CSIRO PUBLISHING

www.publish.csiro.au/journals/fpb Functional Plant Biology, 2005, 32, 933–944

Phenotypic plasticity of an invasive acacia versus two nativeMediterranean species

Ralf PeperkornA,B, Christiane WernerA and Wolfram BeyschlagA

ADepartment of Experimental and Systems Ecology, Universitatsstrasse 25, D-33615 Bielefeld, Germany.BCorresponding author. Email: ralf.peperkorn@uni-bielefeld.de

Abstract. The phenotypic plasticity and the competitive ability of the invasive Acacia longifolia v. the indigenousMediterranean dune species Halimium halimifolium and Pinus pinea were evaluated. In particular, we explored thehypothesis that phenotypic plasticity in response to biotic and abiotic factors explains the observed differences incompetitiveness between invasive and native species. The seedlings’ ability to exploit different resource availabilitieswas examined in a two factorial experimental design of light and nutrient treatments by analysing 20 physiologicaland morphological traits. Competitiveness was tested using an additive experimental design in combination with15N-labelling experiments. Light and nutrient availability had only minor effects on most physiological traits anddifferences between species were not significant. Plasticity in response to changes in resource availability occurred inmorphological and allocation traits, revealing A. longifolia to be a species of intermediate responsiveness. The majorcompetitive advantage of A. longifolia was its constitutively high shoot elongation rate at most resource treatmentsand its effective nutrient acquisition. Further, A. longifolia was found to be highly tolerant against competitionfrom native species. In contrast to common expectations, the competition experiment indicated that A. longifoliaexpressed a constant allocation pattern and a phenotypic plasticity similar to that of the native species.

Keywords: Acacia longifolia, competition, Halimium halimifolium, light and nutrient availability, physiological andmorphological traits, Pinus pinea, resource use.

Introduction

Acacia species were introduced into costal dune systemsin Portugal during the middle of the 20th century with theobjective of stabilising the dunes along roads, to prevent sanderosion or just for ornamental purposes. These sand dunesare habitats of great interest for nature conservation and beara very characteristic and rich flora. There is a high diversityof evergreen and semi-deciduous woody and herbal speciesas well as of numerous mosses and lichens. Characteristichigher plant species are for example Pinus pinea, Coremaalbum, Helicrysum virescens, Cistus salvifolius, Halimiumhalimifolium, Scrophularia frutescens and Armeria pungens.

However, some decades after planting, the introducedacacia species became dominant and extensively invadedthese dune ecosystems in some areas of the Portuguesecoastline. This invasion has caused serious ecologicalproblems, negatively affecting native species (Marchanteet al. 2003), resulting in the possible extinction of native

Abbreviations used: Aarea, net photosynthetic rate per area; Amass, net photosynthetic rate per mass; Fv / Fm, maximal photochemical efficiency ofPSII; �F / Fm, effective quantum yield of PSII; LAR, leaf area ratio; LMR, leaf mass ratio; MPP, mean phenotypic plasticity; PI, plasticity index;RMR, root mass ratio; SER, shoot elongation rate; SLA, specific leaf area; SMR, stem mass ratio; WUE, water-use efficiency.

species through rampant growth and / or indirect effects andthus, lowering biodiversity (Marchante et al. 2003). Furtherconsequences can be the alteration of coastal sedimentmovement patterns, changes in fire regime, alteration of soilcomposition and changes in plant and animal communitiesas shown in other coastal environments (Van Wilgen et al.1997). Since invasive species endanger native plant habitatsworld wide, one of the most crucial research questions is theunderstanding of the traits of alien species that are responsiblefor their competitiveness (see Mooney 1999 and literaturecited therein).

Enhanced phenotypic plasticity has been hypothesised toallow species to become invasive and to successfully colonisenew habitats (Durand and Goldstein 2001; Yamashitaet al. 2002), for example, by showing a high degree ofmorphological and physiological acclimation after beingtransferred into a new light regime (Yamashita et al. 2002;Niinemets et al. 2003). In general, it has been suggested

© CSIRO 2005 10.1071/FP04197 1445-4408/05/100933

934 Functional Plant Biology R. Peperkorn et al.

that enhanced phenotypic plasticity may be one of themost important traits of successful invaders (Bloom 1985;Poorter and Lambers 1986; Aerts et al. 1991; Williams et al.1995; Aerts 1999; Sultan 2000, 2001; Dietz and Steinlein2004 and references therein). Furthermore, high resource-use efficiency (e.g. light, nutrient, water, space) has beenshown to enable species to become invasive (Davis et al.2000; Huxman and Smith 2001).

In general, understanding the patterns of plant resourceacquisition (in particular for nutrients and light) is crucialfor the interpretation of competitive ability and invasivenessof a particular plant species. Especially in Mediterranean-type ecosystems, tolerance of high light intensities isan important constraint for plants to survive (Valladaresand Pugnaire 1999). This tolerance is not only importantfor habitats with excessive irradiance but is also neededunder shade conditions due to the appearance of numeroussunflecks with rather high irradiance levels (Pearcy 1994),especially for seedlings in the understorey. Nutrient-poorsoils, like Mediterranean sand dunes, impose limitationson plant growth and development, as indicated by studiesof plant responses to nutrient additions (Ingestad 1982;Kruger 1987; Witkowski et al. 1990), litter decompositionprocesses (Mitchell et al. 1986), and N allocation patterns(Stock et al. 1987). To cope with such limitations,plants exhibit traits that allow them to survive underthese adverse conditions, for example high allocation toroots, low allocation to stems, nutrient conservation vialow tissue N content and / or long-lived leaves (Smithet al. 1999).

Additional nitrogen input can severely alter theenvironmental conditions of ecosystems. Witkowski (1991)found that the N status of the Cape Fynbos ecosystemsin south-west Africa has increased through the invasion ofalien acacias. This is because the acacias produce largeamounts of litter containing about three times more nitrogenthan the litter of the native species. Therefore, one of theeffects of the invasion of nitrogen-fixing acacia species inMediterranean dune systems may be the alteration of thenutrient availability (as has been found at the Portuguesesite, Marchante 2001), with positive or negative effects onthe life history of the existing native species. Addition ofN to an ecosystem typically changes species composition(Tilman 1988), decreases diversity (Aerts and Berendse1988; Bobbink et al. 1988; Huenneke et al. 1990), andenhances replacement of native species by non-native species(Thurston 1969; Bobbink et al. 1988; Huenneke et al. 1990).In environments altered by introduced nitrogen-fixing plants,persistence of plant species requires traits different fromthose required in natural, less productive environments.Hence, species exhibiting a high plastic response to thealtered environment benefit from the new circumstancesand are, therefore, able to dominate the habitat. Rhizobiawould enhance N availability solely for acacia plants and

we intended to evaluate the competitive strength under equalexperimental conditions.

This study examined seedling ability to exploitdifferent resource availabilities in an experimentaldesign of light and nutrient treatments and competition.We evaluated the competitive ability of the invasiveA. longifolia compared to the indigenous speciesH. halimifolium and P. pinea by exploring 20 physiologicaland morphological traits. In particular, we tested thehypothesis that the differences in phenotypic plasticity(calculated according to Valladares et al. 2000a) ofphysiological, morphological and allocation traits explainthe differences in competitiveness between invasive andnative species.

Materials and methodsPlant material and experimental design

Seeds of the invasive Acacia longifolia (Andr.) Willd.(Mimosaceae) and two native Mediterranean plant species[Halimium halimifolium (L.) Willk. (Cistaceae) and Pinus pinea L.(Pinaceae)] growing in direct competition with A. longifoliaat the field side, were collected in September 2001at the peninsula Troia, 70 km south of Lisbon, Portugal. Seedswere germinated in Petri dishes and planted in washed river sand into2.4-L tubes (30 cm height) and 6.65-L tubes (70 cm height) in theplasticity experiment and the competition experiment, respectively.Plants were not inoculated with rhizobia, to ensure the same nitrogenavailability for all species. Plants were grown in the greenhouse ofthe University of Bielefeld, Germany, under semi-controlled long day(12-h day / night cycle) conditions (± 25◦C and ± 15◦C day and nighttemperature, respectively).

Plasticity experiment

For this experiment five plants of each species were used foreach treatment. A two-factorial experimental design of four levelsof nutrient and two light treatments was used to explore the effectson several morphological and physiological variables. Plants ofthe shade treatment were covered by a neutral density shadecloth and fertilised with 50 mL of three-quarter-strength modifiedHoagland solution (see below). Photon flux densities (PFD) weremaximum 250 µmol m−2 s−1 in shade and daylight (up to a total of1400 µmol m−2 s−1) plus additional 300 µmol m−2 s−1 under high-lightconditions. Under the high-light regime four nutrient levels wereapplied by weekly fertilisation with 50 mL of one-eighth, three-quarters, 1- or 2-fold modified Hoagland solutions. 1-fold modifiedHoagland solution consisted of 7.5 mM NH4

+, 7.35 mM NO3−,

1.0 mM H2PO4−, 5.95 mM K+, 2.45 mM Ca2+, 2.0 mM Mg2+, 5.0 mM

Fe3+, 5.75 mM SO42−, 2.5 mM Cl− plus micronutrients. Plants were

harvested after cultivation for seven months (from 10 February to5 September).

Competition experiment

This experiment took place under high-light conditions as describedabove. Plants of the three species were planted in an additive designwhere a single plant individual served as control. There were intra-and interspecific competition treatments (i.e. acacia v. one nativespecies) always consisting of two plant individuals, with 7–10 replicates.Plants were fertilised weekly with 100 mL of a 1-fold modifiedHoagland solution. The experiment lasted 7 months (3 March to6 October 2003).

Phenotypic plasticity of an invasive acacia Functional Plant Biology 935

Morphological and allocation measurements and nutrient analysis

Throughout the plasticity experiment plant height was recorded atregular intervals. At the end of the experiment all plants were harvestedand divided into leaves, stems and roots. In the case of A. longifoliaphyllodes (petioles metamorphosis) and in the case of P. pinea needleswere measured instead of leaves. Leaf fresh weight was determinedimmediately. Leaf area was measured with a Delta-T Image AnalysisSystem (Delta-T Devices Ltd, Cambridge, UK). Roots were cut intosmall pieces, mixed up and a representative subset was scannedto measure root length and root area with root-analysis software(Win / MacRHIZO 2002, Regent Instruments Inc., Quebec, Canada).Total plant root length and total root area were estimated from the dryweight of the subset and total biomass (method modified from Boumaet al. 2001). Leaves (phyllodes, needles), stems and roots were driedat 70◦C for 48 h and finely ground with a ball mill (model MM-2000,Retsch GmbH & Co. KG, Haan, Germany). The C / N ratio and totalleaf N content of this material was then determined in a CNS-analyser(Vario El, Elementar, Germany). Leaf area and dry weights were usedto calculate the following parameters: specific leaf area (SLA; leaf areaper unit dry weight), leaf area ratio (LAR; total leaf area per total plantdry weight), leaf mass ratio (LMR, leaf mass per total plant mass),stem mass ratio (SMR; stem mass per total plant mass), root mass ratio(RMR; root mass per total plant mass) and root / shoot ratio (root drymass per shoot dry mass). The stem elongation rate (SER, mm week−1)was calculated from the increase in plant height, estimated as the slopeof the growing curve.

Short-term 15 N labelling

Plants of the competition experiment were traced 48 h beforeharvest with 10 mL of a 15N-labelled solution [12.62 µmol L−1

15NH4+ (95% enriched), 6.31 µmol L−1 SO4

−, 22.64 µmol L−1 15NO3−

(99% enriched, 22.64 µmol L−1 K+) in proportion 1 : 1 (both fromChemotrade, Leipzig, Germany)]. The solution was applied at 5 cmsoil depth at the centre of the pot with a syringe. Harvest plants weretreated like plants from the plasticity experiment. 14N / 15N isotope ratiosof dried roots were measured using a continuous flow–isotope massspectrometer (IsoPrime GV Instruments, Manchester, UK) coupled withan Elementar Analyser (Vario EL, Elementar Analysensysteme GmbH,Hanau, Germany). The standard deviation of repeated-measurementswas less than ± 0.2‰.

Gas-exchange measurements

Gas-exchange measurements of one fully expanded, intact leaf of 3–5plants of A. longifolia and H. halimifolium were made with a CompactMinicuvette System (Walz, Effeltrich, Germany). Measurements onP. pinea were not possible since needles were too small to beinserted into the leaf cuvette of the gas-exchange system. Maximalphotosynthetic rates at ambient (350 µmol mol−1) and elevated CO2

(>2000 µmol mol−1) was determined. Different PFD was suppliedby a halogen lamp (FL-400, Walz) with neutral density grey filters.Temperature inside the cuvette was kept constant at 25◦C andrelative humidity was set to 65%. From these gas-exchange data thefollowing parameters were estimated: photosynthetic rate on area basis(Aarea) and on dry weight basis (Amass), maximum photosyntheticrate (Amax) at ambient and elevated CO2, light-use efficiency, darkrespiration, compensation point, water-use efficiency calculated as netphotosynthesis per transpiration (WUE). Photosynthesis measurementswere always carried out on leaves of the same ontogenic status,since ontogenic status can influence the capacity for photosyntheticacclimation (e.g. Frak et al. 2001).

Chlorophyll fluorescence measurements

Chlorophyll a fluorescence of five plants per species and treatmentwere measured with a portable fluorometer PAM-2000 (Walz) with

leaf clip holder (model 2030-B). Light-response curves were measuredwith a halogen lamp (model 2050-HB). Maximal (Fm) and minimalfluorescence (F0) were measured to calculate maximal photochemicalefficiency of PSII (Fv / Fm) after 20 min dark adaptation with leafclips. Effective quantum yield of PSII (�F / Fm

′) was determined at400 µmol m−2 s−1 and 1500 µmol m−2 s−1.

Phenotypic plasticity index

Following Valladares et al. (2000a), an index of phenotypic plasticity(PPI) ranging from 0 to 1 was calculated for each variable and speciesof both experiments. The phenotypic plasticity index has the advantagethat variables with different units and contrasting variation rangescan be compared (Valladares et al. 2000b). PPI was calculated foreach parameter as the difference between the highest and lowestmean values of all treatments divided by the maximum mean value.Mean phenotypic plasticity (MPP) of each species was averagedfrom phenotypic plasticity indices of up to 20 traits, and meanphenotypic plasticity of three trait groups (physiology, morphologyand allocation) in response to abiotic and competitive interactionswas calculated.

Statistics

One-way analysis of variance (ANOVA, l.s.d. test, STATISTICA,StatSoft, Inc. 1995, Tulsa, USA) was used to test for differences amongspecies and nutrient treatments. A t-test for independent samples wasused to test for differences among PFD treatments. In cases where datadid not meet the assumptions of normality, they were transformed bylog or square-root functions.

Results

The plasticity experiment: response to abiotic factors

The clearest differences between the invasive andnative species were found for the shoot elongationrates under different abiotic conditions (Fig. 1). The invasivespecies A. longifolia exhibited a higher growth (shootelongation rate, mm week−1) at all but the highest nutrienttreatment where H. halimifolium exhibited similar rates. Withfull-strength Hoagland solution (1 N, Fig. 1) growth of acaciawas up to three times higher than that of H. halimifoliumand more then ten times higher than that of P. pinea. WhileP. pinea showed no shoot elongation response to increasingN availability at all, a linear increase was observed forA. longifolia and H. halimifolium. Light availability had nosignificant effect on growth of A. longifolia while shadeincreased shoot elongation rate of the native P. pinea.

Specific leaf area (SLA) and leaf area ratio (LAR)exhibited significant differences between treatments andspecies with A. longifolia being within the range of theindigenous H. halimifolium and P. pinea (Table 1). Underhigh light conditions all species exhibited a decrease inSLA and LAR relative to shade conditions by ∼50% and75%, respectively (Table 1, compare + 3 / 4 and – 3 / 4).Increasing nitrogen availability had no effect on SLA andLAR of A. longifolia, whereas both increased in P. pinea.H. halimifolium exhibited an increase in SLA with increasingnitrogen. The pattern of biomass allocation to leaves, stemsand roots (LMR, SMR and RMR mass ratio, respectively)was not significantly different between invasive and native

936 Functional Plant Biology R. Peperkorn et al.

0

5

10

15

20

25

30

1/8

N

3/4

N

1 N

2 N

3/4

N

1/8

N

3/4

N

1 N

2 N

3/4

N

1/8

N

3/4

N

1 N

2 N

3/4

N

Gro

wth

(sh

oot e

long

atio

n, m

m w

eek–

1 )

H. halimifolium P. pineaA. longifolia

Light treatment

Shade treatment

aA

abA

bA

bA

A

aB

bB

bB

cA

BabA

bC bBaB

*B

Fig. 1. Growth (shoot elongation rate; mm week−1) calculated from the increase in stem length over timeof the invasive and native species grown at different nutrient concentrations (1 / 8 N, 3 / 4 N, 1 N, 2-fold N;see material and methods) and two light levels; lower and upper case letters indicate significant differencesbetween nutrient treatments and species, respectively, (ANOVA; P<0.05), * indicates significant differencesbetween shade and high light treatments (t-test; P<0.05), mean + SE (n = 5).

species. A. longifolia responded to a small increase innitrogen by changes in allocation pattern, while a furtherincrease did not have an additional effect. Higher PFDincreased allocation to roots and decreased SMR. Theallocation pattern of H. halimifolium was comparable toA. longifolia, whereas P. pinea responded only at the highestnitrogen treatment with changes in LMR and RMR. Incontrast to A. longifolia, the native species exhibited asignificant decrease in root / shoot ratio with increasingnutrient availability. High light led to an increase in root /shoot ratio and root length of all species. Total root length ofP. pinea was unaffected by the nutrient treatments, whereasH. halimifolium and A. longifolia exhibited an increasein root length. While the leaf, stem and total biomass ofP. pinea and additionally root biomass of H. halimifoliumsignificantly increased with increasing nitrogen availability,A. longifolia exhibited saturation of biomass productionat high nitrogen availability. Higher PFD significantlyincreased biomass of A. longifolia and P. pinea. In general,A. longifolia produced similar or even higher biomass than thetwo native species.

Chlorophyll fluorescence

There were no significant effects of nitrogentreatments on effective quantum yield of PSII (�F / Fm

′)measured at growth and high light conditions (400 and1500 µmol m−2 s−1, respectively) and light-use efficiency(Table 2). Light-use efficiency of all did not differ amongspecies. Fv / Fm significantly increased with increasing

nitrogen treatment in A. longifolia, while P. pineaand H. halimifolium were unaffected. PFD treatmentdid not have an effect on any fluorescence parameterof H. halimifolium. Fv / Fm increased under shadeconditions in A. longifolia and P. pinea. Values ofA. longifolia were within the range of the native speciesbut were lower than optimum (0.84, see Bjorkman andDemmig 1987). With increasing light �F / Fm

′ measuredat high light decreased in A. longifolia while in P. pinea�F / Fm

′ at growth light and light-use efficiency decreased.Fluorescence values of A. longifolia were within therange of the native species.

Leaf gas exchange

Photosynthetic rates (Aarea, Amass), photosyntheticcapacity (at saturating CO2 and PFD, Amax) and the lightcompensation point were significantly increased by nitrogentreatments in A. longifolia (Table 2), but no effect was foundin H. halimifolium. Aarea, Amass and Amax of A. longifolia weresignificantly lower compared with the native H. halimifolium,while the other variables did not differ. Shade treatmentincreased Amass and water-use efficiency (WUE) of bothA. longifolia and H. halimifolium, reflecting changes inbiomass allocation. H. halimifolium reached significantlyhigher Amass (368 µmol kg−1 s−1) values as A. longifolia.All gas-exchange parameters showed a high variability, andsignificant differences were difficult to track within theavailable number of replicates (n = 2–5).

Phenotypic plasticity of an invasive acacia Functional Plant Biology 937

Table 1. Morphological and allocation responses to abiotic factorsMean values (± standard deviation) of morphological and allocation traits of all species and treatments (light and nutrient); N = nitrogen,L = high (+) / low (–) light; lower and upper case superscript letters indicate significant differences between nitrogen treatments and species,respectively, (ANOVA, P<0.05; n = 5) and ∗ indicates differences between light treatments at „ N (t-test, P<0.05; n = 5), abbreviations see

Materials and methods

Traits L N Acacia longifolia Halimium halimifolium Pinus pinea

SLA (m2 kg−1) + ‘ 10.62 ± 1.06aA 19.84 ± 14.92aA 7.49 ± 0.78aA

+ „ 9.29 ± 0.66aA 11.61 ± 0.38aB 8.02 ± 1.06abC

+ 1 9.94 ± 0.72aA 12.97 ± 1.59aB 9.71 ± 1.30cA

+ 2 10.38 ± 0.72aA 13.43 ± 1.64aB 9.09 ± 0.46bcA

– „ 22.45 ± 2.73A∗ 29.68 ± 4.11B∗ 18.37 ± 2.30C∗

LAR (cm2 g−1) + ‘ 45.64 ± 14.08aA 85.57 ± 3.31aA 29.96 ± 3.77aA

+ „ 50.60 ± 4.22aA 59.90 ± 5.48bB 30.38 ± 4.81aC

+ 1 54.50 ± 5.99aA 77.78 ± 9.25cB 40.19 ± 8.65bC

+ 2 58.13 ± 4.41aA 76.70 ± 11.26cB 45.59 ± 1.96bC

– „ 129.70 ± 22.63A∗ 178.28 ± 10.51B∗ 98.17 ± 17.36C∗

LMR (g g−1) + ‘ 0.43 ± 0.13aA 0.38 ± 0.08aA 0.40 ± 0.02aA

+ „ 0.55 ± 0.02bA 0.54 ± 0.02bA 0.38 ± 0.02aB

+ 1 0.55 ± 0.03bA 0.60 ± 0.03bA 0.41 ± 0.04aB

+ 2 0.56 ± 0.05bA 0.57 ± 0.05bA 0.50 ± 0.02bB

– „ 0.58 ± 0.08A 0.60 ± 0.05A 0.53 ± 0.04A∗

SMR (g g−1) + ‘ 0.11 ± 0.03aA 0.21 ± 0.05aB 0.15 ± 0.03aA

+ „ 0.16 ± 0.02bA 0.14 ± 0.02bA 0.14 ± 0.02aA

+ 1 0.16 ± 0.03bA 0.18 ± 0.01abB 0.14 ± 0.01aA

+ 2 0.14 ± 0.03abA 0.20 ± 0.04aB 0.16 ± 0.04aAB

– „ 0.26 ± 0.07A∗ 0.28 ± 0.07A∗ 0.21 ± 0.04A∗

RMR (g g−1) + ‘ 0.45 ± 0.14aA 0.35 ± 0.14aA 0.41 ± 0.04aA

+ „ 0.29 ± 0.02bA 0.25 ± 0.02aB 0.44 ± 0.03aC

+ 1 0.28 ± 0.03bA 0.19 ± 0.03aB 0.43 ± 0.04aC

+ 2 0.28 ± 0.02bA 0.20 ± 0.02aB 0.33 ± 0.04bA

– „ 0.16 ± 0.02A∗ 0.08 ± 0.02B∗ 0.25 ± 0.05C∗

Root / shoot (g g−1) + ‘ 0.66 ± 0.16aA 0.62 ± 0.51aA 0.69 ± 0.11aA

+ „ 0.41 ± 0.05bA 0.33 ± 0.02bA 0.80 ± 0.08aB

+ 1 0.40 ± 0.06bA 0.23 ± 0.05cB 0.77 ± 0.12aC

+ 2 0.39 ± 0.07bA 0.25 ± 0.02bcB 0.49 ± 0.08bC

– „ 0.19 ± 0.02A∗ 0.09 ± 0.03A∗ 0.34 ± 0.10B∗

Leaf (g DW) + ‘ 0.38 ± 0.27aA 0.01 ± 0.003aB 1.31 ± 0.19aC

+ „ 1.92 ± 0.47bA 1.00 ± 0.40bB 1.56 ± 0.19abAB

+ 1 3.07 ± 0.93cA 1.74 ± 0.36cB 1.72 ± 0.21bB

+ 2 3.73 ± 0.54cA 3.72 ± 0.24dAB 2.66 ± 0.22cB

– „ 0.70 ± 0.24A∗ 0.26 ± 0.17B 0.57 ± 0.09AB∗

Stem (g DW) + ‘ 0.10 ± 0.08aA 0.003 ± 0.002aB 0.48 ± 0.05aC

+ „ 0.56 ± 0.11bA 0.26 ± 0.15bB 0.58 ± 0.14aA

+ 1 0.96 ± 0.46cA 0.52 ± 0.13cA 0.59 ± 0.11aA

+ 2 0.97 ± 0.30cA 1.16 ± 0.17dA 0.87 ± 0.19bA

– „ 0.33 ± 0.17A∗ 0.13 ± 0.12A 0.23 ± 0.06A∗

Root (g DW) + ‘ 0.41 ± 0.23aA 0.005 ± 0.002aB 1.35 ± 0.35aC

+ „ 1.04 ± 0.33bA 0.47 ± 0.23bB 1.84 ± 0.32aC

+ 1 1.64 ± 0.73cA 0.54 ± 0.16bB 1.85 ± 0.46aA

+ 2 1.88 ± 0.38cA 1.17 ± 0.44cB 1.74 ± 0.14aA

– „ 0.20 ± 0.09A∗ 0.03 ± 0.02B 0.26 ± 0.03A∗

Total biomass (g DW) + ‘ 0.90 ± 0.53aA 0.02 ± 0.01aB 3.29 ± 0.56aC

+ „ 3.53 ± 0.87bA 1.89 ± 0.86bB 4.13 ± 0.61bA

+ 1 5.70 ± 2.09cA 2.92 ± 0.67bB 4.23 ± 0.71bAB

+ 2 6.67 ± 1.06cA 5.74 ± 0.99cA 5.29 ± 0.30cA

– „ 1.23 ± 0.47A∗ 0.44 ± 0.31B 1.07 ± 0.12A∗

Total root length (m) + ‘ 48.7 ± 31.2aA 0.59 ± 0.3aB 28.3 ± 7.3aA

+ „ 77.7 ± 22.3abA 48.3 ± 2.3abB 32.8 ± 6.6aB

+ 1 113.6 ± 60.8bA 73.2 ± 35.6bAB 28.4 ± 8.7aB

+ 2 109.4 ± 37.7bA 137.4 ± 55.4cA 33.5 ± 7.1aB

– „ 13.7 ± 5.92A∗ 5.6 ± 1.94B∗ 3.2 ± 0.78B∗

938 Functional Plant Biology R. Peperkorn et al.

Table 2. Physiological responses to abiotic factorsMean values (± standard deviation) of physiological traits of all species and treatments (light and nutrient); lower and upper case superscriptletters indicate significant differences between nitrogen treatments and species, respectively, (ANOVA, P<0.05; n = 2–5), ∗ indicates differencesbetween light treatments at 3 / 4 N (t-test, P<0.05), – not measured, N = nitrogen, L = high (+) / low (–) light, other abbreviations, see Materials

and methods

Traits L N Acacia longifolia Halimium halimifolium Pinus pinea

Aarea (µmol m−2 s−1) + ‘ 10.0 ± 3.2a – –+ „ 15.3 ± 3.1bA 18.3 ± 0.9aA –+ 1 17.8 ± 2.6bA 19.5 ± 3.8aA –+ 2 14.8 ± 0.9bA 15.0 ± 1.4aA –– „ 12.4 ± 1.6A 12.6 ± 2.8A∗ –

Amass (µmol kg−1 s−1) + ‘ 104 ± 23a – –+ „ 139 ± 19bA 204 ± 3aB –+ 1 174 ± 26cA 252 ± 56aB –+ 2 154 ± 19bcA 202 ± 45aA –– „ 278 ± 44A∗ 368 ± 32B∗ –

Amax (µmol m−2 s−1) + ‘ 22.2 ± 4.7a – –+ „ 28.6 ± 3.4bA 34.5 ± 5.1aA –+ 1 30.0 ± 2.1bcA 36.8 ± 4.4aB –+ 2 33.1 ± 1.2cA 31.1 ± 6.7aA –– „ 27.2 ± 3.9A 25.5 ± 0.9A –

Dark respiration (µmol m−2 s−1) + ‘ –0.57 ± 0.51a – –+ „ –0.31 ± 0.18aA –0.24 ± 0.17aA –+ 1 –0.35 ± 0.14aA –0.23 ± 0.13aA –+ 2 –0.51 ± 0.28aA –0.44 ± 0.12aA –– „ –0.16 ± 0.03A –0.41 ± 0.16B –

WUE (µmol CO2 mmol−1 H2O) + ‘ 4.68 ± 0.47a – –+ „ 5.68 ± 0.61aA 5.96 ± 0.07aA –+ 1 6.93 ± 1.13bA 6.17 ± 0.45aA –+ 2 5.11 ± 0.44aA 6.64 ± 0.77aB –– „ 4.42 ± 0.52A∗ 4.66 ± 0.66A∗ –

Fv / Fm + ‘ 0.69 ± 0.12aA – 0.74 ± 0.06aA

+ „ 0.70 ± 0.04abA 0.80 ± 0.02aB 0.72 ± 0.03aA

+ 1 0.78 ± 0.03bcA 0.80 ± 0.01aA 0.76 ± 0.01aA

+ 2 0.78 ± 0.01bA 0.80 ± 0.02aA 0.77 ± 0.05aA

– „ 0.80 ± 0.01A∗ 0.78 ± 0.01A 0.78 ± 0.01A∗

�F / Fm′ (400) + ‘ 0.41 ± 0.14aA – 0.54 ± 0.02aA

+ „ 0.46 ± 0.09aA 0.59 ± 0.01aB 0.41 ± 0.05bA

+ 1 0.57 ± 0.05aA 0.61 ± 0.01aA 0.55 ± 0.02aA

+ 2 0.50 ± 0.04aA 0.59 ± 0.04aB 0.54 ± 0.05aAB

– „ 0.53 ± 0.03A 0.58 ± 0.04A 0.51 ± 0.03A∗

�F / Fm′ (1500) + ‘ 0.13 ± 0.06aA – 0.27 ± 0.03aB

+ „ 0.14 ± 0.04aA 0.24 ± 0.03aB 0.18 ± 0.05bAB

+ 1 0.33 ± 0.22bA 0.29 ± 0.04aA 0.29 ± 0.06aA

+ 2 0.16 ± 0.02aA 0.27 ± 0.07aA 0.25 ± 0.08abA

– „ 0.20 ± 0.02A∗ 0.23 ± 0.04A 0.24 ± 0.05A

Light-use efficiency (α) + ‘ 0.26 ± 0.05aA – 0.29 ± 0.01aA

+ „ 0.28 ± 0.02aAB 0.29 ± 0.01aA 0.25 ± 0.02bB

+ 1 0.30 ± 0.01aA 0.31 ± 0.01aA 0.29 ± 0.01aA

+ 2 0.28 ± 0.03aA 0.30 ± 0.01aA 0.29 ± 0.01aA

– „ 0.29 ± 0.01A 0.30 ± 0.002A 0.29 ± 0.01A∗

The competition experiment: response to biotic factors

Competition (Table 3) did not significantly influence biomassproduction, leaf area and SLA of A. longifolia and P. pinea,except that interspecific competition of these species reducedroot biomass compared with the control. All biomassparameters and the leaf area of H. halimifolium were

significantly reduced in competition with A. longifolia,while SLA was unaffected. The allocation pattern ofA. longifolia and H. halimifolium were independent ofthe competition treatment, whereas P. pinea exhibited asignificant increase in biomass allocation to leaves and stemsand a reduction in RMR as response to both, intraspecificand interspecific competition. All species showed a reduced

Phenotypic plasticity of an invasive acacia Functional Plant Biology 939

Tab

le3.

Mor

phol

ogic

alan

dal

loca

tion

resp

onse

toco

mpe

titi

onM

ean

valu

es(±

stan

dard

devi

atio

n)of

mor

phol

ogic

alan

dal

loca

tion

trai

tsof

the

com

petit

ion

expe

rim

ent

ofea

chsp

ecie

sgr

own

asa

sing

leco

ntro

lpl

ant

(A=

A.

long

ifolia

,H

=H

.ha

limifo

lium

,P

=P.

pine

a)an

din

tras

peci

fic(A

A,

HH

,PP

)an

din

ters

peci

fic(A

H,

AP)

inco

mpe

titio

n;lo

wer

case

supe

rscr

ipt

lette

rsin

dica

tesi

gnifi

cant

diff

eren

ces

betw

een

trea

tmen

ts(A

NO

VA

,P<

0.05

;n=

7–10

)

Lea

fSt

emR

oot

Tota

lL

MR

SMR

RM

RR

oot/

shoo

tSL

AL

AR

(mg

DW

)(m

gD

W)

(mg

DW

)(m

gD

W)

(gg−1

)(g

g−1)

(gg−1

)(g

g−1)

(m2

kg−1

)(c

m2

g−1)

A.l

ongi

folia

Con

trol

A98

9±

378a

255

±12

6a50

0±

293a

1743

±71

6a0.

58±

0.05

a0.

15±

0.05

a0.

24±

0.08

a0.

39±

0.16

a12

.8±

1.2a

74±

10a

Intr

aspe

cific

AA

893

±48

0a30

7±

255a

337

±15

8ab15

36±

743a

0.59

±0.

12a

0.19

±0.

13a

0.19

±0.

05a

0.29

±0.

10b

12.7

±1.

5a75

±19

a

com

petit

ion

Inte

rspe

cific

AH

870

±55

2a24

8±

178a

389

±27

7ab14

86±

946a

0.59

±0.

14a

0.16

±0.

03a

0.22

±0.

12a

0.30

±0.

07b

12.7

±1.

5a74

±18

a

com

petit

ion

Inte

rspe

cific

AP

859

±34

0a25

3±

111a

264

±12

3b13

98±

555a

0.61

±0.

03a

0.18

±0.

03a

0.18

±0.

03a

0.27

±0.

06b

13.6

±1.

7a84

±13

a

com

petit

ion

H.h

alim

ifoliu

mC

ontr

olH

112

±73

a16

±10

a41

±26

a16

8±

105a

0.65

±0.

06a

0.09

±0.

03a

0.22

±0.

07a

0.35

±0.

13a

19.6

±2.

2a12

8±

19a

Intr

aspe

cific

HH

95±

39a

12±

6a34

±25

ab14

0±

56a

0.68

±0.

10a

0.08

±0.

03a

0.22

±0.

10a

0.26

±0.

07b

20.1

±2.

8a13

8±

28a

com

petit

ion

Inte

rspe

cific

AH

50±

23b

5±

2b17

±5b

72±

27b

0.68

±0.

05a

0.08

±0.

02a

0.21

±0.

05a

0.32

±0.

06ab

19.5

±2.

1a13

2±

12a

com

petit

ion

P.pi

nea

Con

trol

P11

40±

566a

248

±13

6a13

29±

483a

2717

±11

31a

0.42

±0.

04a

0.09

±0.

01a

0.42

±0.

05a

1.01

±0.

19a

6.5

±0.

8a27

±5a

Intr

aspe

cific

PP11

49±

372a

253

±95

a11

20±

394ab

2514

±84

2a0.

46±

0.03

b0.

10±

0.01

b0.

36±

0.05

b0.

79±

0.11

b6.

6±

0.6a

31±

4b

com

petit

ion

Inte

rspe

cific

AP

1039

±34

5a24

0±

95a

964

±36

0b22

43±

779a

0.47

±0.

03b

0.11

±0.

01b

0.37

±0.

04b

0.75

±0.

12b

6.5

±0.

4a31

±2b

com

petit

ion

940 Functional Plant Biology R. Peperkorn et al.

root / shoot ratio due to the presence of any neighbour.Intraspecific competition did not affect most biomassparameters in A. longifolia and P. pinea. In H. halimifoliumit was even less effective than interspecific competition.

Short-term 15N uptake under competition

Compared with the other species A. longifolia wassignificantly more efficient in the uptake of the 15N-labellednitrogen pulse (Fig. 2). 15N uptake was less than half inH. halimifolium, the species with the lowest root biomass.Even though P. pinea reached the highest root biomass andsimilar root surface area (Fig. 2 and inset, respectively) toA. longifolia, 15N uptake was similar to H. halimifolium.While competition treatments did not have a significanteffect on the 15N isotope concentration of P. pinea andA. longifolia, interspecific competition of H. halimifoliumand A. longifolia significantly reduced the 15N uptake of theformer species. Intraspecific competition of A. longifoliaresulted in a similar reduction in 15N uptake as interspecificcompetition between A. longifolia and P. pinea. Intraspecificcompetition did not reduce 15N uptake in P. pineaand H. halimifolium.

Phenotypic plasticity

Mean phenotypic plasticity (MPP) in relation to abioticfactors did not show pronounced differences betweeninvasive and native species (Fig. 3A). However, differencesoccurred when the plasticity of various traits was treatedseparately (Fig. 3A). Independent of species, plasticity wassignificantly higher in structural than in physiological traits.

0

50

100

150

200

250

0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6

Root biomass (g)

15N

exc

ess

in to

tal r

oot (

nmol

)

0

50

100

150

200

250

0 100 200 300 400 500 600

Total surface area (cm2)

15N

exc

ess

in to

tal r

oot (

nmol

)

AH

AH

AP

AP

AA

HHH

PP

PP

AP

AH

HH

AA

AP

AHA

P

A

HP

Fig. 2. 15N isotope concentration in roots v. root biomass of single control plants (open symbolsmarked with A = A. longifolia, H = H. halimifolium, P = P. pinea), intraspecific competition (grey symbolsmarked with AA, HH, PP, respectively) and interspecific competition (black symbols marked with AH,AP), � = A. longifolia, ◦= H. halimifolium, � = P. pinea; inset: 15N isotope concentration in roots v.calculated total root surface area, mean ± s.e., n = 5–10.

Structural variables were separated into morphologicaland allocation parameters. P. pinea exhibited the lowestplasticity in morphological and allocation traits. The highestplasticity was detected for H. halimifolium in allocationand morphological traits (0.84 and 0.97, respectively).A. longifolia exhibited the highest plasticity of physiologicalvariables compared to the other species, although thedifference was not significant.

Mean phenotypic plasticity in relation to competitiveinteractions (Fig. 3B) was lower than to abiotic factors.H. halimifolium exhibited a significantly higher MPPcompared to the other species. This was also truefor the allocation traits, while for morphological traitsthese differences were not significant. For all species nosignificant differences were detected between allocation andmorphological traits.

Discussion

High phenotypic plasticity has often been described to becharacteristic for invasive species (e.g. Davis et al. 2000;Durand and Goldstein 2001; Huxman and Smith 2001;Yamashita et al. 2002). Surprisingly, mean phenotypicplasticity (MPP) to abiotic factors (light and nitrogen)does not reveal differences between native and invasivespecies (Fig. 2). The values of 0.54–0.57 shown here arecomparable to evergreen shrubs from the tropical rainforest(0.5–0.65; Valladares et al. 2000a), but contrast with typicalplasticity values for other Mediterranean sclerophylls(approximately 0.10–0.45, Valladares et al. 2000b). Thismight be due to different weighting of physiological and

Phenotypic plasticity of an invasive acacia Functional Plant Biology 941

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1.0

MPP morphology allocation0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1.0

MPP physiology morphology allocation

A. longifolia

H. halimifolium

P. pinea

Phe

noty

pic

plas

ticity

inde

x [(

max

–min

)/m

ax]

Phe

noty

pic

plas

ticity

inde

x [(

max

–min

)/m

ax]

A

A B

AA

aA

aAaA

bA

bA

bA bA

bB

bA

A

B

A

aA

aA

aA

aA

aB

aA

Fig. 3. Phenotypic plasticity index of the native and invasive species to abiotic (light and nutrients, A) factorsand competition (B); physiological traits were not measured in the competition experiment (B). MPP comprises20 and 12 traits in (A) and (B), respectively. Lower and upper case letters indicate significant differences betweentrait (groups of one species) and species (within one trait group), respectively, (ANOVA P<0.05), mean ± s.e.(n = 5–20).

structural traits. Valladares et al. (2000b) focused on leaftraits and included a higher quantity of photosynthesis-relatedtraits, which have been shown to be less plastic. Therefore,the use of different numbers of traits within the scopeof comparison of trait assemblies of different plasticitiesis a weak point of the plasticity index, since parametertrait groups seem to have a significant effect on the result.Nevertheless, species comparison of plasticity indices fromthe same basis is possible and can be very useful to identifysignificant differences.

In spite of similar overall plasticity, differences aroseamong the phenotypic plasticities of trait groups withlow plastic response in physiological parameters and acomparatively higher plasticity in morphological andallocation parameters. Physiological characteristics ofA. longifolia were not consistently different from thenative species. This has been described before for otherinvasive species (Smith and Knapp 2001), and physiologicalresponses to changing environmental conditions do not seemto be a key factor for the invasion in the Mediterraneandune ecosystem. This also supports the findings ofKraaij and Cramer (1999), who suggested the same forsuccessful invasive alien acacia species (A. longifolia andA. saligna) in the Fynbos biome. Several authors described asignificantly higher maximal photosynthetic rate for invasivespecies than for native species, when comparing similarlife forms (Pattison et al. 1998; Durand and Goldstein2001). Acacia, which forms phyllodes instead of leaves,did not exhibit high photosynthetic capacities. In general,invasion by A. longifolia was not related to physiologicaldifferences and plasticity of these traits seems to be ofminor importance for adaptations to different Mediterraneanenvironmental conditions.

The examined species differ in their strategies and lifeforms, H. halimifolium being a small shrub, A. longifoliaforming large shrub or small tree canopies, while P. pinea

forms open pine forests on these dune habitats. Interestingly,the invasive acacia exhibits several strategies comparableto the earlier successional, drought semi-deciduousH. halimifolium, such as a rapid growth rate and high seedrain (Peperkorn 2005). Acacia can sustain high biomassand rapid leaf turnover (e.g. through leaf shedding duringdrought) even though it forms larger, thicker phyllodescompared with malacophyllous leaves of H. halimifolium.These species co-occur in the same habitat and fieldobservations have shown that they frequently appearclosely associated (C Maguas unpubl. data), probablycompeting for the same resources. However, ultimatelyacacia occupies the place of the late successional treespecies, forming dense, monotype stands, displacingpine species.

While physiology seems to be of little relevance, plasticityin allocation and morphological traits were of comparativelyhigher importance for adaptation to different environmentalconditions in the studied plants. This is in agreement withfindings that in a nutrient-limited environment growth ismore hampered than photosynthesis (Poorter and Villar 1997;Poorter and Nagel 2000). Major species differences occurredin the plastic response of allocation parameters. HereA. longifolia showed an intermediate plasticity within thenative species with a significantly lower plasticity comparedto H. halimifolium. Species allocation pattern followed moreor less the predictions of the ‘functional equilibrium theory’of Brouwer (1962, 1963), which states that above-groundplant parts are favoured when light or CO2 are in poorsupply, and growth of below-ground parts is promoted ifwater or mineral nutrients are short (Poorter and Nagel 2000;Arndt and Wanek 2002). An indicator of this allocationpattern is the root / shoot ratio (Gower et al. 1992; Reynoldsand Dantonio 1996; Garnier 1998; Perkins and Owens2003). Both native and invasive species behaved as expected:their root / shoot values ranged within the expected margins

942 Functional Plant Biology R. Peperkorn et al.

(e.g. 0.1–4.8; Hilbert and Canadell 1995) which characterisesthe species as adapted to drought-prone and nutrient-poorenvironments (Chapin 1980; Gedroc et al. 1996). Plasticityin morphological parameters did not exhibit any speciesdifference, although H. halimifolium tended to be themost plastic species. In general, plasticity in allocationand morphological traits seems to be of comparablyhigh importance for species adaptation to environmentalheterogeneity, but invasion of Mediterranean dunes byA. longifolia does not seem to be related to a higherplasticity, since neither mean plasticity nor physiological,morphological or allocation plasticity differed from thenative species.

While species differences in plasticity in response toabiotic factors did not occur, plasticity in response tobiotic factors (competition) exhibited significant speciesdifferences. Generally, plastic response to competitionwas lower for all species than to abiotic factors. Meanphenotypic plasticity of H. halimifolium was significantlyhigher compared with the other species, which did not differ.Allocation parameters seemed to be responsible for theobserved differences, as it was the main difference betweenthe species of concern, similar to the pattern found for theresponse to different abiotic conditions. This may indicatethat competing neighbour plants can alter below-groundresource availability and therefore affect neighbours in avery similar way to variation of abiotic resources (Robinsonand Rorison 1988). Usually intraspecific competition isexpected to be greater than interspecific competition (Hodgeet al. 2000; Olson and Blicker 2003) because plants of thesame species require the same environmental conditions.The discrepancy between this expectation and the presentresults implicates that A. longifolia and P. pinea showedan equal competitive effect on each other in relation tonutrient uptake, which was not significantly different fromintraspecific competition. However, H. halimifolium wassignificantly less competitive than A. longifolia resulting in ahigh competitive pressure of A. longifolia with a significantreduction of biomass and leaf area of H. halimifolium(Table 3). Thus, the high competitive ability of A. longifoliais also reflected in the plasticity index, showing a lowresponse to competitive interactions. The low plastic responseimplements competitive advantage because a high shootelongation rate is expressed under all investigated conditions.On the contrary the species showing higher phenotypicplasticity (H. halimifolium) in allocation traits was inhibitedby A. longifolia.

The results of the current investigation indicate differentgrowth strategies of the examined species, with the invasivespecies showing the highest shoot elongation rate (Fig. 1).Even in open dune ecosystems high elongation rates mayprovide a competitive advantage for seedlings in occupyingspace and shading out competing plants. LAR, one factorresponsible for RGR (Potter and Jones 1977; Poorter 1990),

was also significantly higher in A. longifolia than in P. pinea,but lower compared with H. halimifolium, and speciesdifferences were not influenced by competitive interaction(Table 3). Its fast shoot elongation rate characterisesA. longifolia as a species exhibiting a pioneer growthstrategy (Hicks et al. 2001). Likewise, H. halimifoliumshows typical traits of pioneer species with early seedgermination and a very fast increase of population size(Dıaz Barradas et al. 1999). On the other hand, P. pineashows a moderate growth (Gilman and Watson 1993)with a compact and dense growth form. P. pinea indeedaccumulated a higher biomass and showed similar elongationrate at the lowest nutrient availability compared toA. longifolia. This might be at least partially due to thesignificant larger seeds of P. pinea (Acacia = 19.1 ± 3.1 mg,Pinus = 676.9 ± 144.4 mg; P<0.01). The high shootelongation rate of A. longifolia, independent of nutrientavailability, corresponds with findings that at growth-limitingnitrogen supply growth rates of potentially fast-growingspecies are typically higher than that of naturally slow-growing species (Hull and Mooney 1990; Lambers andPoorter 1992; Van de Vijver et al. 1993; Fogarty andFacelli 1999). The observed differences in shoot heightbetween native and invasive species were enhanced withincreasing nutrient supply. P. pinea was insensitive tonitrogen, indicating that either growth was not limitedby nitrogen or an additional N-availability could not beefficiently transferred into a higher shoot elongation (Fig. 1).The insensitivity reflects that P. pinea is well adapted to soilsof low nutrient status (Richardson 1998). This is underlinedby the impassivity of P. pinea to competition (see above).

In contrast to the present study, several authors (Poorter1990; Van der Werf 1996; Hunt and Cornelissen 1997)found that fast-growing species tend to have a higher SLAthan slow-growing species. Particularly, compared to theslow growing P. pinea, a typical Mediterranean-type woodyspecies, SLA of the fast growing A. longifolia was unaltered.This discrepancy was previously recognised by Kraaij andCramer (1999), comparing two acacia species with Fynbosspecies in South Africa. They argued that the differentlight intensities in these studies might be a reason for thecontrasting findings. Another reason may also be that themajority of available data come from plants from temperateclimates, whereas the study of Kraaij and Cramer (1999)and the present work focused on plants from Mediterranean-type ecosystems. However, A. longifolia produces phyllodesinstead of leaves, which are thicker and might be less plasticwith respect to SLA. The same is true for needles of P. pinea.

While phenotypic plasticity in response to abioticfactors seems to be of minor relevance for invasion ofMediterranean dune ecosystems, it can be concluded that thecombination of an efficient nitrogen uptake and a competitiveadvantage of a higher shoot elongation rate in nutrient-limited Mediterranean-type environments may, in fact, be

Phenotypic plasticity of an invasive acacia Functional Plant Biology 943

an important trait for the invasive species to establish andpersist in the new habitat, as generally postulated for invasivespecies (Burke and Grime 1996). Further A. longifolia,being a legume, can use an additional nitrogen source andtherefore enhance its advantage over the non-nitrogen fixingindigenous species even further. Additionally, there is someevidence that nitrogen fixing acacia species increase theN status of the ecosystems they invade (Witkowski 1991), andtherefore ameliorate the conditions for the establishment oftheir offspring, while native species are less facilitated by thenew conditions. Finally, the persistence could be supported bya high tolerance against competition with some native speciesand a high competitiveness over others.

References

Aerts R (1999) Interspecific competition in natural plant communities:mechanisms, trade-offs and plant–soil feedback. Journal ofExperimental Botany 50, 29–37. doi: 10.1093/jexbot/50.330.29

Aerts R, Berendse F (1988) The effect of increased nutrient availabilityon vegetation dynamics in wet heathlands. Vegetatio 76, 63–69.

Aerts R, Boot RGA, van der Aart PJM (1991) The relation betweenabove- and belowground biomass allocation patterns andcompetitive ability. Oecologia 87, 551–559. doi: 10.1007/BF00320419

Arndt SK, Wanek W (2002) Use of decreasing foliar carbon isotopediscrimination during water limitation as a carbon tracer to studywhole plant carbon allocation. Plant, Cell & Environment 25,609–616. doi: 10.1046/j.1365-3040.2002.00838.x

Bjorkman O, Demmig B (1987) Photon yield of O2 evolutionand chlorophyll fluorescence characteristics at 77 K amongvascular plants of diverse origins. Planta 170, 489–504.doi: 10.1007/BF00402983

Bloom AJ (1985) Resource limitation in plants — an economic analogy.Annual Review of Ecology and Systematics 16, 363–392.

Bobbink R, Bik L, Willems JH (1988) Effects of nitrogen fertilization onvegetation structure and dominance of Brachypodium pinnatum (L.)Beauv. in chalk grassland. Acta Botanica Neerlandica 37, 231–242.

Bouma TJ, Koutstaal BP, van Dongen M, Nielsen KL (2001)Coping with low nutrient availability and inundation: rootgrowth responses of three halophytic grass species from differentelevations along a flooding gradient. Oecologia 126, 472–481.doi: 10.1007/s004420000545

Brouwer R (1962) Nutritive influences on the distribution of drymatter in the plant. Netherlands Journal of Agricultural Sciences 10,361–376.

Brouwer R (1963) Some aspects of the equilibrium between overgroundand underground plant parts. In ‘Jaarboek van het Instituut voorBiologisch en Scheikundig onderzoek aan Landbouwgewassen’.Vol. 213. pp. 31–39. (SPB Academic Publishing: The Hague)

Burke MJW, Grime JP (1996) An experimental study of plantcommunities invasibility. Ecology 77, 776–790.

Chapin FS III (1980) The mineral nutrition of wild plants. AnnualReview of Ecology and Systematics 11, 233–260. doi: 10.1146/annurev.es.11.110180.001313

Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plantcommunities: a general theory of invisibility. Journal of Ecology 88,528–534. doi: 10.1046/j.1365-2745.2000.00473.x

Dıaz Barradas MC, Zunzunegui M, Garcia Novo F (1999) Autecologicaltraits of Halimium halimifolium in contrasting habitats underMediterranean type climate — a review. Folia Geobotanica 43,189–208.

Dietz H, Steinlein T (2004) Recent advances in understanding plantinvasion. In ‘Progress in botany. Vol. 65’. (Eds K Esser, U Luttge,W Beyschlag, J Murata) pp. 539–573. (Springer-Verlag: Berlin)

Durand LZ, Goldstein G (2001) Photosynthesis, photoinhibition, andnitrogen use efficiency in native and invasive ferns in Hawaii.Oecologia 126, 345–354. doi: 10.1007/s004420000535

Fogarty G, Facelli JM (1999) Growth and competition of Cytisusscoparius, an invasive shrub, and Australian native shrubs. PlantEcology 144, 27–35. doi: 10.1023/A:1009808116068

Frak E, Le Roux E, Millard P, Dreyer E, Jaouen G, Saint-Joanis B,Wedler R (2001) Changes in total leaf nitrogen and partitioning,of leaf drive photosynthetic acclimation to light in fully developedwalnut leaves. Plant, Cell & Environment 18, 605–618.

Garnier E (1998) Interspecific variation in plasticity of grasses inresponse to nitrogen supply. In ‘Population biology of grasses’.(Ed. GP Cheplick) pp. 155–182. (Cambridge University Press:Cambridge, UK)

Gedroc JJ, McConnaughay KDM, Coleman JS (1996) Plasticity inroot / shoot partitioning: optimal, ontogenetic, or both? FunctionalEcology 10, 44–50.

Gilman EF, Watson DG (1993) Pinus pinea: stone pine. ENH-631,Institute of Food and Agricultural Science, University of Florida, FL.

Gower ST, Vogt KA, Grier CC (1992) Carbon dynamics of RockyMountain Douglas-fir: influence of water and nutrient availability.Ecological Monographs 62, 43–65.

Hicks DL, Campbell DJ, Atkinson IAE (2001) Options for managingthe Kaimaumau wetland, Northland, New Zealand. In ‘Science forconservation (Wellington, NZ), 155’. (Ed. G Gregory) pp. 36–38.(Science Publication, Department of Conservation: Wellington)

Hilbert DW, Canadell J (1995) Biomass partitioning and resourceallocation of plants from Mediterranean-type ecosystems: possibleresponses to elevated atmospheric CO2. In ‘Global change andMediterranean-type ecosystems’. (Eds EO Lange, HA Mooney)pp. 76–101. (Springer Verlag: New York)

Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter A (2000)Spatial and physical heterogeneity of N supply from soil does notinfluence N capture by two grass species. Functional Ecology 14,645–653.

Huenneke LF, Hamburg SP, Koide R, Mooney HA, Vitousek PM(1990) Effects of soil resources on plant invasion andcommunity structure in California serpentine grassland. Ecology 71,478–491.

Hull JC, Mooney HA (1990) Effects of nitrogen on photosynthesis andgrowth-rates of four California annual grasses. Acta Oecologica 11,453–468.

Hunt R, Cornelissen JHC (1997) Components of relative growth rate andtheir interrelations in 59 temperate plant species. New Phytologist135, 395–417. doi: 10.1046/j.1469-8137.1997.00671.x

Huxman TE, Smith SD (2001) Photosynthesis in an invasive grass andnative forbs at elevated CO2 during an El Nino year in the MojaveDesert. Oecologia 128, 193–201. doi: 10.1007/s004420100658

Ingestad T (1982) Relative addition rate and external concentration:driving variables in plant nutrition research. Plant, Cell &Environment 5, 443–453.

Kraaij T, Cramer MD (1999) Do the gas exchange characteristics ofalien acacias enable them to successfully invade the fynbos? SouthAfrican Journal of Botany 63, 232–238.

Kruger FJ (1987) Responses of plants to nutrient supply inMediterranean-type ecosystems. In ‘Plant response to stress’. NATOASI Series, Vol. G15 (Eds JD Tenhunen, FM Catarino, OL Lange,WC Oechel) pp. 415–427. (Springer-Verlag: Berlin)

Lambers H, Poorter H (1992) Inherent variation in growth rate betweenhigher plants: a search for physiological causes and ecologicalconsequences. Advances in Ecological Research 23, 187–261.

944 Functional Plant Biology R. Peperkorn et al.

Marchante H (2001) Invasao dos ecossistemas dunares portugesespor Acacia: uma ameaca para biodiversidade nativa. MSc Thesis.University of Coimbra, Portugal.

Marchante H, Marchante E, Freitas H (2003) Invasion of the Portuguesedune ecosystems by the exotic species A. longifolia (Andrews)Willd.: effects at the community level. In ‘Plant invasions:ecological threats and management solutions’. (Eds LE Child,JH Brock, G Brundu, K Prach, P Pysek, PM Wade, M Williamson)pp. 75–85. (Backhuys Publisher: The Netherlands)

Mitchell DT, Coley PGF, Webb S, Allsopp N (1986) Litterfall anddecomposition processes in the coastal fynbos vegetation, south-western Cape, South Africa. Journal of Ecology 74, 977–993.

Mooney HA (1999) Species without frontiers. Nature 397, 665–666.doi: 10.1038/17740

Niinemets U, Valladares F, Ceulemans R (2003) Leaf-level phenotypicvariability and plasticity of invasive Rhododendron ponticumand non-invasive Ilex aquifolium co-occurring at two contrastingEuropean sites. Plant, Cell & Environment 26, 941–956.doi: 10.1046/j.1365-3040.2003.01027.x

Olson BE, Blicker PS (2003) Response of the invasive Centaureamaculosa and two grasses to N-pulses. Plant and Soil 254,457–467. doi: 10.1023/A:1025536100535

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

Pearcy RW (1994) Photosynthetic response to sunflecks and light gaps:mechanisms and constraints. In ‘Photo-inhibition of photosynthesisfrom molecular mechanisms to the field’. (Eds NR Baker,JR Bowyer) pp. 255–272. (Bios Scientific Publishers: Oxford, UK)

Peperkorn R (2005) Key factors of invasiveness of Acacia longifolia —experimental comparison with native species from Mediterraneansand ecosystems. PhD Thesis, University of Bielefeld, Germany.

Perkins SR, Owens MK (2003) Growth and biomass allocationof shrub and grass seedlings in response to predicted changesin precipitation seasonality. Plant Ecology 168, 107–120.doi: 10.1023/A:1024447305422

Poorter H (1990) Interspecific variation in relative growth rate.In ‘Causes and consequences of variation in growth rate andproductivity of higher plants’. (Ed. H Lambers) pp. 45–68.(SPB Academic Publishing: The Hague)

Poorter H, Lambers H (1986) Growth and competitive ability of ahighly plastic and marginally plastic genotype of Plantago majorin a fluctuating environment. Physiologia Plantarum 67, 217–222.

Poorter H, Villar R (1997) Chemical composition of plants: causesand consequences of variation in allocation of C to different plantconstituents. In ‘Plant resource allocation’. (Eds F Bazzaz andJ Grace) pp. 39–72. (Academic Press: New York)

Poorter H, Nagel O (2000) The role of biomass allocation in the growthresponse of plants to different levels of light, CO2, nutrients andwater: a quantitative review. Australian Journal of Plant Physiology27, 595–607.

Potter JR, Jones JW (1977) Leaf area partitioning as an important factorin growth. Plant Physiology 59, 10–14.

Reynolds HL, Dantonio C (1996) The ecological significance ofplasticity in root weight ratio in response to nitrogen. Plant andSoil 185, 75–97.

Richardson DM (1998) ‘Ecology and biogeography of Pinus’.(Cambridge University Press: Cambridge, UK)

Robinson D, Rorison IH (1988) Plasticity in grass species in relation tonitrogen supply. Functional Ecology 2, 249–257.

Smith MD, Knapp AL (2001) Physiological and morphological traitsof exotic, invasive exotic, and native plant species in tallgrassprairie. International Journal of Plant Sciences 162, 785–792.doi: 10.1086/320774

Smith VH, Tilman GD, Nekola JC (1999) Eutrophication:impacts of excess nutrient inputs on freshwater, marine, andterrestrial ecosystems. Environmental Pollution 100, 179–196.doi: 10.1016/S0269-7491(99)00091-3

Stock WD, Sommerville JEM, Lewis OAM (1987) Seasonal allocationof dry mass and nitrogen in a fynbos endemic Restionaceaespecies Thamnochortus punctatus Pill. Oecologia 72, 315–320.doi: 10.1007/BF00379284

Sultan SE (2000) Phenotypic plasticity for plant development,function and life history. Trends in Plant Science 5, 537–542.doi: 10.1016/S1360-1385(00)01797-0

Sultan SE (2001) Phenotypic plasticity for fitness components inPolygonum species of contrasting ecological breadth. Ecology 82,328–343.

Thurston J (1969) The effect of limiting and fertilizers on the botanicalcomposition of permanent grassland, and on the yield of hay. In‘Ecological aspects of the mineral nutrition of plants’. (Ed. I Rorison)pp. 3–10. (Blackwell Scientific: Oxford, UK)

Tilman D (1988) ‘Plant strategies and the dynamics and structure ofplant communities.’ (Princeton University Press: Princeton, NJ)

Valladares F, Pugnaire FI (1999) Trade-off between irradiancecapture and avoidance in semi-arid environments assessed witha crown architecture model. Annals of Botany 83, 459–469.doi: 10.1006/anbo.1998.0843

Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW (2000a)Plastic phenotypic response to light of 16 congeneric shrubs from aPanamanian rainforest. Ecology 81, 1925–1936.

Valladares F, Martınez-Ferri E, Balaguer L, Perez-Corona E,Manrique E (2000b) Low leaf-level response to light andnutrients in Mediterranean evergreen oaks: a conservative resource-use strategy? New Phytologist 148, 79–91. doi: 10.1046/j.1469-8137.2000.00737.x

Van der Werf A (1996) Growth analysis and photo-assimilatepartitioning. In ‘Photo-assimilate distribution in plants and crops:source–sink relationship’. (Eds E Zamski, AA Schaffer) pp. 1–20.(Marcel Dekker Inc.: New York)

Van de Vijver CADM, Boot RGA, Poorter H, Lambers H (1993)Phenotypic plasticity in response to nitrate supply of an inherentlyfast-growing species from a fertile habitat and an inherently slow-growing species from an infertile habitat. Oecologia 96, 548–554.doi: 10.1007/BF00320512

Van Wilgen BW, Little PR, Chapman RA, Gorgens AHM, Willems T,Marais C (1997) The sustainable development of water resources:history, financial cost, and benefits of alien plant controlprogrammes. South African Journal of Science 93, 404–411.

Williams DG, Mack RN, Black RA (1995) Ecophysiology of introducedPennisetum setaceum on Hawaii: the role of phenotypic plasticity.Ecology 76, 1569–1580.

Witkowski ETF (1991) Effects of invasive alien acacias on nutrientcycling in the coastal lowlands of the Cape Fynbos. Journalof Applied Ecology 28, 1–15.

Witkowski ETF, Mitchell DT, Stock WD (1990) Response of Capefynbos ecosystem to nutrient additions: shoot growth and nutrientcontents of a proteoid (Leucospermum parile) and an ericoid(Phylica cephalantha) evergreen shrub. Acta Oecologica 11,311–326.

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

Manuscript received 27 October 2004, received in revised form22 March 2005, accepted 24 May 2005

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