Skip to main content
Log in

Responses to nitrogen pulses and growth under low nitrogen availability in invasive and native tree species with differing successional status

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Invasive species are frequently found in recently disturbed sites. To examine how these disturbance-dependent invasive species exploit resource pulses resulting from disturbance, twelve physiological and morphological traits, including age-dependent responsiveness in leaf traits to nitrogen pulse, were compared between Bischofia javanica, an invasive tree species in Ogasawara islands, and three native Ogasawara species, each having a different successional status. When exposed to a nitrogen pulse, invasive B. javanica showed higher increases in photosynthetic capacity, leaf area, epidermal cell number and cell size in leaves of broad age classes, and root nitrogen absorption ability than two native mid-/late or late-successional species, but showed no particular superiority to a native pioneer species in these responses. Under low nitrogen, however, it showed the largest relative growth rate among the four species, while the native pioneer showed the lowest growth. From these results, we concluded that the combination of moderately high responsiveness to resource pulses and the ability to maintain steady growth under resource limitations may give B. javanica a competitive advantage over a series of native species with different successional status from early to late-successional stages.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

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 Ecol Evol Syst 3:52–66. doi:10.1078/1433-8319-00004

    Article  Google Scholar 

  • Bhuyan P, Khan M (2003) Tree diversity and population structure in undisturbed and human-impacted stands of tropical wet evergreen forest in Arunachal Pradesh, Eastern Himalayas, India. Biodivers Conserv 12:1735–1773. doi:10.1023/A:1023619017786

    Article  Google Scholar 

  • Burke MJ, Grime JP (1996) An experimental study of plant community invasibility. Ecology 77:776–790. doi:10.2307/2265501

    Article  Google Scholar 

  • Closset-Kopp D, Chabrerie O, Valentin B, Delachapelle H, Decocq G (2007) When Oskar meets Alice: does a lack of trade-off in r/K-strategies make Prunus serotina a successful invader of European forests? Forest Ecol Manag 247:120–130. doi:10.1016/j.foreco.2007.04.023

    Article  Google Scholar 

  • Coley PD, Kursar T (1996) Anti-herbivore defenses of young tropical leaves: physiological constraints and ecological trade-offs: In: Mulkey SS, Chazdon RL, Smith AP (eds) Tropical Forest Plant Ecophysiology. Springer, New York, pp 305–336

  • 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

    Google Scholar 

  • D’Antonio CM, Dudley TL, Mack M (1999) Disturbance and biological invasions: Direct effects and feedbacks. In: Walker LR (ed) Ecosystems of disturbed ground. Elsevier, New York, pp 413–452

    Google Scholar 

  • Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol Lett 14:419–431. doi:10.1111/j.1461-0248.2011.01596.x

    Article  PubMed  Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534. doi:10.1046/j.1365-2745.2000.00473.x

    Article  Google Scholar 

  • Denslow JS, Space JC (2009) Invasive exotic plants in the tropical Pacific Islands: patterns of diversity. Biotropica 41:162–170. doi:10.1111/j.1744-7429.2008.00469.x

    Article  Google Scholar 

  • Denslow JS, Ellison AM, Sanford RE (1998) Treefall gap size effects on above- and below- ground processes in a tropical wet forest. J Ecol 86:597–609. doi:10.1046/j.1365-2745.1998.00295.x

    Article  Google Scholar 

  • Drown DM, Levri EP, Dybdahl MF (2011) Invasive genotypes are opportunistic specialists not general purpose genotypes. Evol Appl 4:132–143. doi:10.1111/j.1752-4571.2010.00149.x

    Article  PubMed Central  Google Scholar 

  • Fricke W, Mcdonald AJS, Mattson-Djos L (1997) Why do leaves and leaf cells of N-limited barley elongate at reduced rates? Planta 202:522–530. doi:10.1007/s004250050157

    Article  CAS  Google Scholar 

  • Funk JL (2008) Differences in plasticity between invasive and native plants from a low resource environment. J Ecol 96:1162–1173. doi:10.1111/j.1365-2745.2008.01435.x

    Article  Google Scholar 

  • Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081. doi:10.1038/nature05719

    Article  CAS  PubMed  Google Scholar 

  • Gelman A, Carlin JB, Stern HS, Rubin DB (2004) Bayesian data analysis Chapman & Hall/CRC, London

  • Gibson N, Keighery G, Keighery B (2000) Threatened plant communities of the western Australia 1, the ironstone communities of the Swan and Scott Coastal Plains. J R Soc Western Aust 83:1–11

    Google Scholar 

  • Godoy O, Valladares F, Castro-Díez P (2011) Multispecies comparison reveals that invasive and native plants differ in their traits but not in their plasticity. Funct Ecol 25:1248–1259. doi:10.1111/j.1365-2435.2011.01886.x

    Article  Google Scholar 

  • Godoy O, Valladares F, Castro-Díez P (2012) The relative importance for plant invasiveness of trait means, and their plasticity and integration in a multivariate framework. New Phytol 195:912–922. doi:10.1111/j.1469-8137.2012.04205.x

    Article  PubMed  Google Scholar 

  • Granier C, Tardieu F (2009) Multi-scale phenotyping of leaf expansion in response to environmental changes: the whole is more than the sum of parts. Plant Cell Env 32:1175–1184. doi: 10.1111/j.1365-3040.2009.01955.x

  • Hanba YT, Kogami H, Terashima I (2002) The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand. Plant Cell Env 25:1021–1030

    Google Scholar 

  • Hata K, Suzuki JI, Kachi N, Yamamura Y (2006) A 19-year study of the dynamics of an Invasive Alien Tree, Bischofia javanica, on a Subtropical Oceanic Island 1. Pac Sci 60:455–470. doi:10.1353/psc 2006.0029

    Article  Google Scholar 

  • 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. doi:10.1111/j.0022-0477.2004.00953.x

    Article  Google Scholar 

  • Hunt R (1982) Plant growth analysis. The Lavenham Press Limited, Suffolk

    Google Scholar 

  • Jurik TW, Chabot JF, Chabot BF (1979) Ontogeny of photosynthetic performance in Fragaria virginiana under changing light regimes. Plant Physiol 63:542–547. doi:10.1104/pp.63.3.542

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kamaluddin M, Grace J (1992) Photoinhibition and light acclimation in seedlings of Bischofia javanica, a tropical forest tree from Asia. Annal Bot 69:47–52

    Google Scholar 

  • Kamo K (2003) Bichofia javanica in Mt Kinabalu, Malaysia. Trop For 58:17–24 (in Japanese)

    Google Scholar 

  • Kitayama K, Mueller-Dombois D (1995) Biological invasion on an oceanic island mountain: Do alien plant species have wider ecological ranges than native species? J Veg Sci 6:667–674. doi:10.2307/3236436

    Article  Google Scholar 

  • Kobayashi S (1978) A list of the vascular plants occuring in the Ogasawara (Bonin) Islands. Ogasawara Res 1:1–33

    Google Scholar 

  • Kueffer C, Kronauer L, Edwards PJ (2009) Wider spectrum of fruit traits in invasive than native floras may increase the vulnerability of oceanic islands to plant invasions. Oikos 118:1327–1334. doi:10.1111/j.1600-0706.2009.17185.x

    Article  CAS  Google Scholar 

  • Leishman MR, Thomson VP (2005) Experimental evidence for the effects of additional water, nutrients and physical disturbance on invasive plants in low fertility Hawkesbury Sandstone soils, Sydney, Australia. J Ecol 93:38–49. doi:10.1111/j.1365-2745.2004.00938.x

    Article  Google Scholar 

  • Lemmens RHMJ, Soerianegara I, Wong WC (1995) Timber trees: minor commercial timbers: plant resources of south-east Asia. Backhuys Publishers, Leiden, pp 324–325

    Google Scholar 

  • Naidu SL, DeLucia EH (1997) Growth, allocation and water relations of shade-grown Quercus rubra L. saplings exposed to a late-season canopy gap. Annal Bot 80:335–344. doi:10.1023/A:1009780114992

    Article  Google Scholar 

  • Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy?. Plant Cell Env 26:505–512

    Google Scholar 

  • Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant Cell Env 28:916–927. doi:10.1111/j.1365-3040.2005.01344.x-&gt

    Article  Google Scholar 

  • Oguchi R, Hikosaka K, Hiura T, Hirose T (2006) Leaf anatomy and light acclimation in woody seedlings after gap formation in a cool-temperate deciduous forest. Oecologia 149:571–582. doi:10.1007/s00442-006-0485-1

    Article  CAS  PubMed  Google Scholar 

  • Ono K, Watanabe A (1997) Levels of endogenous sugars, transcripts of rbcS and rbcL, and of RuBisCO protein in senescing sunflower leaves. Plant Cell Physiol 38:1032–1038

    Article  CAS  Google Scholar 

  • Palacio-López K, Gianoli E (2011) Invasive plants do not display greater phenotypic plasticity than their native or non-invasive counterparts: a meta-analysis. Oikos 120:1393–1401. doi:10.1111/j.1600-0706.2010.19114.x

    Article  Google Scholar 

  • Paquette A, Fontaine B, Berninger F, Dubois K, Lechowicz MJ, Messier C, Posada JM, Valladares F, Brisson J (2012) Norway maple displays greater seasonal growth and phenotypic plasticity to light than native sugar maple. Tree Physiol 32:1339–1347. doi:10.1093/treephys/tps092

    Article  CAS  PubMed  Google Scholar 

  • Parsons WFJ, Knight DH, Miller SL (1994) Root gap dynamics in lodgepole pine forest: nitrogen transformations in gaps of different size. Ecol Appl 4:354–362. doi:10.2307/1941939

    Article  Google Scholar 

  • Pattison RR, Goldstein G, Ares A (1998) Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. Oecologia 117:449–459. doi:10.1007/s004420050680

    Article  Google Scholar 

  • Pearcy RW, Sims DA (1994) Photosynthetic acclimation to changing light environments: scaling from the leaf to the whole plant. In: Caldwell MM, Pearcy RW (eds) Exploitation of environmental heterogeneity by plants: ecophysiological processes above and below ground. Academic Press, San Diego, pp 145–174

    Chapter  Google Scholar 

  • Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486. doi:10.1111/j.1365-2745.2008.01435.x

    Article  PubMed  Google Scholar 

  • Poorter L (1999) Growth responses of 15 rain-forest tree species to a light gradient: the relative importance of morphological and physiological traits. Funct Ecol 13:396–410. doi:10.1046/j.1365-2435.1999.00332.x

    Article  Google Scholar 

  • Poorter L, van de Plassche M, Willems S, Boot RGA (2004) Leaf traits and herbivory rates of tropical tree species differing in successional status. Plant Biol 6:746–754. doi:10.1055/s-2004-821269

    Article  CAS  PubMed  Google Scholar 

  • Reich PB, Tjoelker MG, Walters MB, Vanderklein DW, Buschena C (1998) Close association of RGR, leaf and root morphology, seed mass and shade tolerance in seedlings of nine boreal tree species grown in high and low light. Funct Ecol 12:327–338. doi:10.1046/j.1365-2435.1998.00208.x

    Article  Google Scholar 

  • Reich PB, Ellsworth D, Walters M, Vose J, Gresham C, Volin J, Bowman W (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969. doi:10.1890/0012-9658(1999)080

    Article  Google Scholar 

  • Rejmánek M (1989) Invasibility of plant communities. In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmanek M, Williamson M (eds) Biological invasions: a global perspective. John Wiley, New York, pp 369–388

    Google Scholar 

  • Rejmánek M, Richardson DM, Pysek P (2005) Plant invasions and invasibility of plant communities, In: van der Maarel (ed) Vegetation ecology. Blackwell Publishing, Oxford, pp 332–355

  • Roggatz U, Donald AJSMC, Stadenberg I, Schurr U (1999) Effects of nitrogen deprivation on cell division and expansion in leaves of Ricinus communis L. Plant Cell Env 22:81–89. doi:10.1046/j.1365-3040.1999.00383.x

    Article  Google Scholar 

  • Sakai AK, Wagner WL, Mehrhoff LA (2002) Patterns of endangerment in the Hawaiian flora. Syst Biol 51:276–302. doi:10.1080/10635150252899770

    Article  PubMed  Google Scholar 

  • Sanford NL, Harrington RA, Fownes JH (2003) Survival and growth of native and alien woody seedlings in open and understory environments. For Ecol Manag 183:377–385. doi:10.1016/S0378-1127(03)00141-5

    Article  Google Scholar 

  • Scharenbroch BC, Bockheim JG (2007) Impacts of forest gaps on soil properties and processes in old growth northern hardwood-hemlock forests. Plant Soil 294:219–233. doi:10.1007/s11104-007-9248-y

    Article  CAS  Google Scholar 

  • Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annu Rev Ecol Syst 17:667–693

    Article  Google Scholar 

  • Schumacher E, Kueffer C, Edwards PJ, Dietz H (2008) Influence of drought and shade on seedling growth of native and invasive trees in the Seychelles. Biotropica 40:543–549. doi:10.1111/j.1744-7429.2008.00407.x

    Article  Google Scholar 

  • Schumacher E, Kueffer C, Edwards PJ, Dietz H (2009) Influence of light and nutrient conditions on seedling growth of native and invasive trees in the Seychelles. Biol Invasions 11:1941–1954. doi:10.1007/s10530-008-9371-6

    Article  Google Scholar 

  • Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176. doi:10.1016/S0169-5347(02)02495-3

    Article  Google Scholar 

  • Shimizu Y (1988) Vegetation of Mt. Kuwanoki in the Bonin (Ogasawara) Islands with reference to the invasion of an introduced tree species Bischofia javanica. Regional Views 1:31–46 (in Japanese)

    Google Scholar 

  • Shimizu Y, Tabata H (1991) Forest structure, composition and distribution on a Pacific island with reference to ecological release and speciation. Pac Sci 45:28–49

    Google Scholar 

  • Sims DA, Pearcy RW (1992) Response of leaf anatomy and photosynthetic capacity in Alocasia macrorrhiza (Araceae) to a transfer from low to high light. Am J Bot 79:449–455

    Article  Google Scholar 

  • Sugiyama S (2005) Developmental basis of interspecific differences in leaf size and specific leaf area among C3 grass species. Funct Ecol 19(916):924. doi:10.1111/j.1365-2435.2005.01044.x

    Google Scholar 

  • Sultan SE (2001) Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. Ecology 82:28–343. doi:10.1111/j.1399-3054.1982.tb00282.x

    Google Scholar 

  • Tanimoto T, Toyoda T (1996) Survivorship and growth of Akagi (Bischofia javanica BI) seedlings under the forest canopy and different temperature conditions. Bull For For Prod Res Inst 370:1–19 (in Japanese with English summary)

    Google Scholar 

  • Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Natl Acad Sci USA 101:10854–10861. doi:10.1073/pnas.0403458101

    Article  CAS  PubMed  Google Scholar 

  • Toyoda T. (2003) Flora of Bonin Islands (Enlarged & Revised). Aboc, Kanagawa

  • Trapani N, Hall AJ, Weber M (1999) Effects of constant and variable nitrogen supply on sunflower (Helianthus annuus L.) leaf cell number and size. Ann Bot 84:599–606. doi:10.1006/anbo 1999.0954

    Article  CAS  Google Scholar 

  • Turnbull MH, Doley D, Yates DJ (1993) The dynamics of photosynthetic acclimation to changes in light quantity and quality in three Australian rainforest tree species. Oecologia 94:218–228. doi:10.1007/BF00341320

    Article  Google Scholar 

  • van Staden J, Carmi A (1982) The effects of decapitation on the distribution of cytokinins and growth of Phaseolus vulgaris plants. Physiol Plantarum 55:39–44. doi:10.1111/j.1399-3054.1982.tb00282.x

    Article  Google Scholar 

  • Yamashita N, Koike N, Ishida A (2002) Leaf ontogenetic dependence of light acclimation in invasive and native subtropical trees of different successional status. Plant Cell Env 25:1341–1356. doi:10.1046/j.1365-3040.2002.00907.x

    Article  Google Scholar 

  • Yamashita N, Tanaka N, Hoshi Y, Kushima H, Kamo K (2003) Seed and seedling demography of invasive and native trees of subtropical Pacific islands. J Veg Sci 14:15–24. doi:10.1111/j.1654-1103.2003.tb02123.x

    Article  Google Scholar 

Download references

Acknowledgments

We thank Naoko Yamashita and Shuichi Sugiyama for helpful advice in the analysis and collection of data, and Kouki Hikosaka for valuable comments of earlier version of this manuscript. Two anonymous reviewers provided insightful comments on the manuscript. This work was supported by Grant-in-aid of the Japan Ministry of Education, Science and Culture [18770022, 24370009] and by grant-in-aid from Fujiwara Natural History foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yoko Osone.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Osone, Y., Yazaki, K., Masaki, T. et al. Responses to nitrogen pulses and growth under low nitrogen availability in invasive and native tree species with differing successional status. J Plant Res 127, 315–328 (2014). https://doi.org/10.1007/s10265-013-0609-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-013-0609-8

Keywords

Navigation