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Applied Soil Ecology 62 (2012) 71– 80

Contents lists available at SciVerse ScienceDirect

Applied Soil Ecology

journa l h o me page: www.elsev ier .com/ locate /apsoi l

nteractions between arbuscular mycorrhiza and the growth of the invasive aliennnual Impatiens parviflora DC: A study of forest type and soil properties inature reserves (S Poland)

amian Chmuraa,∗, Ewa Gucwa-Przepiórab

Institute of Engineering and Environmental Protection, Faculty of Materials and Environmental Sciences, University of Bielsko-Biała, 2 Willowa Str, PL 43-309 Bielsko-Biała, PolandDepartment of Plant Systematics, Faculty of Biology and Environmental Protection, University of Silesia, Jagiellonska 28, PL 40-032 Katowice, Poland

r t i c l e i n f o

rticle history:eceived 24 January 2012eceived in revised form 24 July 2012ccepted 29 July 2012

eywords:ycorrhiza

oillant invasionlant growth

a b s t r a c t

Invasive alien plants can benefit from interactions with mycorrhizal fungi in their spread and competitionwith native species. Hitherto, little was known about the ecological conditions related to the presence ofarbuscular mycorrhiza (AM) in the annual invasive alien species Impatiens parviflora. The soil properties,plant morphometric features, mycorrhizal status, degree of root colonization and morphotype of arbus-cular mycorrhiza were evaluated in different forest communities: alder-ash carrs, oak-hornbeam forests,beech forests and mixed forests. Mycorrhizal plants of this species were found in all of the analyzed forestcommunities and the Arum-type of morphology was reported. The largest and most fecund individualsas well as the highest mycorrhizal frequency (F%) and relative arbuscular richness (A%) were recordedin individuals from populations growing in alder-ash carrs and oak-hornbeam forests. A comparison ofsites where non-mycorrhizal AM− and mycorrhizal AM+ individuals of I. parviflora were found revealedthat AM+ plants grow on soils with a higher magnesium content and that were more alkalized. The Pear-son and Spearman correlations yielded positive significant coefficients with respect to the relationshipsbetween mycorrhizal frequency and pH. The arbuscule richness in root fragments where mycorrhiza was

present (a%) was found to be positively correlated with pH and Ellenberg moisture as well. However, theratio of C/N was negatively correlated with F% and a%. The mean height of plants was positively correlatedwith (F%), relative mycorrhizal root length (M%) and relative arbuscular richness (A%). The latter werealso positively correlated with the number of flowers and fruits. The study revealed that I. parviflora is notan obligatory mycorrhizal plant and AM seems to influence the growth and reproduction of this plant,and that it can indirectly enable the spread and naturalization of the species.

. Introduction

The roots of 90–95% of vascular plant species are colonized byymbiotic mycorrhizal fungi in a symbiotic association in natu-al plant communities (Read, 1991; Entry et al., 2002). Arbuscularycorrhizal symbioses are the most abundant of the several differ-

nt types of mycorrhizas. They are formed by a wide variety of hostlants, including angiosperms, gymnosperms, pteridophytes andome mosses, lycopods and psilotales with a relatively small groupf aseptate filamentous fungi. In this association the host plant

rovides the fungus with soluble carbon sources. Nutrients andater are taken up by the fungus and translocated to the host. The

elowground abundance and diversity of arbuscular mycorrhizal

∗ Corresponding author. Tel.: +48 82 79171; fax: +48 82 79101.E-mail addresses: dchmura@ath.bielsko.pl, dachmura@gmail.com (D. Chmura),

wa.Gucwa-Przepiora@us.edu.pl (E. Gucwa-Przepióra).

929-1393/$ – see front matter © 2012 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.apsoil.2012.07.013

© 2012 Elsevier B.V. All rights reserved.

fungi (AMF) and the different mycorrhizal dependencies of plantspecies can determine plant community structure and ecosystemvariability (Entry et al., 2002).

It has been found that invasive alien plants benefit from inter-actions with mycorrhizal fungi (van der Heijden et al., 1998; vander Heijden, 2002; Klironomos, 2002). The feedback between alienplants and soil communities may strongly determine the ability ofa plant to establish, invade and persist in a local habitat. On theother hand, invasive plants can affect the species composition andfunction of soil organisms. Some plant invaders produce allelo-pathicals which disrupt the belowground competitive outcomebetween plants and mycorrhizal fungi. The reduction of mycor-rhizal colonization caused by allelopathic invasive alien plants canindirectly have a negative impact on the native plants which bene-

fit from mycorrhiza (Bothe et al., 2010 and literature cited therein).There are many case studies showing that arbuscular mycorrhiza-invasive plant feedback can be positive or negative. It may occurthat arbuscular mycorrhiza may facilitate the invasiveness of a

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2 D. Chmura, E. Gucwa-Przepióra

iven species or have no effect on it. When the effect is positive,t includes an increase in the ability to spread, competitive ability,iomass and growth of the invasive plant (Shah et al., 2009).

In the present study, we focused on the small balsam Impa-iens parviflora DC. This ballochorous annual of Asiatic origin wasecorded in Poland for the first time near Gdansk in 1850. Sincehen, it has spread through almost the entire territory of the coun-ry. It mainly invades deciduous forests (Tokarska-Guzik, 2005).t is questionable whether this species is able to displace nativepecies (Łysik, 2008) and no possible negative impact has beenbserved (Hejda, 2012). The phenomenon of biological controly the rust Puccinia komarovii – a natural enemy of I. parvifloraBacigalova et al., 1998; Piskorz and Klimko, 2006) is quite wellnown. However, the literature data on the relation of I. parvi-ora with mycorrhizal fungi are ambiguous or not fully known.he earliest reports (Truszkowska, 1953) indicated that mycorrhi-al plants in this species were found in a population growing in ansh-alder carr Fraxino-Alnetum near Domaszyn. In a review work,oombe (1956) stated that mycorrhiza had not been detected in I.arviflora in Great Britain at all. Peace and Grubb (1982), in theirxperiment with the interaction of the addition of fertilizer andight supply on the growth of this species, showed that arbuscules

ere found in unfertilized plants at the highest levels of irradiance.herefore, in this study we wanted to examine whether mycor-hiza in I. parviflora is present in natural habitats. We particularlyanted to answer the following questions: (1) In which naturallant communities, where I. parviflora was found, are there mycor-hizal individuals of this species? (2) Do mycorrhizal plants differn relation to the intensity of root cortex colonization between theistinguished, invaded plant communities? (3) Are there relation-hips between mycorrhizal colonization and soil properties? (4)nd finally, are there any relationships between the intensity ofycorrhizal colonization and plant height, the number of flowers

nd fruits – features that are associated with invasiveness?

. Materials and methods

.1. Sites descriptions

The investigations were carried out in prevailing vegetationypes in 7 forest nature reserves in the Kraków-Czestochowapland situated in Southern Poland. This region covers an area ofbout 2615 km2 and is mostly built from Jurassic dolomites. Theharacteristic elements of the landscape are limestone rocks andumerous caves. The mean elevation of the area is about 350 m.s.l. The soils of this area are rather poor, 60% are podzolic soils andore rarely, brown soils occur. The mean annual temperature is ca.

.5 ◦C and the mean annual precipitation amounts to ca. 700 mm.he forest vegetation of the nature reserves is characterized by aigh degree of naturalness. The phytosociological character and

ocation of these reserves as well as their soil properties have beenescribed in detail elsewhere (Chmura and Sierka, 2006a,b; Chmurat al., 2007). The focal species I. parviflora is an invasive species inhe study area that has penetrated the natural forest vegetationituated in nature reserves (Chmura and Sierka, 2006a,b, 2007).ites for soil sampling, biometrical and mycorrhizal studies wereelected randomly in such a way so as to avoid pseudoreplicationensu Hurlbert (1984) in well-developed patches in the forest inte-iors of four woodland communities. Each type of investigation waserformed on the same study plots. The studied forest types occurlong an environmental gradient from the bottom of river valleys

o the top of hills within the area of the nature reserves that werexamined. The patches of ash-alder carr occupy the bottom of riveralleys while patches of oak-hornbeam and beech forests grow atigher altitudes. Patches of mixed forest are sites where conifers

lied Soil Ecology 62 (2012) 71– 80

such as Pinus sylvestris or Picea abies were planted in the habitatof oak-hornbeam forests. A total of 30 sites were selected from3 to 6 sites per nature reserve and from 6 to 9 sites per forestcommunity within the area of the nature reserves (Table 1). Theforest vegetation in the 30 randomly selected sites was classifiedphytosociologically into the 4 forest types: oak-hornbeam forests(Tilio-Carpinetum Tracz. 1962), alder-ash carrs (Fraxino-Alnetum W.Mat. 1952), beech forests (Dentario glandulosae-Fagetum W. Mat.1964 ex Guzikowa et Kornas), and mixed forests (Querco robori-Pinetum W. Mat. 1981 J. Mat. 1988). The nomenclature of plantcommunities follows Matuszkiewicz (2001).

2.2. Soil sampling

Four soil sub-samples from topsoil were collected from 0 to20 cm depths and mixed into one composite sample. Each samplewas taken from the rhizosphere of I. parviflora.

After air-drying and sieving over 2 mm, they were analyzed forpH, measured potentiometrically in H2O and in 1 N KCl and totalorganic C (%), according to the Tiurin method. Loss on ignition wastested in a muffle furnace (%), total N content (%) using the Kjel-dahl method, available Mg using FAAS (Flame Atomic AbsorptionSpectrometry), available phosphorus P in an ammonium lactateextraction using the colorimetry method, sodium Na and potas-sium K were detected using flame emission spectroscopy and Caby spectrophotometry in 1 N ammonium acetate (mg/kg) (Litynskiet al., 1976; Ostrowska et al., 1991). The Ellenberg moisture indi-cator value was used as the measure of soil moisture. The meanarithmetic values of this indicator were calculated for each sitebased on the presence/absence of data of vascular plant speciesin the phytosociological records. The species defined in the Ellen-berg system as indifferent were omitted from the computations(Dzwonko, 1997).

2.3. Mycorrhizal studies

Mycorrhizal research was carried out on roots of I. parvifloracollected during the period of flowering at the end of June 2006.At every sampling site, 10 replicate samples containing roots ofrandomly chosen plant individuals were collected from an area of5 m × 5 m and at a depth of 0–20 cm. Due to the high variability inmorphological plasticity and abundance as well as the area occu-pied by each population of I. parviflora, only specimens exclusivelyfrom codominant and dominant plant classes were randomly cho-sen. Whole plants were excavated and cleaned mechanically fromthe substrate. The roots were cut from the specimens, washed inwater and stored in 50% ethanol. In total 900, 1-cm long root pieceswere analyzed. For the estimation of mycorrhizal development, theroots were prepared according to a modified method of Phillips andHayman (1970). After careful washing in tap water, the roots weresoftened in 7% KOH for 24 h and then rinsed in a few changes ofwater. The material was acidified in 5% lactic acid for 24 h and thenstained with 0.01% aniline blue in lactic acid for 24 h. The entireprocedure was carried out at room temperature.

The following parameters describing the intensity and effec-tiveness of the mycorrhization were recorded: mycorrhizalfrequency (F%) – the ratio between root fragments colonized byAMF mycelium and the total number of root fragments analyzed,relative mycorrhizal root length (M%) – an estimate of the amountof root cortex that was mycorrhizal relative to the whole root

system, the intensity of colonization within individual mycor-rhizal roots (m%), relative arbuscular richness (A%) – arbusculerichness in the whole root system and arbuscule richness in rootfragments where the arbuscules were present (a%) (Trouvelot

D. Chmura, E. Gucwa-Przepióra / Applied Soil Ecology 62 (2012) 71– 80 73

Table 1Number of samples per site and forest type in the study area.

Nature reserve Forest type Total

Alder-ash carr Beech forest Oak-hornbeam forest Mixed forest

Bukowica (50◦04′43′′N, 19◦23′55′′S) 3 2 5Dolina Eliaszowki (50◦10′18′′N, 19◦38′02′′S) 1 2 3Dolina Kluczwody (50◦09′54′′N, 19◦49′10′′S) 2 1 1 4Dolina Racławki (50◦09′49′′N, 19◦41′33′′S) 3 1 4Lipowiec (50◦04′42′′N, 19◦26′38′′S) 2 3 1 6Skała Kmity (50◦06′06′′N, 19◦48′38′′S) 2 2 4

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Total 8

t al., 1986, http://www2.dijon.inra.fr/mychintec/Mycocalc-rg/download.html)

.4. Morphometric studies

The same plants from which roots were collected were usedor morphometric studies. The following features were examined:lant height, width and length of the longest leaf, number of flow-rs, number of fruits per plant and cumulative number of flowersnd fruits.

.5. Data analysis

Before the statistical analyses, the normality and homogene-ty of the variance of data were checked. When necessary the soilnd morphometric data were log-transformed. Mycorrhizal col-nization expressed as a percentage was arcsin-transformed fornalysis. To examine differences between forest types in the soilarameters and in morphometric features of I. parviflora, analysis ofariance ANOVA followed by the LSD Fisher test was applied. Whenhe data did not meet the assumptions for parametrical tests, theruskal–Wallis test and the Conover test for pairwise comparisonsere employed. The soil data between sites with mycorrhiza was

ound and sites without it were compared using the Student’s testr the Wilcoxon sum rank test, respectively. Differences betweenommunities in relation to F%, M%, m%, A%, and a% were estimatedy analysis of variance ANOVA followed by the LSD Fisher testr by the Kruskal–Wallis test and the Conover test. In order tovaluate the relationship between mycorrhiza coefficients and soilariables or selected morphometric features, the Pearson correla-ion test or Spearman rank correlation test were employed. Onlymycorrhizal) AM+ plants were taken into account for the pur-ose of this analysis and soil variables per a sample. Following theorrelation tests, Principal Components Analysis (PCA) was usedo reduce the dimensionality of the soil dataset and to produce aet of uncorrelated variables to aid in explaining any variation inycorrhizal and morphometric plant parameters. Interpretation

f principal component analysis was done by observing the com-on characteristics of soil variables with the highest loadings per

rincipal component. As an alternative approach to examine themportance of the factors influencing AM colonization and plantarameters, Redundancy Analysis (RDA) was calculated (Ter Braaknd Smilauer, 2002). This method is based on PCA (Principal Com-onents Analysis) in which the linear dependency of the studiedariables on environmental factors is constrained (Jongman et al.,000). Two RDAs permitted us to study which explanatory factors,

.e. soil parameters influence the dependent variables, i.e. all plantarameters including AM colonization combined and which AM

olonization parameters have a significant impact on plant mor-hometric parameters. In this method mean morphometric plantarameters per a sample were used. The significance of the modelas checked by forward selection of the Monte Carlo test with 999

4

7 6 30

permutations. Each explanatory variable which had an inflationfactor >10 was excluded from the analysis.

All statistics were computed using R software (R DevelopmentCore Team, 2008).

3. Results

3.1. Differences in soil variables and morphometric features ofImpatiens parviflora between forest types

The forest types studied differ in some soil variables (Table 2).The patches of alder-ash carrs appeared to have the highest valueof pH, the lowest value of C/N and the highest value of Ellenbergmoisture. There were higher values of magnesium content in alder-ash carrs and beech forests in comparison with mixed forests. Inalder-ash carrs, there was a significantly higher concentration ofCa2+ than in mixed forests (Table 2). The largest and most fecundindividuals of small balsam were observed in the ground flora ofan alder-ash carr. In relation to the width of leaves, there are alsosignificant differences between oak-hornbeam forests and beechforests (Table 2).

3.2. AM status and colonization

Arbuscular mycorrhizae with arbuscules, which are the struc-tural and functional criterion of symbiosis, were found in the rootsof Impatiens parviflora in all of the forest communities analyzed,but not in all samples (Fig. 1). In addition to the arbuscules, vesiclesand coils were also present in the plants; however, the former wererarer and the latter were encountered in only one sample. All ofthe plants examined showed the Arum-type morphotype in whichAMF most often colonizes the inner cortex cells and arbuscules areformed terminally.

The richness of mycorrhizal structures varied among differentstands. The highest mycorrhizal frequency (F%) was recorded inspecimens from populations growing in alder-ash carrs, the inter-mediate in oak-hornbeam forests and mixed forests. The lowest(F%) was reported from populations occurring in beech forests(Fig. 1a). With respect to relative arbuscule richness (A%), speci-mens from alder-ash carrs were characterized by a significantlyhigher value compared to plants from the remaining types of com-munities (Fig. 1b); also beech forests had the lowest value of relativearbuscule richness. As regards arbuscule richness in mycorrhizalroot fragments (a%), the highest values of this parameter weredetected in individuals from alder-ash carrs and oak-hornbeamforests and the lowest – in mixed forests and beech forests (Fig. 1c).In terms of the intensity of root cortex colonization (M%), the high-

est values were observed in alder carrs (Fig. 1d); likewise in thecase of the intensity of colonization within individual mycorrhizalroots (m%) (Fig. 1e). Mycorrhizal plants (AM+) were the largest andmost fecund when compared to non-mycorrhizal (AM−) (Table 3).

74 D. Chmura, E. Gucwa-Przepióra / Applied Soil Ecology 62 (2012) 71– 80

Table 2Mean and standard deviation values of the soil elements, Ellenberg moisture and morphometric features in Impatiens parviflora between forest types. Means with the sameletter are not significantly different (ANOVA or Kruskal–Wallis test followed by LSD Fisher or Conover test, respectively); ns – non-significant.

Variable Alder-ash carr Beech forest Oak Hornbeam forest Mixed forest P-value

pH H2O 7.07 ± 0.43a 5.32 ± 1.45b 5.03 ± 1.56b 3.74 ± 0.48b <0.001pH KCl 6.71 ± 0.48a 4.86 ± 1.51b 4.48 ± 1.63b 3.27 ± 0.47b <0.001Corg (%) 3.42 ± 1.65 6.35 ± 4.03 4.83 ± 1.15 4.89 ± 1.22 nsLoss on ignition (%) 10.80 ± 4.34 14.70 ± 7.10 11.25 ± 1.45 10.50 ± 1.84 nsNtot (%) 0.25 ± 0.09 0.36 ± 0.20 0.29 ± 0.04 0.43 ± 0.40 nsC/N 13.22 ± 1.72a 17.66 ± 3.71b 16.90 ± 3.59b 16.31 ± 6.94b <0.05P (mg/100 g) 2.49 ± 3.02 9.77 ± 18.48 2.20 ± 1.50 4.96 ± 3.72 nsMg2+ (cmol+ kg−1) 0.48 ± 0.22a 0.69 ± 1.04a 0.27 ± 0.34ab 0.03 ± 0.05b <0.05K+ (cmol+ kg−1) 0.14 ± 0.14 0.17 ± 0.11 0.06 ± 0.12 2.27 ± 0.04 nsCa2+ (cmol+ kg−1) 33.97 ± 18.99a 20.47 ± 15.58ab 14.86 ± 13.63ab 3.96 ± 3.84b <0.01Na+ (cmol+ kg−1) 0.13 ± 0.03 0.15 ± 0.04 0.14 ± 0.02 0.14 ± 0.02 nsMoisture 6.31 ± 0.25a 5.51 ± 0.19b 5.24 ± 0.33b 5.54 ± .08b <0.001Height of plants 66.9 ± 25.7a 28.4 ± 14.5b 30.6 ± 16.7b 28.8 ± 15.2b <0.001Number of flowers 27.1 ± 51.5a 2.7 ± 3.5b 3.5 ± 4.1b 2.7 ± 2.1b <0.01

3.9 ± 4.2b 4.3 ± 4.8b <0.018.3 ± 2.3b 8.0 ± 2.3b <0.054.5 ± 1.1c 4.3 ± 1.1bc <0.05

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Table 4The Pearson and Spearman coefficients between soil variables and mycorrhiza col-onization (P < 0.05); ns – nonsignificant (only those soil data which gave significantresults are shown). F%: mycorrhizal frequency; a%: arbuscules richness in root frag-ments where AM was present.

Soil properties Mycorrhizal parameters

F% a%

pH KCl 0.58 0.65Ca2+ ns 0.51

Number of fruits 20.8 ± 41.3a 4.8 ± 3.5b

Length of leaves 10.0 ± 3.6a 8.0 ± 2.38b

Width of leaves 5.2 ± 1.9a 3.9 ± 1.3b

.3. Relationship between AM colonization and soil properties

A comparison of sites where AM− and AM+ individuals of I. parv-flora were present revealed that AM+ plants were found on soilsignificantly richer in magnesium content and with a higher pHTable 3). The Principal Components Analysis showed an 80% cumu-ative variance for the first four components. Principal component

was highly loaded for both pH in aqua and pH in KCl and calciumons; principal component 2 was highly loaded for loss on ignition.rincipal component 3 was loaded for C/N, whereas principal com-onent 4 was the most loaded for the Ellenberg moisture index andhosphorus.

The Pearson and Spearman correlations yielded positive signifi-ant coefficients with respect to relationships between mycorrhizalrequency F and pH value. The relationship between the richness ofrbuscules in mycorrhizal root fragments (a%) and pH was foundo be significant, as well as between this variable and Ca content.owever, the ratio of C/N was negatively correlated with F% and%. The Ellenberg moisture index positively correlated with a%Table 4). There were no significant relationships between A%, M%,nd m% and any soil properties. The arrangement of 30 samples of

. parviflora in the RDA ordination in relation to soil variables and

orphometric features and AM colonization is shown in Fig. 2a.he eigenvalues of the first and second axis were 0.487 and 0.038,espectively. Table 5 contains the variance explained by each of the

able 3omparison of the soil properties (mean ± SD) of sites with mycorrhiza (AMF+) andithout (AMF-) and morphometric features in Impatiens parviflora. Bolded values

re significant at P < 0.05 (Student’s test or the Wilcoxon sum rank test).

AMF+ AMF−Height of plants 45.0 ± 6.9 31.6 ± 4.4Number of flowers 15.6 ± 8.9 3.2 ± 0.5Number of fruits 12.2 ± 3.9 6.5 ± 1.6Mean length of leaves 9.0 ± 0.8 8.6 ± 0.5Mean width of leaves 4.5 ± 0.3 4.4 ± 0.2pH H2O 5.9 ± 1.5 4.7 ± 1.6pH KCl 5.4 ± 1.6 4.2 ± 1.6Corg 4.9 ± 2.9 5.0 ± 2.3Loss on ignition 12.0 ± 5.6 12.0 ± 3.3NT 0.3 ± 0.1 0.4 ± 0.3C/N 15.6 ± 3.5 16.6 ± 5.5P 3.0 ± 2.9 8.2 ± 16.1Mg2+ 0.55 ± 0.75 0.53 ± 0.32K+ 0.15 ± 0.14 0.15 ± 0.7Ca2+ 21.06 ± 13.23 21.06 ± 23.02Na+ 0.14 ± 0.03 0.14 ± 0.03Moisture 5.7 ± 0.5 5.5 ± 0.3

C/N −0.51 −0.56Moisture ns 0.4

variables. The variance explained by 10 of 12 soil parameters was63% and 55% in marginal and conditional effects, respectively. Onlytwo variables significantly explained the variation of all morpho-metric and AM colonization parameters of I. parviflora ranked asfollows: pH KCl, Ca content.

3.4. Relationship between AM colonization and morphometricfeatures

The Pearson correlation coefficients between mycorrhizal col-onization indexes and the morphometric features of individualsof I. parviflora that were selected revealed some significant rela-tionships (Table 6). Mycorrhizal frequency (F%) was positively

correlated with the mean height of plants but not with the meannumber of flowers or fruits per plant. Relative arbuscular richness(A%) positively correlated with the height of plants and the num-ber of flowers and fruits (Table 6). Relative mycorrhizal root length

Table 5Percentage explained by explanatory variables and significance level in RedundancyAnalysis (Monte Carlo test) based on mean morphometric and AM colonizationparameters of Impatiens parviflora and soil parameters.

Independentvariable

Variance explainedby single variable(%)

Variance explained byvariables in order of theirinclusion in the model (%)

P-value

pH KCl 22 22 0.001Ca2+ 4 15 0.007Mg2+ 5 6 0.077Loss on ignition 4 6 0.073P 2 1 0.495K+ 2 1 0.746Moisture 11 1 0.742NT 3 1 0.833C/N 6 1 0.768Na+ 4 1 0.983

D. Chmura, E. Gucwa-Przepióra / Applied Soil Ecology 62 (2012) 71– 80 75

Fig. 1. (a–e) Differences in mycorrhizal colonization of Impatiens parviflora between forest communities. Means with SE are shown. Different letters above the bars indicatestatistically significant differences (P < 0.05). AC: alder-ash carrs; BF: beech forests; OH: oak hornbeam forests; MF: mixed forests; F%: mycorrhizal frequency; M%: relativem l rootA

(nzcaabF1ei

ycorrhizal root length; m%: intensity of colonization within individual mycorrhizaM was present.

M%) positively correlated with the height of plants and the meanumber of flowers and fruits. Arbuscule abundance in mycorrhi-al parts of root fragments (a%) and intensity of the mycorrhizalolonization within individual mycorrhizal roots (m%) were notssociated with any morphometric features of I. parviflora. Therrangement of 30 samples with I. parviflora in the RDA ordinationased on morphometric features and AM colonization is shown in

ig. 2b. The variance explained by all variables was 35% accounting3%, 11%, 6%, 4%, 1% for F%, m%, A%, M% and a%, respectively. How-ver, M% and A% are highly correlated with each other and F%. Theirnflation factor was more than 20.

s; A%: relative arbuscular richness; a%: arbuscule richness in root fragments where

4. Discussion

In our study, we present for the first time, to the best of ourknowledge, a detailed report of AMF associations in I. parvifloraroots (mycorrhizal structures, AMF morphotype and abundance ofcolonization in roots). Previous studies gave ambiguous results,which was presented in the review work by Harley and Harley

(1987) where the status of present or absent was assigned to I.parviflora. The facultative character of AM in I. parviflora was con-firmed by Lipinska (2005, 2010). Only the latest work (Stajerováet al., 2009), which presented the mycorrhizal status of 44 invasive

76 D. Chmura, E. Gucwa-Przepióra / Applied Soil Ecology 62 (2012) 71– 80

Fig. 2. Redundancy analysis (RDA) ordination of 30 samples with Impatiens parviflora showing AM colonization and mean morphometric plant parameters versus soilparameters (a) and mean morphometric plant parameters vs. AM colonization parameters (b). Only samples where mycorrhizal plants were present were shown. F%:m zationr

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ycorrhizal frequency; M%: relative mycorrhizal root length; m%: intensity of coloniichness in root fragments where AM was present.

lien plants in the Czech Republic, demonstrated that the speciess definitely mycorrhizal. The way the root cortex is penetrated by

ycorrhizal hyphae, e.g. terminally formed arbuscules, indicateshe Arum-type (Peterson et al., 2004). This type of morphology isommon in representatives of families from the Rosidae subclassike Fabaceae and Rosaceae (Zubek et al., 2008). Small balsam, as

representative of the family Balsaminaceae, belongs to this sub-lass. It is well recognized that the AM morphology may depend onhe host plant and fungal identity, and that different environmentalactors may have an impact on the AM pattern of root colonizationSmith and Read, 2008; Zubek et al., 2010).

AM colonization of I. parviflora in the plant communities studieday be influenced by plant hosts already present in phytocoenoses

nd/or soil parameters. Frequency and other mycorrhiza parame-ers vary significantly between the distinguished vegetation types

Fig. 1). Alder-ash carrs were the most abundant in AM+ plants of. parviflora followed by oak-hornbeam forests, mixed forests andnally beech forests. In addition, ordination (Fig. 2a) showed that

able 6he Pearson correlation coefficients between mycorrhiza colonization and the mor-hometric properties of Impatiens parviflora plants (P < 0.05); ns – non-significant.%: mycorrhizal frequency; A%: relative arbuscular richness; M%: relative mycorrhi-al root length.

Morphometric properties of I. parviflora Mycorrhizal parameters

F% A% M%

Height of plants 0.62 0.77 0.71Number of flowers ns 0.74 0.69Number of fruits ns 0.76 0.71Mean length of leaves ns 0.66 0.62Mean width of leaves ns 0.65 0.62

within individual mycorrhizal roots; A%: relative arbuscular richness; a%: arbuscule

samples of alder carrs are associated with an increasing value ofAM colonization parameters. Alder carrs are usually known for theoccurrence of ectomycorrhizal fungi, especially with Alnus gluti-nosa (Baar et al., 2000). However, many studies have reported thatA. glutinosa can be colonized by both ectomycorrhizal and arbus-cular mycorrhizal fungi (Oliveira et al., 2005; Orfanoudakis et al.,2010). Truszkowska (1953) recorded mycorrhizal individuals of I.parviflora in riparian and floodplain forests (alder-ash carrs), butshe did not give any information on the abundance of mycorrhizain these habitats. She also demonstrated that in alder-ash foreststhe percentage of mycorrhizal plant species was quite high andvaried between 46.5 and 79% of all species present in the forestground flora. Root colonization by AM fungi can be influenced bylocal plant species as well as the establishment of a local AMF com-munity (Zubek et al., 2009; Shah et al., 2008). The major role ofthe extraradical hyphae is to build connections between the rootsof neighbor plants and to form new colonization sites within aroot. Extramatrical mycelium constitute a common mycorrhizalnetwork (CMNs) which enables the transfer of substances betweenplants of different species. It favors an increase in species diversityin plant communities (Giovanetti, 2008). Thus, it is possible thatAM+ plants of other species could have an impact on AM coloniza-tion in I. parviflora. Taking all deciduous forest types combined inthe present study, they dominate over mixed forests in terms ofmycorrhizal parameters. As Zechmeister-Boltenstern et al. (2011)state, in general, soils of deciduous forests are characterized by ahigher proportion of AM fungi when compared to coniferous for-est soils. In our study, beech forests were the least abundant in

AM+ plants of I. parviflora. This could be the result of the location ofpatches of beech forests in the nature reserves studied. They are sit-uated at a higher altitude than the phytocoenoses of the remainingvegetation types.

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The obtained significant differences in AM colonization amonghe forest types are obviously also connected with edaphic con-itions. Several studies have demonstrated that soil nutrientoncentration is spatially and temporally varied in all ecosystemsOliveira and Oliveira, 2005); thus soil fertility has a strong impactn AMF population and AMF colonization.

Of the environmental variables, pH is the most influential fac-or which explains more than 20% of variation in plant parameters.ur investigation confirmed other studies that demonstrated thatM colonization increases along with an increasing pH. Samples

rom alder carrs are the ones most associated with this parameter.n increasing value of pH corresponds to mycorrhizal frequency

F%) and (a%) – arbuscule richness in root fragments where AM wasresent (Fig. 2a) (Table 4). Göransson et al. (2008) obtained a posi-ive relationship between pH and mycorrhizal colonization in fouroodland grass species, similar to Postma et al. (2007), who stud-

ed mycorrhizal colonization in four woodland forbs. In addition toorests, a positive relationship between pH and AMF colonizations known from other habitats such as an agroforestry plantationn Central Amazonia (Oliveira and Oliveira, 2005). Goltapeh et al.2008) state that the relationship between soil reaction and the

ycorrhizal effect is complex and dependant on the plant speciesnd type of soil, as well as the forms of phosphorus and fun-al species involved. Our results partially confirmed the patternsllustrated by Klein et al. (2006), whose study revealed a negativeelationship between the C/N ratio and the level of mycorrhizal col-nization but it was non-significant; whereas active hyphal lengthsere negatively and significantly correlated with the ratio of carbon

nd nitrogen. The positive correlation between Ca2+ (a%) – arbus-ule richness in root fragments where arbuscules were present isongruent with correlation between (a%) and pH.

Another of the crucial factors is soil moisture. Although as a sin-le variable it explains 11% of the variation in morphometric andolonization parameters, it weakly correlates with (a%) as well –rbuscule richness in root fragments where AM was present; inhe entire model, it is not a significant explanatory environmentalarameter. Thus, the potential influence of this parameter shoulde treated with caution. The soils of alder-ash carrs are generallyharacterized by higher moisture when compared to other forestabitat types. Although, we did not study soil moisture, in nat-ral phytocoenoses the Ellenberg moisture index is a very goodxplanatory variable. Stajerová et al. (2009) showed that there is

positive relationship between the relative arbuscular coloniza-ion of the invaders and soil wetness measured as the Ellenberg

oisture index. In our study, plants in alder-ash carrs, which arehe wettest communities, had the highest values in the majorityf mycorrhizal parameters as well as in the relationship betweenhe Ellenberg moisture index and the richness of arbuscules in rootragments where arbuscules were present was positive. It is oftentressed that soil moisture is negatively correlated with mycorrhi-al colonization in vascular plants. Nevertheless, there are somexceptions. Yang et al. (2008) reported an increase in the inten-ity of AM colonization with an increasing water content in soilsn 11 plants in a desert riparian forest, whereas the relationship

ith pH was negative in contrast to a present study. Apple et al.2005) also found significant changes in the percentage of all AMFtructures (arbuscules, vesicles and hyphae) associated with soiloisture. Soil moisture content was positively correlated with AMF

olonization in two fruit species in Central Amazonia (Oliveira andliveira, 2005).

In our investigations, AM+ plants were encountered on soilsharacterized by a higher concentration of magnesium. Root col-

nization is said to be stimulated by an increased concentration ofagnesium ions (Gryndler et al., 1991). Both magnesium sulphate

nd magnesium chloride influenced the colonization of the rootsf maize by Glomus. In a study by Turnau et al. (1992), fertilization

ied Soil Ecology 62 (2012) 71– 80 77

affected the mycorrhizal status of I. parviflora. After treatmentwith NPK, the percentage of coverage of plants increased but nomycorrhizae were found. Prior to fertilization, they were rarelypresent. As in our study, it has been shown that higher concen-trations of nutrients have no impact at all on the presence ofmycorrhiza in relation to total nitrogen, phosphorus and potassium(Table 4). In another work (Chmura et al., 2007) where the soil prop-erties of 139 forest sites occupied by small balsam were examined,there was no distinct relationship between the presence of I. parvi-flora and higher values of these ions. Weglarski (1991) reported thatI. parviflora is confined to soils rich in phosphorus, magnesium andpotassium. Chmura et al. (2007) showed that I. parviflora occurredmore frequently on soils poor in these nutrients. However, the factthat nitrogen content has little influence on the size of plants wasrevealed in the study by Chmura (2008a) and likewise in researchby Elemans (2004), who showed that I. parviflora had the highestbiomass with a high nutrient treatment in a greenhouse experi-ment. Another issue that remains unclear is the role of C/N becausewith an increasing value of this parameter mycorrhizal frequencyand arbuscule richness decreased (Table 5). However, in a previouswork (Chmura et al., 2007), it was demonstrated that the majorityof forest habitats occupied by small balsam were characterized byhigher values of C/N. Assuming that mycorrhiza occurs randomlyin I. parviflora, it could have been expected that with an increasingconcentration of carbon or a decreasing content of nitrogen (simul-taneously a decrease in value of C/N), the role of AM colonizationshould increase. However, our observations did not confirm this.

In our study we focused only on soil properties. Other environ-mental factors such as climatic changes at increasing elevationsabove sea level do not play a crucial role in AM colonization (Zubeket al., 2009). Small balsam I. parviflora also occurs in mountain areas,but it is not as invasive there as in lowlands (Tokarska-Guzik, 2005).

With an increasing value of pH, the soil morphometric valuesof I. parviflora also increase (Fig. 2a). Morphometric features suchas the length and width of leaves are correlated with the height ofan individual. As far as the generative features, such as the num-ber of flowers or fruits per plant, is concerned even a very smallplant (e.g. 4 cm high) can produce flowers (Chmura et al., 2007).Nevertheless, taller plants generally have more flowers and fruits(Fig. 2a). In the study by Chmura et al. (2007), it was shown thatpH had a positive influence on the height of plants, whereas C/Nhad a negative impact, which was confirmed by this study (Fig. 2a).It has long been known that arbuscular mycorrhiza enhances thegrowth of a plant (Smith and Read, 2008). Mycorrhizal coloniza-tion has been shown to stimulate the growth of a plant in manystudies. Much of the early work was devoted to crop plants, espe-cially the effect of mycorrhiza on growth on nutrient-poor soils,e.g. phosphorus (Harley and Smith, 1983), or on trees and hortic-ular plants (Eftekhari et al., 2010). However, recent studies havedemonstrated the effect of AM on plant invasions. The majorityof experiments and observations have revealed the positive influ-ence of mycorrhiza on growth and biomass, among others, in theannual herbs Centaurea maculosa (Marler et al., 1999; Callawayet al., 2004) and Anthemis cotula (Shah and Reshi, 2007). Some stud-ies have stressed an increase in the competitive ability and spreadof some invasive alien species like Centaurea melitensis (Callawayet al., 2005), Ambrosia artemisifolia (Fumanal et al., 2006) or Sol-idago canadensis (Liang et al., 2004). This is not a rule becauseother studies have shown the negative impact of AM on compet-itive ability – Centaurea maculosa (Walling and Zabinski, 2006).In our study AM+ plants were generally larger and more fecundthan AM−. There are probably two reasons for this. One is that

these are more favorable conditions which can result in a highervigorousness of plants especially in alder-ash carrs. Individuals ofI. parviflora were the largest and the most fecund on these sites.Yet Coombe (1956) stated that individuals of I. parviflora were

7 / App

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8 D. Chmura, E. Gucwa-Przepióra

ost gregarious on fringe woodlands or river-banks or analogousabitats for alder-ash carrs. The other reason could be the effectf AM colonization itself. We showed that mycorrhizal frequencyF%) and relative mycorrhizal root length (M%) positively correlatedith the height of plants. Obviously, AM colonization parameters

re also correlated with each other, which is a result of appliedethodology (Trouvelot et al., 1986). According to RDA analysis,ycorrhizal frequency (F%) is the only one variable which signif-

cantly explains variations in the morphometric parameters of I.arviflora. Although many studies have demonstrated the effectsf AM on biomass, plant height or shoot height are also taken intoccount. A study by Shah and Reshi (2007) showed that an inocula-ion of Glomus mossae enhanced stem length, as well as the numberf capitula and propagules in Anthemis cotula. Higher growth haslso been observed in crop plants such as pepper Capsicum annuumn a greenhouse inoculation experiment and in parsley Petroselinumrispum in a field inoculation experiment (Regvar et al., 2003).mall balsam is known for its very high morphological variation.he smallest fruiting individual was 4 cm and the tallest ones –00.5 cm (Chmura, 2008a,b; Danko, 2009). In the past, the differ-nces in the height of I. parviflora were believed to have resultedrom the light conditions occurring at the forest bottom (Coombe,956). In tree stand gaps individuals of this plant are the tallesthen compared to those under a compact tree canopy, whichas shown by Piskorz (2005) in her study on the phenology of

he species. Kujawa-Pawlaczyk (1991) also observed the shortestlants in shady forest interiors (1–20 cm) and the tallest ones (upo 70 cm) in paths with higher light availability in an old-growthak-hornbeam forest Tilio-Carpinetum in the Białowieza Primevalorest. Elemans (2004) demonstrated that I. parviflora had the high-st total biomass at a high nutrient treatment and at a 60% lightreatment in simulated conditions in a greenhouse. However, theo-occurrence of other species on the forest floor can affect the sizef I. parviflora plants. Other species such as Pteridium aquilinuman mechanically hamper the growth of the stems of I. parvifloraPiskorz and Klimko, 2007). Under conditions with lower competi-ion, even on sites with a lower light availability on northern slopes,ndividuals can be taller (Chmura, 2008b). The results obtainedhowed that AM colonization may be an additional factor that influ-nces the size of plants.

We also observed a correlation between mycorrhizal coloniza-ion and the number of flowers and fruits per plant. This coulde an effect of growth stimulation by AM. This is an importantnding because diasporas in annuals determine the persistence ofopulations as well as the further spread of plants. These factors

nfluence the invasiveness of a species. The impact of mycorrhizalolonization on the production of flowers and fruits is also knownrom crop plants, e.g. pepper, where in inoculated- and double-noculated fields a larger number of flowers and fruits was recordedRegvar et al., 2003); however, in a work by Castillo et al. (2009)M-inoculated plants showed the lowest number of leaves.

An enormous body of literature is focused on beneficiallant-microbe relations in nutrient-poor habitats such as dry cal-areous grasslands or under extreme conditions such as industrialastes rich in potentially toxic metals, low in macronutrients andith a poor water holding ability (Gucwa-Przepióra and Turnau,

001; Orłowska et al., 2002; Gucwa-Przepióra and Błaszkowski,007; Gucwa-Przepióra et al., 2007). Arbuscular fungi influencelant community development, nutrient uptake, water relationsnd aboveground productivity in the above-mentioned habitatsJeffries et al., 2003; Turnau et al., 2008). However, in terms of alienlant invasions, attention is usually paid to natural habitats, espe-

ially those present in protected areas such as nature reserves orational parks. The majority of invasive alien plants have changedoth the structure and function of ecosystems or have had a neg-tive impact on native and resident species. However, not a single

lied Soil Ecology 62 (2012) 71– 80

native plant species is known to have been driven to extinction dueto interactions with alien plants alone; however, the influence ofalien taxa has been proven in many taxa. Many native taxa whichare endangered are threatened by loss of habitat and by invaders.This is important in the present study, which was conducted onlywithin old-growth forests and in nature reserves. AM+ plants werefound in 60% of the observed sites.

To sum up, it can be said that small balsam I. parviflora is notan obligatory mycorrhizal species and that AM colonization is nota random phenomenon because it seems to be influenced by someecological factors such as soil properties. The results obtained sug-gest that arbuscular mycorrhiza can have a positive impact on bothfruit and seed production and the vigorousness of plants. Thesetraits are associated with invasiveness and competition ability,which enhance the invasion success of a given species. In additionto the number of flowers and fruits, other aspects of sexual repro-duction may be influenced by the colonization of mycorrhizal fungi,including the timing of reproductive events, the amount of pollenper flower, the proportion of flowers producing fruits and the num-ber of seeds per fruit. Seed quality can also be strongly influencedby the colonization of mycorrhizal fungi, thus resulting in varia-tion in seedling vigor and the resulting competitive ability (Koide,2010). Further research is needed to explain how AM colonizationchanges during a vegetation season, which is especially interest-ing in the case of an annual plant. Another interesting issue is theoccupation of semi-natural and manmade habitats by I. parviflorawhere the species is also invasive.

Acknowledgements

We are grateful to the four anonymous reviewers for insightfulcomments on early version of this text. We also acknowledge Ms.Michele Simmons for the linguistic comments on the manuscript.The study was partially supported financially by Polish Ministry ofScience and Higher Education (grant no. 3 PO4 G093 25).

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