Invasive plants are usually fast-growing species with a high rate of physiological processes. However, the relative growth rate has not been estimated for many invasive species, including Acer negundo L. (Sapindaceae) and Amelanchier spicata (Lam.) K. Koch (Rosaceae); this hampers the understanding of the reasons for the success of their invasion. The authors compared the absorbing roots of A. negundo and A. spicata with respect to mycorrhizal colonization with two native woody species of the same families, Acer platanoides L. and Sorbus aucuparia L. The samples were collected from several sites in the Central Urals and analysed using standard morphological and anatomical methods. The abundance of arbuscular mycorrhiza,dark septate endophytes and root hairs did not differ between the invasive and native species. Nevertheless, the roots of the invasive species were shown to have a thicker cortex parenchyma formed by larger cells. We suggest that this could contribute to invasion success, but a higher growth rate of the roots of invasive species has not yet been proven.
Keywords: Acer negundo, Amelanchier spicata, invasive plants, absorbing roots, arbuscular mycorrhiza, root cortex, parenchyma
&nbsp

Betekhtina, A A

Veselkin, D V

KnE Life Sciences

English

Invasive plants are usually Fast-growing species with a high rate of physiological processes. However, the relative growth rate has not been estimated for many invasive species, including Acer negundo L. (Sapindaceae) and Amelanchier spicata (Lam.) K. Koch (Rosaceae); this hampers the understanding of the reasons for the success of their invasion. The authors compared the absorbing roots of A. negundo and A. spicata with respect to mycorrhizal colonization with two native woody species of the same families, Acer platanoides L. and Sorbus aucuparia L. The samples were collected from several sites in the Central Urals and analysed using standard morphological and anatomical methods. The abundance of arbuscular mycorrhiza,dark septate endophytes and root hairs did not differ between the invasive and native species. Nevertheless, the roots of the invasive species were shown to have a thicker cortex parenchyma formed by larger cells. We suggest that this could contribute to invasion success, but a higher growth rate of the roots of invasive species has not yet been proven.
Keywords: Acer negundo, Amelanchier spicata, invasive plants, absorbing roots, arbuscular mycorrhiza, root cortex, parenchyma
&nbsp

Betekhtina, A. A. (A)

Veselkin, D. V. (D)

Neliti

Absorbing Roots of Invasive Woody Plants Apparently Have A Thicker Cortex Parenchyma Compared to Native Species

Invasive plants are usually fast-growing species with a high rate of physiological processes. However, the relative growth rate has not been estimated for many invasive species, including Acer negundo L. (Sapindaceae) and Amelanchier spicata (Lam.) K. Koch (Rosaceae); this hampers the understanding of the reasons for the success of their invasion. The authors compared the absorbing roots of A. negundo and A. spicata with respect to mycorrhizal colonization with two native woody species of the same families, Acer platanoides L. and Sorbus aucuparia L. The samples were collected from several sites in the Central Urals and analysed using standard morphological and anatomical methods. The abundance of arbuscular mycorrhiza, dark septate endophytes and root hairs did not differ between the invasive and native species. Nevertheless, the roots of the invasive species were shown to have a thicker cortex parenchyma formed by larger cells. We suggest that this could contribute to invasion success, but a higher growth rate of the roots of invasive species has not yet been proven

Betekhtina, A. A.

Veselkin, D. V.

Institutional repository of Ural Federal University named after the first President of Russia B.N.Yeltsin

Ecology and Geography of Plants and Plant CommunitiesThe fourth International Scientiﬁc Conference onEcology and Geography of Plants and Plant CommunitiesVolume 2018Conference PaperAbsorbing Roots of Invasive Woody PlantsApparently Have a Thicker CortexParenchyma Compared to Native SpeciesA. A. Betekhtina1 and D. V. Veselkin1,21Institute of the Natural Sciences and Mathematics, Ural Federal University, 620000 Ekaterin-burg, Russia2Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences, 620144Ekaterinburg, RussiaAbstractInvasive plants are usually fast-growing species with a high rate of physiologicalprocesses. However, the relative growth rate has not been estimated for manyinvasive species, including Acer negundo L. (Sapindaceae) and Amelanchier spicata(Lam.) K. Koch (Rosaceae); this hampers the understanding of the reasons for thesuccess of their invasion. The authors compared the absorbing roots of A. negundoand A. spicata with respect to mycorrhizal colonization with two native woodyspecies of the same families, Acer platanoides L. and Sorbus aucuparia L. The sampleswere collected from several sites in the Central Urals and analysed using standardmorphological and anatomical methods. The abundance of arbuscular mycorrhiza,dark septate endophytes and root hairs did not differ between the invasive and nativespecies. Nevertheless, the roots of the invasive species were shown to have a thickercortex parenchyma formed by larger cells. We suggest that this could contribute toinvasion success, but a higher growth rate of the roots of invasive species has not yetbeen proven.Keywords: Acer negundo, Amelanchier spicata, invasive plants, absorbing roots,arbuscular mycorrhiza, root cortex, parenchyma1. IntroductionInvasive species have morphological and functional traits allowing them to success-fully invade new regions and communities; their analysis is important to better under-stand the general mechanisms of plant invasion and is thus of considerable appliedrelevance. Invasive plants have been shown to have a high growth rate, a high rate ofphysiological processes and a preferential allocation of biomass and nutrients to leavesand shoots [1]. However, the relative growth rate has not been estimated for manyHow to cite this article: A. A. Betekhtina and D. V. Veselkin, (2018), “Absorbing Roots of Invasive Woody Plants Apparently Have a Thicker CortexParenchyma Compared to Native Species” in The fourth International Scientific Conference on Ecology and Geography of Plants and Plant Communities,KnE Life Sciences, pages 34–42. DOI 10.18502/kls.v4i7.3217Page 34Corresponding Author:A. A. Betekhtinabetechtina@mail.ruReceived: 12 September 2018Accepted: 15 October 2018Published: 29 October 2018Publishing services provided byKnowledge EA. A. Betekhtina and D. V.Veselkin. This article isdistributed under the terms ofthe Creative CommonsAttribution License, whichpermits unrestricted use andredistribution provided that theoriginal author and source arecredited.Selection and Peer-reviewunder the responsibility of theEcology and Geography ofPlants and Plant CommunitiesConference Committee.Ecology and Geography of Plants and Plant Communitiesinvasive species, including Acer negundo L. and Amelanchier spicata (Lam.) K. Koch. Itwas important for us to reveal the morphological traits associated with the suggestedhigh growth rate. Such traits can be found in both above- and below-ground plantorgans [2, 3].As far as below-ground organs are concerned, the strategic characteristics ofplants are associated mainly with the root cortex [4], more speciﬁcally with the mostmetabolically active tissue such as cortex parenchyma [5]. Usually, thicker roots witha greater number of cortex parenchyma cell layers and higher tissue density requiremore energy and nutrients, grow slower and live longer [4, 6]. In contrast, the rootsof fast-growing species have a high speciﬁc root length (SRL) and a small number ofcell layers; therefore, they are able to grow faster and intercept resources [7]. Invasiveplants have been shown to have a high SRL as well [8], which means that their rootsare energetically cheap to produce [4]. Although SRL strongly correlates with rootdiameter [9], it is usually calculated for all roots less than 1 mm in diameter which arefunctionally divergent: this does allow for an accurate comparison. The data on ﬁneroot diameter are limited; it has been shown to be the same [10, 11], smaller [12] orgreater [14, 15] in invasive plants than in native species. Such a difference betweenstudies could be due to the analysis of either taxonomically or ecologically distinctplant species.The aim of the present study was to compare several morphological and anatomicaltraits between (i) functionally homogeneous absorbing roots with primary develop-ment and (ii) taxonomically close invasive and native species growing in the sameconditions. This will reduce methodological, taxonomic and ecological effects.2. Methods2.1. Plant speciesWe selected two invasive species, box elder (Acer negundo L.) and low juneberry(Amelanchier spicata L.), shown to be invasive in Europe [16], Russia [17] and theCentral Urals [18]. For comparison, two native species were studied: Norway maple(Acer platanoides L.) and rowan (Sorbus aucuparia L.). Both species are rather commonin the Central Urals, where the samples were collected.DOI 10.18502/kls.v4i7.3217 Page 35Ecology and Geography of Plants and Plant Communities2.2. Study sitesThe roots were collected in Ekaterinburg, a city in the south taiga zone with a temper-ate continental climate. To measure stable morphological and anatomical characteris-tics, two sites were chosen; an additional sampling from a third site was performedto analyse arbuscular mycorrhizal (AM) colonization as a more variable feature. In allsites, invasive and native species grew together or in close proximity to each other.2.3. Sampling and morphological analysisRoot fragments were sampled during June and July in 2015, from 5–15 cm deep for ﬁveplants of each species at each sampling site. Only the live roots of two–three distalorders were selected and ﬁxed in 70% ethanol. For each plant, 5–10 intact apical rootswere transversally cut into sections 15–20 µm in depth on a freezing microtome. Thefollowing parameters were then determined: root diameter, central cylinder diameter,the thickness of the cortex parenchyma, number of cortex parenchyma cell layers andparenchyma cell diameter. Only parenchyma cells without any cell wall thickeningwere analysed. Additionally, the abundance of AM fungi was assessed in 15 randomroot segments 1 cm in length and isolated from the roots of two distal orders. Thesesegments were macerated in KOH for 1 hour, then coloured with aniline blue and usedto make squash preparations. For each segment, ﬁve ﬁelds of view were inspectedwith a Leica DM 5000 microscope (Leica, Germany) at 100x magniﬁcation to measurethe proportion of the ﬁeld of view covered by (1) AM hyphae; (2) arbuscles; (3) vesi-cles; (4) dark septate endophytes (DSE); and (5) root hairs.Statistical analysis was carried out using the package STATISTICA 8.0 with three-factors ANOVA. In all cases, individual plants were used as experimental units.3. ResultsIn this study, we analysed the inﬂuence of three main factors: invasive status (inva-sive/native), plant family (Sapindaceae/Rosaceae) and sampling site. The commonfeature of all absorbing roots of the studied species was a high mean proportion of thecortex, 95–96%, and a small mean diameter of the central cylinder, 60–76 μm. A highproportion of the cortex is probably needed for the interaction with fungal symbiontssince all the species were mycorrhizal.DOI 10.18502/kls.v4i7.3217 Page 36Ecology and Geography of Plants and Plant CommunitiesThe number of cortex parenchyma cell layers depended on plant family: the rootsof Rosaceae plants usually had two layers of parenchyma cells while the roots of Acersp. had two or three layers. It is worth noting that the roots of A. negundo had threecell layers signiﬁcantly more frequently, but not more than 8% overall.The abundance of AM fungi, DSE and root hairs differed depending on the site;root hair abundance in Sapindaceae species was signiﬁcantly higher, which could be afamily-speciﬁc trait. No clear association between invasive status and AM abundancewas found, except for a higher abundance of AM hyphae, vesicles and arbuscles in theroots of the invasive species A. negundo (15–75% in different sites) compared with thenative A. platanoides (11–35%). A. spicata and S. aucuparia had a similar AM abundance,but in A. spicata this feature differed more strongly between sampling sites. The factthat the abundance of AM fungi depends on the site rather than other factors is inline with the current conception of symbiosis as a tool that allows the ﬁne tuning ofabsorbing roots to function in speciﬁc soil conditions [15].Root diameter varied depending on the site and plant family but was greater in thespecies of Sapindaceae (Figure 1). Most importantly, the roots of invasive species werethicker by 10%, mainly due to larger cortex parenchyma cells (Figure 1), and partly dueto a larger number of cell layers in A. negundo. The ANOVA interactions of the ‘invasivestatus’ factor together with ‘plant family’ or ‘sampling site’ were not signiﬁcant for thisparameter (Table 1).Thus, the absorbing roots of two invasive and two native species that are bothtaxonomically and ecologically related differed in root diameter, the thickness of theroot cortex parenchyma and parenchyma cell diameter. Invasive A. negundo and A.spicata had thicker roots with a thicker parenchyma formed by larger cells. Theseresults are supported by the fact that A. negundo has thicker roots compared to thenative Acer species in the Southern Urals [15]; a similar pattern has been shown for theinvasive species Heracleum sosnowskyi [14, 15]. However, our results do not correspondwith the previous studies showing the same or thinner roots [10–12] or a higher SRL [8]in invasive plants. We found that rootswithmore parenchyma cell layers (three vs two)were signiﬁcantly more frequent in invasive A. negundo than in native A. platanoides:however, since this frequency did not exceed 8%, we cannot claim that invasive andnative plants signiﬁcantly differ in the metabolic cost of root growth. Although we didour best to reduce all the effects of the choice of samples and methods, the data arestill insufﬁcient to make any clear conclusion.The question is how a thicker cortex parenchyma with larger cells would contributeto invasion success. We think that large parenchyma cells with a large central vacuoleDOI 10.18502/kls.v4i7.3217 Page 37Ecology and Geography of Plants and Plant CommunitiesT˔˕˟˘ 1: ANOVA F-values for several parameters of absorbing roots calculated for the three main factorsand their interactions.Parameter Factor Factor Interactions R2𝑎𝑑𝑗InvasiveStatus(dF = 1) [1]PlantFamily(dF = 1) [2]SamplingSite [3][1] × [2] [1] × [3] [2] × [3]Root diameter § 7.65∗∗ 12.76∗∗∗ 17.96∗∗∗ 0.41 0.30 15.00∗∗∗ 0.54Central cylinderdiameter §3.84 0.06 1.97 0.05 0.01 4.44∗ 0.10Cortex parenchymathickness §13.65∗∗∗ 6.46∗ 14.05∗∗∗ 0.05 0.27 4.11 0.44Number of cell layers § 7.49∗ 60.28∗∗∗ 6.85∗ 1.79 0.11 6.05∗ 0.66Cell diameter § 5.51∗ 2.49 5.95∗ 1.51 0.16 0.71 0.24Abundance of AMhyphae §§3.66 2.50 41.60∗∗∗ 1.93 2.39 2.99 0.61Arbuscles §§ 0.39 5.84∗ 37.24∗∗∗ 0.44 1.33 4.20 0.59Vesicles §§ 2.58 0.35 8.94∗∗∗ 0.87 4.55∗ 0.01 0.28DSE §§ 1.49 0.04 7.33∗∗ 0.01 3.80∗ 4.79∗ 0.39Root hairs §§ 1.81 15.88∗∗∗ 3.88∗ 0.79 1.06 2.30 0.36Source: Authors’ own work.Note: # dF = 1 for root diameter, central cylinder diameter and parameters of the cortex parenchyma;dF = 2 for the other parameters. The following transformations were made for ANOVA: §x’ = ln (x+ 1); §§ x’ = asin (sqrt (x)). Statistical signiﬁcance of F-values: ∗P < 0.05, ∗∗P < 0.01, ∗∗∗P < 0.001.F-values for the interaction of all three factors are not shown. R2𝑎𝑑𝑗 – R2 adjusted for the full ANOVAmodel.could optimize their water and nutrient uptake by substantially reducing cell respi-ration [5]. Moreover, the presence of large intercellular spaces in such parenchymatissue could be an additional factor minimizing root respiration. The positive correlationbetween the size of parenchyma cells and growth rate seems to be universal, as it hasbeen shown for photosynthetic tissues of fast-growing plants as well [2].4. ConclusionOur results suggest that the same or even lower thickness of the absorbing roots ofinvasive plants, shown previously might be inferred while comparing an integral valuesuch as SRL; also, the plants studied differed not only in invasive status but also in theirtaxonomic position or habitat. Whenwe compared both taxonomically and ecologicallyclose species using a directly measured value, the diameter of absorbing roots withprimary development, the roots of invasive plants turned out to have a thicker cortexparenchymawith larger cells. We suggest that this could contribute to invasion successby reducing root respiration, but data proving a higher growth rate in the roots ofinvasive species are still insufﬁcient.DOI 10.18502/kls.v4i7.3217 Page 38Ecology and Geography of Plants and Plant CommunitiesFigure 1: Comparison of the studied features of absorbing roots between invasive and native species ofSapindaceae (∘) and Rosaceae (•) families. Mean values and standard errors are shown. Source: Authors’own work.AcknowledgementThe authors are grateful to Dr L. A. Ivanova (Botanical Garden, Ural Branch of RAS,Ekaterinburg, Russia) for her valuable comments.FundingThe part of the project headed by Dr Anna Betekhtina was supported by the Ministryof Education and Science of the Russian Federation within the framework of the stateDOI 10.18502/kls.v4i7.3217 Page 39Ecology and Geography of Plants and Plant Communitiesassignment No. 6.7696.2017/8.9. The part headed by Dr Denis Veselkin was performedwithin the State Contract of the Institute of Plant and Animal Ecology, UB RAS.References[1] van Kleunen, M., Weber, E., and Fischer, M. (2010). A metaanalysis of traitdifferences between invasive and noninvasive plant species. Ecology Letters, vol.13, no. 2, pp. 235–245.[2] Pyankov, V. I., Ivanova, L. A., and Lambers, H. (1998). Quantitative anatomy ofphotosynthetic tissues of plants species of different functional types in a borealvegetation, in Inherent Variation in Plant Growth. Physiological Mechanisms andEcological Consequences, pp. 71–87. Leiden: Backhuys Publishers.[3] Semchenko, M., Lepik, A., Abakumova, M., et al. (2017). Different sets ofbelowground traits predict the ability of plant species to suppress and tolerate theircompetitors. Plant and Soil, vol. 424, no. 1–2, pp. 157–169.[4] Eissenstat, D. M., Wells, C. E., Yanai, R. D., et al. (2000). Whitbeck, building roots ina changing environment: Implications for root longevity. New Phytologist, vol. 147,no. 1, pp. 33–42.[5] Lynch, J. P., Chimungu, J. G., and Brown, K. M. (2014). Root anatomical phenesassociated with water acquisition from drying soil: Targets for crop improvement.Journal of Experimental Botany, vol. 65, no. 21, pp. 6155–6166.[6] McCormack, L. M., Adams, T. S., Smithwick, E. A., et al. (2012). Predicting ﬁne rootlifespan from plant functional traits in temperate trees. New Phytologist, vol. 195,no. 4, pp. 823–831.[7] Comas, L. H. and Eissenstat, D. M. (2004). Linking ﬁne root traits to maximumpotential growth rate among 11 mature temperate tree species. Functional Ecology,vol. 18, no. 3, pp. 388–397.[8] Jo, I., Fridley, J. D., and Frank, D. A. (2017). Invasive plants accelerate nitrogen cycling:Evidence from experimental woody monocultures. Journal of Ecology, vol. 105, pp.1105–1110.[9] Ostonen, I., Püttsepp, Ü., Biel, C, et al. (2007). Speciﬁc root length as an indicator ofenvironmental change. Plant Biosystems, vol. 141, no. 3, pp. 426–442.[10] Craine, J. M. and Lee, W. G. (2003). Covariation in leaf and root traits for native andnon-native grasses along an altitudinal gradient in New Zealand. Oecologia, vol. 134,no. 4, pp. 471–478.DOI 10.18502/kls.v4i7.3217 Page 40Ecology and Geography of Plants and Plant Communities[11] Keser, L. H., Visser, E. J., Dawson, W., et al. (2015). Herbaceous plant species invadingnatural areas tend to have stronger adaptive root foraging than other naturalizedspecies. Frontiers in Plant Science, vol. 6, no. 273.[12] Smith, M. S., Fridley, J. D., Goebel, M., et al. (2014). Links between belowground andaboveground resource-related traits reveal species growth strategies that promoteinvasive advantages. PLoS One, vol. 9, no. 8.[13] Betekhtina, A. A., Sergienko, A. O., and Veselkin, D. V. (2018). Root structureindicates the ability of Heracleum sosnowskyi to Absorb resources quickly underoptimum soil conditions. Biology Bulletin, vol. 45, no. 3, pp. 247–254.[14] Veselkin, D. V., Ivanova, L. A., Ivanov, L. A., et al. (2017). Rapid use of resourcesas a basis of the Heracleum sosnowskyi invasive syndrome. Proceedings BiologicalSciences, vol. 473, pp. 53–56.[15] Veselkin, D. V., P’yankov, S. V., Safonov, M. A., et al. (2017). The structure ofabsorbing roots in invasive and native maple species. Russian Journal of Ecology,vol. 48, no. 4, pp. 303–310.[16] Delivering alien invasive species inventories for Europe (DAISIE), www.europe-aliens.org.DOI 10.18502/kls.v4i7.3217 Page 41Ecology and Geography of Plants and Plant Communities[17] Vinogradova, Yu. K., Mayorov, S. R., and Khorun, L. V. (2010). The Black Data Bookof Flora of Central Russia: Alien Species of Plants in the Ecosystems of Central Russia.Moscow: GEOS.[18] Tretyakova, A. S. (2011). Invasive potential of adventive plant species of the CentralUrals. Russian Journal of Biological Invasions, vol. 2, no. 4, pp. 281–285.DOI 10.18502/kls.v4i7.3217 Page 42

Absorbing Roots of Invasive Woody Plants Apparently Have a Thicker Cortex Parenchyma Compared to Native Species

KnE Publishing Platform

Ecology and Geography of Plants and Plant CommunitiesThe fourth International Scientific Conference onEcology and Geography of Plants and Plant CommunitiesVolume 2018Conference PaperAbsorbing Roots of Invasive Woody PlantsApparently Have a Thicker CortexParenchyma Compared to Native SpeciesA. A. Betekhtina1 and D. V. Veselkin1,21Institute of the Natural Sciences and Mathematics, Ural Federal University, 620000 Ekaterin-burg, Russia2Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences, 620144Ekaterinburg, RussiaAbstractInvasive plants are usually fast-growing species with a high rate of physiologicalprocesses. However, the relative growth rate has not been estimated for manyinvasive species, including Acer negundo L. (Sapindaceae) and Amelanchier spicata(Lam.) K. Koch (Rosaceae); this hampers the understanding of the reasons for thesuccess of their invasion. The authors compared the absorbing roots of A. negundoand A. spicata with respect to mycorrhizal colonization with two native woodyspecies of the same families, Acer platanoides L. and Sorbus aucuparia L. The sampleswere collected from several sites in the Central Urals and analysed using standardmorphological and anatomical methods. The abundance of arbuscular mycorrhiza,dark septate endophytes and root hairs did not differ between the invasive and nativespecies. Nevertheless, the roots of the invasive species were shown to have a thickercortex parenchyma formed by larger cells. We suggest that this could contribute toinvasion success, but a higher growth rate of the roots of invasive species has not yetbeen proven.Keywords: Acer negundo, Amelanchier spicata, invasive plants, absorbing roots,arbuscular mycorrhiza, root cortex, parenchyma1. IntroductionInvasive species have morphological and functional traits allowing them to success-fully invade new regions and communities; their analysis is important to better under-stand the general mechanisms of plant invasion and is thus of considerable appliedrelevance. Invasive plants have been shown to have a high growth rate, a high rate ofphysiological processes and a preferential allocation of biomass and nutrients to leavesand shoots [1]. However, the relative growth rate has not been estimated for manyHow to cite this article: A. A. Betekhtina and D. V. Veselkin, (2018), “Absorbing Roots of Invasive Woody Plants Apparently Have a Thicker CortexParenchyma Compared to Native Species” in The fourth International Scientific Conference on Ecology and Geography of Plants and Plant Communities,KnE Life Sciences, pages 34–42. DOI 10.18502/kls.v4i7.3217Page 34Corresponding Author:A. A. Betekhtinabetechtina@mail.ruReceived: 12 September 2018Accepted: 15 October 2018Published: 29 October 2018Publishing services provided byKnowledge EA. A. Betekhtina and D. V.Veselkin. This article isdistributed under the terms ofthe Creative CommonsAttribution License, whichpermits unrestricted use andredistribution provided that theoriginal author and source arecredited.Selection and Peer-reviewunder the responsibility of theEcology and Geography ofPlants and Plant CommunitiesConference Committee.Ecology and Geography of Plants and Plant Communitiesinvasive species, including Acer negundo L. and Amelanchier spicata (Lam.) K. Koch. Itwas important for us to reveal the morphological traits associated with the suggestedhigh growth rate. Such traits can be found in both above- and below-ground plantorgans [2, 3].As far as below-ground organs are concerned, the strategic characteristics ofplants are associated mainly with the root cortex [4], more specifically with the mostmetabolically active tissue such as cortex parenchyma [5]. Usually, thicker roots witha greater number of cortex parenchyma cell layers and higher tissue density requiremore energy and nutrients, grow slower and live longer [4, 6]. In contrast, the rootsof fast-growing species have a high specific root length (SRL) and a small number ofcell layers; therefore, they are able to grow faster and intercept resources [7]. Invasiveplants have been shown to have a high SRL as well [8], which means that their rootsare energetically cheap to produce [4]. Although SRL strongly correlates with rootdiameter [9], it is usually calculated for all roots less than 1 mm in diameter which arefunctionally divergent: this does allow for an accurate comparison. The data on fineroot diameter are limited; it has been shown to be the same [10, 11], smaller [12] orgreater [14, 15] in invasive plants than in native species. Such a difference betweenstudies could be due to the analysis of either taxonomically or ecologically distinctplant species.The aim of the present study was to compare several morphological and anatomicaltraits between (i) functionally homogeneous absorbing roots with primary develop-ment and (ii) taxonomically close invasive and native species growing in the sameconditions. This will reduce methodological, taxonomic and ecological effects.2. Methods2.1. Plant speciesWe selected two invasive species, box elder (Acer negundo L.) and low juneberry(Amelanchier spicata L.), shown to be invasive in Europe [16], Russia [17] and theCentral Urals [18]. For comparison, two native species were studied: Norway maple(Acer platanoides L.) and rowan (Sorbus aucuparia L.). Both species are rather commonin the Central Urals, where the samples were collected.DOI 10.18502/kls.v4i7.3217 Page 35Ecology and Geography of Plants and Plant Communities2.2. Study sitesThe roots were collected in Ekaterinburg, a city in the south taiga zone with a temper-ate continental climate. To measure stable morphological and anatomical characteris-tics, two sites were chosen; an additional sampling from a third site was performedto analyse arbuscular mycorrhizal (AM) colonization as a more variable feature. In allsites, invasive and native species grew together or in close proximity to each other.2.3. Sampling and morphological analysisRoot fragments were sampled during June and July in 2015, from 5–15 cm deep for fiveplants of each species at each sampling site. Only the live roots of two–three distalorders were selected and fixed in 70% ethanol. For each plant, 5–10 intact apical rootswere transversally cut into sections 15–20 µm in depth on a freezing microtome. Thefollowing parameters were then determined: root diameter, central cylinder diameter,the thickness of the cortex parenchyma, number of cortex parenchyma cell layers andparenchyma cell diameter. Only parenchyma cells without any cell wall thickeningwere analysed. Additionally, the abundance of AM fungi was assessed in 15 randomroot segments 1 cm in length and isolated from the roots of two distal orders. Thesesegments were macerated in KOH for 1 hour, then coloured with aniline blue and usedto make squash preparations. For each segment, five fields of view were inspectedwith a Leica DM 5000 microscope (Leica, Germany) at 100x magnification to measurethe proportion of the field of view covered by (1) AM hyphae; (2) arbuscles; (3) vesi-cles; (4) dark septate endophytes (DSE); and (5) root hairs.Statistical analysis was carried out using the package STATISTICA 8.0 with three-factors ANOVA. In all cases, individual plants were used as experimental units.3. ResultsIn this study, we analysed the influence of three main factors: invasive status (inva-sive/native), plant family (Sapindaceae/Rosaceae) and sampling site. The commonfeature of all absorbing roots of the studied species was a high mean proportion of thecortex, 95–96%, and a small mean diameter of the central cylinder, 60–76 μm. A highproportion of the cortex is probably needed for the interaction with fungal symbiontssince all the species were mycorrhizal.DOI 10.18502/kls.v4i7.3217 Page 36Ecology and Geography of Plants and Plant CommunitiesThe number of cortex parenchyma cell layers depended on plant family: the rootsof Rosaceae plants usually had two layers of parenchyma cells while the roots of Acersp. had two or three layers. It is worth noting that the roots of A. negundo had threecell layers significantly more frequently, but not more than 8% overall.The abundance of AM fungi, DSE and root hairs differed depending on the site;root hair abundance in Sapindaceae species was significantly higher, which could be afamily-specific trait. No clear association between invasive status and AM abundancewas found, except for a higher abundance of AM hyphae, vesicles and arbuscles in theroots of the invasive species A. negundo (15–75% in different sites) compared with thenative A. platanoides (11–35%). A. spicata and S. aucuparia had a similar AM abundance,but in A. spicata this feature differed more strongly between sampling sites. The factthat the abundance of AM fungi depends on the site rather than other factors is inline with the current conception of symbiosis as a tool that allows the fine tuning ofabsorbing roots to function in specific soil conditions [15].Root diameter varied depending on the site and plant family but was greater in thespecies of Sapindaceae (Figure 1). Most importantly, the roots of invasive species werethicker by 10%, mainly due to larger cortex parenchyma cells (Figure 1), and partly dueto a larger number of cell layers in A. negundo. The ANOVA interactions of the ‘invasivestatus’ factor together with ‘plant family’ or ‘sampling site’ were not significant for thisparameter (Table 1).Thus, the absorbing roots of two invasive and two native species that are bothtaxonomically and ecologically related differed in root diameter, the thickness of theroot cortex parenchyma and parenchyma cell diameter. Invasive A. negundo and A.spicata had thicker roots with a thicker parenchyma formed by larger cells. Theseresults are supported by the fact that A. negundo has thicker roots compared to thenative Acer species in the Southern Urals [15]; a similar pattern has been shown for theinvasive species Heracleum sosnowskyi [14, 15]. However, our results do not correspondwith the previous studies showing the same or thinner roots [10–12] or a higher SRL [8]in invasive plants. We found that rootswithmore parenchyma cell layers (three vs two)were significantly more frequent in invasive A. negundo than in native A. platanoides:however, since this frequency did not exceed 8%, we cannot claim that invasive andnative plants significantly differ in the metabolic cost of root growth. Although we didour best to reduce all the effects of the choice of samples and methods, the data arestill insufficient to make any clear conclusion.The question is how a thicker cortex parenchyma with larger cells would contributeto invasion success. We think that large parenchyma cells with a large central vacuoleDOI 10.18502/kls.v4i7.3217 Page 37Ecology and Geography of Plants and Plant CommunitiesT 1: ANOVA F-values for several parameters of absorbing roots calculated for the three main factorsand their interactions.Parameter Factor Factor Interactions R2𝑎𝑑𝑗InvasiveStatus(dF = 1) [1]PlantFamily(dF = 1) [2]SamplingSite [3][1] × [2] [1] × [3] [2] × [3]Root diameter § 7.65∗∗ 12.76∗∗∗ 17.96∗∗∗ 0.41 0.30 15.00∗∗∗ 0.54Central cylinderdiameter §3.84 0.06 1.97 0.05 0.01 4.44∗ 0.10Cortex parenchymathickness §13.65∗∗∗ 6.46∗ 14.05∗∗∗ 0.05 0.27 4.11 0.44Number of cell layers § 7.49∗ 60.28∗∗∗ 6.85∗ 1.79 0.11 6.05∗ 0.66Cell diameter § 5.51∗ 2.49 5.95∗ 1.51 0.16 0.71 0.24Abundance of AMhyphae §§3.66 2.50 41.60∗∗∗ 1.93 2.39 2.99 0.61Arbuscles §§ 0.39 5.84∗ 37.24∗∗∗ 0.44 1.33 4.20 0.59Vesicles §§ 2.58 0.35 8.94∗∗∗ 0.87 4.55∗ 0.01 0.28DSE §§ 1.49 0.04 7.33∗∗ 0.01 3.80∗ 4.79∗ 0.39Root hairs §§ 1.81 15.88∗∗∗ 3.88∗ 0.79 1.06 2.30 0.36Source: Authors’ own work.Note: # dF = 1 for root diameter, central cylinder diameter and parameters of the cortex parenchyma;dF = 2 for the other parameters. The following transformations were made for ANOVA: §x’ = ln (x+ 1); §§ x’ = asin (sqrt (x)). Statistical significance of F-values: ∗P < 0.05, ∗∗P < 0.01, ∗∗∗P < 0.001.F-values for the interaction of all three factors are not shown. R2𝑎𝑑𝑗 – R2 adjusted for the full ANOVAmodel.could optimize their water and nutrient uptake by substantially reducing cell respi-ration [5]. Moreover, the presence of large intercellular spaces in such parenchymatissue could be an additional factor minimizing root respiration. The positive correlationbetween the size of parenchyma cells and growth rate seems to be universal, as it hasbeen shown for photosynthetic tissues of fast-growing plants as well [2].4. ConclusionOur results suggest that the same or even lower thickness of the absorbing roots ofinvasive plants, shown previously might be inferred while comparing an integral valuesuch as SRL; also, the plants studied differed not only in invasive status but also in theirtaxonomic position or habitat. Whenwe compared both taxonomically and ecologicallyclose species using a directly measured value, the diameter of absorbing roots withprimary development, the roots of invasive plants turned out to have a thicker cortexparenchymawith larger cells. We suggest that this could contribute to invasion successby reducing root respiration, but data proving a higher growth rate in the roots ofinvasive species are still insufficient.DOI 10.18502/kls.v4i7.3217 Page 38Ecology and Geography of Plants and Plant CommunitiesFigure 1: Comparison of the studied features of absorbing roots between invasive and native species ofSapindaceae (∘) and Rosaceae (•) families. Mean values and standard errors are shown. Source: Authors’own work.AcknowledgementThe authors are grateful to Dr L. A. Ivanova (Botanical Garden, Ural Branch of RAS,Ekaterinburg, Russia) for her valuable comments.FundingThe part of the project headed by Dr Anna Betekhtina was supported by the Ministryof Education and Science of the Russian Federation within the framework of the stateDOI 10.18502/kls.v4i7.3217 Page 39Ecology and Geography of Plants and Plant Communitiesassignment No. 6.7696.2017/8.9. The part headed by Dr Denis Veselkin was performedwithin the State Contract of the Institute of Plant and Animal Ecology, UB RAS.References[1] van Kleunen, M., Weber, E., and Fischer, M. (2010). A metaanalysis of traitdifferences between invasive and noninvasive plant species. Ecology Letters, vol.13, no. 2, pp. 235–245.[2] Pyankov, V. I., Ivanova, L. A., and Lambers, H. (1998). Quantitative anatomy ofphotosynthetic tissues of plants species of different functional types in a borealvegetation, in Inherent Variation in Plant Growth. Physiological Mechanisms andEcological Consequences, pp. 71–87. 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Linking fine root traits to maximumpotential growth rate among 11 mature temperate tree species. Functional Ecology,vol. 18, no. 3, pp. 388–397.[8] Jo, I., Fridley, J. D., and Frank, D. A. (2017). Invasive plants accelerate nitrogen cycling:Evidence from experimental woody monocultures. Journal of Ecology, vol. 105, pp.1105–1110.[9] Ostonen, I., Püttsepp, Ü., Biel, C, et al. (2007). Specific root length as an indicator ofenvironmental change. Plant Biosystems, vol. 141, no. 3, pp. 426–442.[10] Craine, J. M. and Lee, W. G. (2003). Covariation in leaf and root traits for native andnon-native grasses along an altitudinal gradient in New Zealand. Oecologia, vol. 134,no. 4, pp. 471–478.DOI 10.18502/kls.v4i7.3217 Page 40Ecology and Geography of Plants and Plant Communities[11] Keser, L. H., Visser, E. J., Dawson, W., et al. (2015). Herbaceous plant species invadingnatural areas tend to have stronger adaptive root foraging than other naturalizedspecies. 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Russian Journal of Ecology,vol. 48, no. 4, pp. 303–310.[16] Delivering alien invasive species inventories for Europe (DAISIE), www.europe-aliens.org.DOI 10.18502/kls.v4i7.3217 Page 41Ecology and Geography of Plants and Plant Communities[17] Vinogradova, Yu. K., Mayorov, S. R., and Khorun, L. V. (2010). The Black Data Bookof Flora of Central Russia: Alien Species of Plants in the Ecosystems of Central Russia.Moscow: GEOS.[18] Tretyakova, A. S. (2011). Invasive potential of adventive plant species of the CentralUrals. Russian Journal of Biological Invasions, vol. 2, no. 4, pp. 281–285.DOI 10.18502/kls.v4i7.3217 Page 42

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Absorbing Roots of Invasive Woody Plants Apparently Have a Thicker Cortex Parenchyma Compared to Native Species

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