (1983) Determination of total carotenoids and chlorophyll a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592
McDowell SCL (2002) Photosynthetic characteristics of invasive and noninvasive species of Rubus (Rosaceae). Am J Bot 89:1431–1438
Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405
Muth NZ, Pigliucci M (2006) Traits of invasives reconsidered: phenotypic comparisons of introduced invasive and introduced noninvasive plant species within two closely related clades. Am J Bot 93:188–196
Niinemets U, Sack L (2006) Structural determinants of leaf light-harvesting capacity and photosynthetic potentials. Prog Bot 67:385–419
Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Func Ecol 18:419–425
Pammenter NW, Drennan PM, Smith VR (1986) Physiological and anatomical aspects of photosynthesis of 2 Agrostis species at a sub-Antarctic island. New Phytol 102:143–160
Patterson TB, Guy RD, Dang QL (1997) Whole-plant nitrogen-and water-relations traits, and their associated trade-offs, in adjacent muskeg and upland boreal spruce species. Oecologia 110:160–168
Pavlik BM (1983) Nutrient and productivity relations of the dune grasses Ammophila arenaria and Elymus mollis. Oecologia 57:227–232
Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? Biol Invasions 3:97–125
Reich PB, Walters MB, Tabone TJ (1989) Response of Ulmus americana seedlings to varying nitrogen and water status. II Water and nitrogen use efficiency in photosynthesis. Tree Physiol 5:173
Reich PB, Walters MB, Tjoelker MG, Vanderklein D, Buschena C (1998) Photosynthesis and respiration rates depend on leaf and root morphology and nitrogen concentration in nine boreal tree species differing in relative growth rate. Func Ecol 12:395–405
Rejmánek M (2000) Invasive plants: approaches and predictions. Aust Ecol 25:497–506
Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661
Ripullone F, Grassi G, Lauteri M, Borghetti M (2003) Photosynthesis-nitrogen relationships: interpretation of different patterns between Pseudotsuga menziesii and Populus x euroamericana in a mini-stand experiment. Tree Physiol 23:137
Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176
Shipley B, Vu TT (2002) Dry matter content as a measure of dry matter concentration in plants and their parts. New Phytol 153:359–364
Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ 27:1047–1054
Török K, Szili-Kovács T, Halassy M, Tóth T, Hayek Z, Paschke M, Wardell L (2000) Immobilization of soil nitrogen as a possible method for the restoration of sandy grassland. Appl Veg Sci 3:7–14
Vitousek PM, Walker LR (1989) Biological invasion by Myrica faya in Hawaii: plant demography, nitrogen-fixation, ecosystem effects. Ecol Monogr 59:247–265
Warren CR, Adams MA (2001) Distribution of N, Rubisco and photosynthesis in Pinus pinaster and acclimation to light. Plant Cell Environ 24:597–609
Warren CR, Adams MA (2002) Phosphorus affects growth and partitioning of nitrogen to Rubisco in Pinus pinaster. Tree Physiol 22:11–19
Warren CR, Adams MA (2004) Evergreen trees do not maximize instantaneous photosynthesis. Trends Plant Sci 9:270–274
Warren CR, Adams MA, Chen ZL (2000) Is photosynthesis related to concentrations of nitrogen and Rubisco in leaves of Australian native plants? Austral J Plant Physiol 27:407–416
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 Struct Func 17:359–366
Westbeek MHM, Pons TL, Cambridge ML, Atkin OK (1999) Analysis of differences in photosynthetic nitrogen use efficiency of alpine and lowland Poa species. Oecologia 120:19–26
Wilson SB, Wilson PC, Albano JA (2004) Growth and development of the native Ruellia caroliniensis and invasive Ruellia tweediana. Hort Sci 39:1015–1019
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 U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veeklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Young JA, Young CG (1992) Seeds of woody plants. Timber Press, Portland
Acknowledgments
This research was funded by a NASA Earth Systems Science fellowship to V. M. The assistance of P. Vitousek, C. Field, and T. DeHoog, and the helpful comments of two anonymous reviewers, are gratefully acknowledged.
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Matzek, V. Superior performance and nutrient-use efficiency of invasive plants over non-invasive congeners in a resource-limited environment. Biol Invasions 13, 3005–3014 (2011). https://doi.org/10.1007/s10530-011-9985-y
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DOI: https://doi.org/10.1007/s10530-011-9985-y