mechanisms of interaction between kalmia angustifolia cover and ...

Mechanisms of interaction between Kalmiaangustifolia cover and Picea mariana seedlings

Anna Wallstedt, Andrew Coughlan, Alison D. Munson, Marie-Charlotte Nilsson,and Hank A. Margolis

Abstract: Sites dominated by Kalmia angustifolia L. are often associated with slow decomposition of organic matter,decreased nitrogen (N) mineralization rates, and low black spruce (Picea mariana (Mill.) BSP) productivity. The objec-tive of this study was to separate the effects of belowground competition by Kalmia from the effects of water-solublesoil phenols on black spruce seedlings growing under different levels of Kalmia cover. A factorial greenhouse bioassaywas established in which black spruce seedlings were grown for 6 months in intact blocks of soil with three differentlevels of Kalmia cover. The soil was treated with charcoal to reduce the amounts of water-soluble phenols, and (or)tubes were inserted to exclude Kalmia roots. At low Kalmia cover, reducing the level of belowground competitionincreased seedling biomass by 134%. However, reducing belowground competition did not increase seedling biomass atthe two higher levels of Kalmia cover. It is possible that seedling biomass remained low because of an increasedimmobilization of N in the organic layer. Furthermore, the proportion of ectomycorrhiza morphotypes differed amongseedlings growing under different levels of Kalmia cover. The effect of water-soluble phenols on seedling growthremains uncertain, since we observed a confounding effect of the charcoal treatment on soil microbial biomass andseedling response.

Résumé : Les stations dominées par le Kalmia augustifolia L. sont souvent associées à une décomposition lente de lamatière organique, une diminution du taux de minéralisation de l’azote (N) et une faible productivité de l’épinette noire(Picea mariana (Mill.) BSP). L’objectif de cette étude consistait à séparer les effets de la compétition souterraine parle Kalmia des effets des composés phénoliques présents dans le sol et solubles dans l’eau sur des semis d’épinettenoire croissant sous différentes intensités de couverture de Kalmia. Un bio-essai factoriel a été établi en serre où dessemis d’épinette ont été cultivés pendant 6 mois dans des blocs de sol intact avec trois intensités différentes de couver-ture de Kalmia. Le sol a été soit traité avec du charbon activé pour réduire la quantité de composés phénoliquessolubles dans l’eau et (ou) des tubes ont été insérés dans le sol pour exclure les racines de Kalmia. Avec une faiblecouverture de Kalmia, la réduction du degré de compétition souterraine a augmenté la biomasse des semis de 134 %.La réduction de la compétition souterraine n’a cependant pas augmenté la biomasse des semis aux deux intensités lesplus fortes de couverture de Kalmia. Il est possible que la biomasse des semis soit demeurée faible à cause d’uneimmobilisation accrue de N dans l’horizon organique. De plus, la proportion de morphotypes d’ectomycorhizes différaitselon l’intensité de la couverture de Kalmia. L’effet des composés phénoliques solubles dans l’eau sur la croissance dessemis demeure incertain étant donné que l’effet du traitement au charbon activé sur la biomasse microbienne du sol etla réaction des semis n’était pas consistant.

[Traduit par la Rédaction] Wallstedt et al. 2031

Introduction

Experiences in Newfoundland have demonstrated that onsites dominated by Kalmia angustifolia L. after harvest, theregeneration of black spruce (Picea mariana (Mill.) BSP)can be significantly hindered (Titus et al. 1995). On thesesites, conifer seedlings grow slowly and have a chlorotic

appearance (Vincent 1965; Titus et al. 1993; Yamasaki1999; Mallik 2001). A survey of plantations in central New-foundland revealed that an increase in Kalmia cover wasassociated with a marked decrease in black spruce height(English and Hackett 1994). However, from this survey itwas not clear whether Kalmia caused the reduction in treeheight, or whether Kalmia was simply an indicator of poorsite quality (Titus et al. 1995). Kalmia, an ericaceous shrub,is suppressed by shade but shows vigorous growth andspreads rapidly after tree removal (van Nostrand 1971; Wall1977). It has even been suggested that failure to control Kal-mia after cutting may lead to a vegetation shift from forest toheathland, particularly on nutrient-poor sites (Mallik 1995).

Kalmia is also a common understory shrub species inblack spruce forests in Quebec. Since 1994, the governmentof Quebec recommends that where possible, harvest shouldbe carried out with a minimum soil disturbance to protectany preestablished natural regeneration (cut with protection

Can. J. For. Res. 32: 2022–2031 (2002) DOI: 10.1139/X02-124 © 2002 NRC Canada

2022

Received 25 July 2001. Accepted 20 June 2002. Published onthe NRC Research Press Web site at http://cjfr.nrc.ca on26 October 2002.

A. Wallstedt, A. Coughlan, A.D. Munson,1 andH.A. Margolis. Centre de recherche en biologie forestière,Université Laval, QC G1K 7P4, Canada.M.-C. Nilsson. Department of Forest Vegetation Ecology,Swedish University of Agricultural Sciences, SE-901 83Umeå, Sweden.

1Corresponding author (e-mail: [email protected]).

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of regeneration and soils). Consequently, the conditions forKalmia growth are improved, and the shrub may spread rap-idly (cf. Mallik 1994, 1995; Titus et al. 1995). Accumulatedexperience from Newfoundland suggests that silviculturaloperations such as trenching, scarification, or herbicide ap-plication are needed to at least temporarily control Kalmiagrowth after tree harvest so as to enable rapid establishmentof black spruce (Richardson 1979; Titus et al. 1995).

Sites dominated by Kalmia are often associated with slowdecomposition and low mineralization rates, and as a result,large quantities of nitrogen (N) are immobilized in a thick or-ganic layer (Damman 1971; Bradley et al. 1997a; Krause1998). Interestingly, in a study comparing N acquisition ofbirch (Betula papyrifera Marsh.), black spruce, and Kalmia,only Kalmia was capable of acquiring N from a spruce–Kalmiadominated soil (Bradley et al. 1997b). Bradley et al. (1997b)suggested that Kalmia may affect black spruce seedlinggrowth by producing high concentrations of leaf tannins,which when released from degrading litter in soil, control Navailability by binding proteins into recalcitrant complexes.Kalmia may also release water-soluble phenolic compoundsthat prevent normal root formation (Mallik 1987; Zhu andMallik 1994) and negatively affect the ectomycorrhizas asso-ciated with black spruce (Mallik and Zhu 1995; Yamasaki etal. 1998). However, it is potentially a combination of theseand other factors that limits growth of black spruce.

Although the negative effects of Kalmia on black sprucehave been thoroughly studied (e.g., Mallik 1987; Zhu andMallik 1994; Titus et al. 1995; Yamasaki et al. 1998), rela-tively little is known about the actual mechanisms causingthe reduction in spruce growth. The purpose of this studywas to separate the negative effects of belowground resourcecompetition by Kalmia from chemical interference causedby water-soluble phenols in Kalmia litter on black spruceseedling growth. We hypothesized that (i) Kalmia interfereswith black spruce seedling growth by competitive uptake ofnutrients; (ii) Kalmia releases water-soluble phenols, whichinhibit spruce seedling growth; and (iii) these negativeeffects are proportional to the amount of Kalmia cover.

Material and methods

Plant material and experimental setupIntact blocks of soil (54 × 35 cm) consisting of the organic

layer and the first 2 cm of the soil mineral layer were cutfrom an open black spruce stand, characterized by a continu-ous layer of feathermoss (Pleurozium schreberi (Bird.) Mitt.and Ptilium crista-castrensis (Hedw.) De Not.) and Kalmia inthe understory layer on a well drained sandy soil (Humo-Ferric Podzol; Soil Classification Working Group 1998) closeto Lac Grave (49°15′N, 73°42′W) in the AshuapmushuanWildlife Reserve, Quebec, on September 12, 1998. Theseblocks, or microcosms, were selected randomly from an ca.2000-m2 area and were then classified by ocular estimates ofKalmia cover so that we obtained 16 microcosms for each ofthree Kalmia cover classes: low cover (<20% cover), me-dium cover (21–40%), and high cover (41–60%). Obtaininga “true” control (i.e., no Kalmia cover) was not possible onthis site because of the amount of Kalmia regeneration. Themicrocosms were placed on a sheet of geotextile in individ-

ual plastic containers with drainage holes and transported toUniversité Laval in the city of Québec. The microcosmswere winterized outside for 3 months to allow the plants toachieve dormancy before being brought into the greenhouse.They were then acclimatized at 10°C (12 h of light) for2 weeks and at 15:10°C (day:night) with 14 h of light for1 week to simulate late spring conditions and induce plantflush. The temperature was increased to 20:15°C (day:night)with 16 h of light, and conditions were maintained at thesesummer levels throughout the experiment. The microcosmswere watered daily and Kalmia was allowed to grow for12 weeks before starting the bioassay with black spruceseedlings.

The experiment was set up as a factorial block designto compare 12 treatments consisting of all combinations ofthree levels of Kalmia cover class (low, medium, high), twolevels of charcoal treatment (no charcoal, charcoal), and twolevels of root competition (no tubes, tubes), replicated fourtimes. The charcoal treatment was used to decrease the con-centration of water-soluble phenols in the soil. A slurry ofactivated charcoal (Sigma-Aldrich Canada Ltd., CASNo. 7440-44-0, EINECS No. 231-153-3) (250 g in 3 L ofdistilled water, pH adjusted to 4.5 with HCl) was spreadover the soil surface in the eight charcoal treatment micro-cosms, randomly chosen from each Kalmia cover class treat-ment within each replicate (method modified from Nilsson1994). The charcoal had a negligible effect on the bulk den-sity of the soil, and a preliminary bioassay (data not pre-sented), in which aspen (Populus tremula L.) seedsgerminated and developed normally, confirmed that the char-coal was capable of detoxifying aqueous Kalmia leaf ex-tracts. Aspen seeds were used in this bioassay because oftheir greater sensitivity to phytotoxins and their more rapidresponse than conifer seeds (Zackrisson and Nilsson 1992).

The charcoal was allowed to penetrate the organic layerfor 2 weeks before root exclusion tubes (ABS pipes, 105 ×52 mm i.d.) were inserted to eliminate potential below-ground competition from Kalmia (see Nilsson 1994). Half ofthe charcoal-treated and half of the untreated microcosms ineach of the three Kalmia cover treatments were randomlychosen for the exclusion of root treatment. To apply thistreatment, three root exclusion tubes were installed along thecenter line (equally spaced) in each exclusion microcosm.This created four treatments within each level of Kalmiacover: (i) untreated microcosms (control), (ii) microcosmstreated with charcoal, (iii) untreated microcosms with rootexclusion tubes, and (iv) charcoal-treated microcosms withroot exclusion tubes. Four weeks after insertion of root ex-clusion tubes, one 8-week-old black spruce seedling grownfrom seed (collected at Lac Elaine, Roberval, Que., 1996,and germinated on moist oven-sterilized sand) was trans-planted into each root exclusion tube (i.e., three per micro-cosm). Three seedlings were also transplanted into each ofthe microcosms without tubes. The microcosms were thenmisted for 30 s every 2 h between 0600 and 2200 hoursdaily.

Since Kalmia may negatively affect spruce growth byshading, we also measured the proportion of photosyntheticphoton flux density (PPFD, µmol photons·m–2·s–1) incidenton each seedling, using two LI-COR quantum meters

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Wallstedt et al. 2023



(Model LI-250, LI-COR, Inc., Lincoln, Nebr., U.S.A.). Onewas placed above the Kalmia and the other next to the seed-ling. The PPFD incident on each seedling was then calcu-lated as the ratio of PPFD reaching the seedling to the PPFDmeasured above the Kalmia.

The black spruce seedlings were grown for 6 months andthen carefully harvested to minimize root damage. The intactseedlings were stored at –18°C. After seedling harvest, soilsamples from the F and H horizons were collected from eachmicrocosm for chemical analyses. There was not enough soilinside the tubes for chemical analysis, which would haveallowed us to more precisely describe the influence of Kal-mia roots on soil processes. Sampling soil from inside andimmediately outside tubes allowed us to make a comparisonwith microcosms without root exclusion tubes and to deter-mine the effect of disturbance of insertion on soil processes.Roots and dead branches (>1 mm) were removed, and thesoils from the H horizon sieved (2 mm). The soil from the Fhorizon was cut into 2-cm cubes and thoroughly mixed.Subsamples from both the F and H horizons were frozen forlater analysis of water-soluble phenols. Remaining soil waskept at 4°C until treated further.

Soil and plant analysesThe following analyses were carried out on soil samples:

(i) moisture content (dry mass basis) on a 10-g (wet mass)sample (60°C, 48 h); (ii) pH (3 g (wet mass) in 30 mL ofdeionized water); (iii) total N using a Kjeltec Auto 1030analyzer (Tecator Inc., Herndon, Va., U.S.A.) followingdigestion of a 0.5-g (dry mass) sample with 10 mL ofH2SO4–H2O2–Se (3:1:0.011, v/v/w) at 380°C for 1.5 h andafter adjusting the volume to 100 mL with distilled water;(iv) total P and K using a P40 Perkin-Elmer ICP analyzer(Perkin-Elmer, Norwalk, Conn., U.S.A.) following the samedigestion as described for total N; (v) proportion of extrac-table NO3-N and NH4-N, using a Lachat QuickChem 8000Automated Ion analyzer (Lachat Instruments, Milwaukee,Wis., U.S.A., Lachat Quickchem method Nos. 12-07-04-1Fand 10-107-06-2B) following extraction of a 2-g (dry mass)sample with 50 mL of 2.0 M KCl (Keeney and Nelson1982); and (vi) water-soluble phenols following extraction of50-g samples (wet mass) with 500 mL of distilled water un-der He in darkness at 4°C for 16 h, filtration, reaction withFolin Ciocalteau reagent, after which absorbance was re-corded at 760 nm using gallic acid (Sigma-Aldrich CanadaLtd., CAS No. 149-91-7, EINECS No. 205-749-9) as a stan-dard (Marigo 1973). The concentration of water-soluble phe-nols was expressed as micrograms gallic acid equivalents(GAE) per gram soil dry mass.

Soil microbial biomass was estimated in 5-g soil samples(stored for a maximum of 2 days) by determination ofmicrobial C using the chloroform fumigation–extractionmethod (Brookes et al. 1985). The soluble organic C wasanalyzed according to Heanes (1984) and converted to mi-crobial C by multiplying by a conversion factor of 2.64(Vance et al. 1987). Each estimate was duplicated. Determi-nation of soluble organic nitrogen (after the chloroformfumigation–extraction method) resulted in negative concen-trations; therefore it was not possible to determine microbialN. The N values may have been reduced because of incom-

plete oxidation of organic material in the extracts (N. Lukai,personal communication).

Black spruce seedlings were thawed and the root systemshydrated in distilled water. Afterwards, the total number ofmycorrhizal and non-mycorrhizal short roots were countedunder a dissecting microscope. Ectomycorrhizas (EM) wereclassified into distinct morphotypes based on macroscopicand microscopic features. The proportion of EM roots foreach seedling was calculated as the ratio of EM short rootsto the total number of short roots; because of a certain pro-portion of mortality, individual seedlings were used for sub-sequent analyses. Seedlings were then dried at 65°C for 72 hfor dry mass determination, but samples were unfortunatelytoo small for mineral content analysis, even if bulked withinthe experimental unit.

Statistical analysisAll data were checked for normality and homogeneity and

transformed using either the natural logarithm or the squareroot, if needed (see Tables 1 and 3), before analyses of vari-ance were performed using GLM. Since several spruce seed-lings lacked EM, we were unable to fit transformed data toa normal distribution for this variable. However, since theanalysis of variance using square root transformed valuesgave similar results to the analysis of ranked values, weassumed that the transformation gave an acceptable fit to themodel (Conover 1980). Analyses of seedling dry mass aswell as the proportion of EM roots were performed using themean squares from the interaction block × cover × charcoal ×tube as the error term. The level of significance was set at0.05 for main effects, 0.01 for first-order interactions, and0.001 for second-order interactions. Significant differencesbetween treatment means were determined using multiplecomparison (Fisher’s least-significant difference test). Least-square (LS) means and standard errors were detransformedaccording to the principles described by Ung and Végiard(1988). Pearson correlations were performed between theproportion of EM roots, seedling dry mass, and the propor-tion of PPFD reaching black spruce seedlings. Correlationsbetween Kalmia density and growth of black spruce or totalsoil nutrients were not revealing, since there were few pointswith very low cover. The statistical analyses were made us-ing SAS version 8 (SAS Institute Inc., Cary, N.C., U.S.A.).

Results

Soil propertiesThe treatments had little effect on measured soil proper-

ties (Table 1), and therefore the overall means of all treat-ments combined are presented in Table 2 to show differencesbetween the F and H horizons.

Relatively little of the total soil N was found as extrac-table mineral N. In the F horizon, only 0.50 ± 0.02%(mean ± SE, n = 48) of total N existed as NH4

+ and 0.10 ±0.01% as NO3

–, while in the H horizon the proportions were0.30 ± 0.02% and 0.15 ± 0.04% for NH4

+ and NO3–, respec-

tively. Furthermore, the concentration of total N in the Fhorizon was significantly higher at high levels Kalmia coverthan at low and medium levels (Fig. 1, Table 1). A similarbut nonsignificant (p = 0.117) trend was found for the con-

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2024 Can. J. For. Res. Vol. 32, 2002



centration of total N in the H horizon. In contrast, the con-centration of total K in the H horizon was significantlylower at high levels of Kalmia cover than at low and me-dium levels (Fig. 2, Table 1).

The concentration of water-soluble phenols in the F hori-zon in microcosms not treated with charcoal was 150 ±6 µg GAE·g–1 soil dry mass (LS mean ± SE), while the con-centration in the H horizon was 88 ± 6 µg GAE·g–1 soil drymass. The added charcoal effectively adsorbed and deacti-vated approximately 70% of these extractable phenolic com-pounds and results were highly significant (Fig. 3, Table 1).Besides decreasing the level of water-soluble phenols in soil,the charcoal treatment also had a significant negative effecton the microbial C biomass in the H horizon (Table 1),which at the end of the experiment was 1.2 ± 0.2 mg·g–1 soil

dry mass (LS means ± SE) compared with 2.0 ± 0.2 mg·g–1

soil dry mass in the nontreated microcosms.The insertion of root exclusion tubes affected only the

moisture content of the soil from inside and immediatelyoutside the tubes in the H horizon (at depth in microcosm),which significantly decreased from 381 ± 30% to 282 ± 22%(Table 1).

© 2002 NRC Canada


Source dfMoisturecontent pH N P K

ExtractableNH4-N

ExtractableNO3-N Phenols Microbial C

F horizonBlock 3 0.203 0.823 0.365 0.061 0.019* 0.033* 0.691 0.131 0.483Cover 2 0.538 0.308 0.017* 0.829 0.309 0.201 0.124 0.963 0.176Charcoal 1 0.074 0.415 0.455 0.765 0.228 0.482 0.659 <0.001* 0.275Tube 1 0.742 0.516 0.722 0.151 0.177 0.579 0.597 0.317 0.579Cover × charcoal 2 0.787 0.509 0.325 0.807 0.867 0.355 0.040 0.835 0.740Cover × tube 2 0.783 0.551 0.164 0.404 0.907 0.576 0.263 0.927 0.644Charcoal × tube 1 0.380 0.945 0.933 0.377 0.861 0.552 0.870 0.616 0.475Cover × charcoal × tube 2 0.840 0.308 0.514 0.141 0.015 0.792 0.521 0.944 0.023Error 33Total 47H horizonBlock 3 0.024* 0.539 0.429 0.499 0.004* 0.292 0.152 0.156 0.014*Cover 2 0.638 0.053 0.117 0.806 0.023* 0.507 0.544 0.352 0.942Charcoal 1 0.648 0.128 0.429 0.363 0.151 0.513 0.242 <0.001* 0.007*Tube 1 0.011* 0.682 0.892 0.460 0.806 0.560 0.209 0.110 0.125Cover × charcoal 2 0.807 0.813 0.585 0.241 0.974 0.468 0.473 0.303 0.824Cover × tube 2 0.350 0.431 0.564 0.960 0.230 0.471 0.351 0.642 0.768Charcoal × tube 1 0.783 0.869 0.893 0.333 0.159 0.125 0.407 0.346 0.472Cover × charcoal × tube 2 0.440 0.459 0.717 0.969 0.924 0.438 0.407 0.784 0.623Error 33

Total 47

Note: The values for K from the F horizon and the moisture content values for the H horizon were transformed using natural logarithms beforeANOVA. Asterisks show significant p values. Main effects, p ≤ 0.05; first-order interactions, p ≤ 0.01; second-order interactions, p ≤ 0.001.

Table 1. Degrees of freedom and p values from ANOVA on soil properties for the F and H horizons.

Soil characteristics F horizon H horizon

Moisture content (%) 497±17 —pH 4.08±0.03 3.99±0.03N (%) —a 0.61±0.03P (ppm) 636±19 475±17K (ppm) 665±51 —Extractable NH4-N (ppm) 35.1±1.1 17.9±8.9Extractable NO3-N (ppm) 6.8±3.0 8.9±2.6Phenols (µg·g–1) — —Microbial C (mg·g–1) 3.0±1.5 —

Note: Values are overall means ± SEs, expressed per soil drymass, n = 48.

aData not shown because significant treatment effects occurred.

Table 2. Soil characteristics of F and H horizons. Fig. 1. The effect of Kalmia cover class on total N (% of soildry mass) in the F horizon. The values are least-square meansand error bars are ±SE. Means with the same letter do not differat p ≤ 0.05 according to Fisher’s least significant difference test.



Black spruce seedling performanceIn general, the biomass of black spruce seedlings was low

(total plant mass = 15.9 ± 1.6 mg (mean ± SE, n = 136)).Kalmia cover class interacted with the root exclusion treat-ment (designed to reduce the level of belowground competi-tion), so that the total biomass (shoot and roots) of seedlingsgrown inside tubes was 134% greater than the biomass ofseedlings grown without tubes in the low Kalmia cover class(Fig. 4, Table 3). There was no effect on the shoot/root ratio(Table 3) and root exclusion tubes did not increase seedlingbiomass in the two higher Kalmia cover classes (Fig. 4).

Contrary to the positive effect of reduced belowgroundcompetition on seedling biomass, the charcoal treatment (de-signed to reduce the level of chemical interference) actuallydecreased seedling biomass by 34% compared with seed-lings in untreated microcosms (Fig. 5, Table 3). The seed-lings grown in charcoal-treated microcosms also allocatedrelatively more resources to roots than to shoots; the shoot/root ratio was 3.14 ± 0.23 compared with 4.07 ± 0.28 (LSmean ± SE) for seedlings grown in untreated microcosms(Table 3).

Seedling biomass was only slightly influenced by theamount of incident light. The proportion of PPFD incidenton the seedlings decreased from 32 ± 3% (LS mean ± SE) atlow levels of Kalmia cover to 24 ± 2% at the high levels ofKalmia cover (Table 3), but only 5% of the variability ofseedling dry mass could be explained by variation in inci-dent PPFD (p = 0.008). Seedling dry mass was also weaklycorrelated with the total proportion of EM roots (r2 = 0.048,p = 0.010).

The overall mean proportion of EM roots on the seedlingswas as low as 19% and ranged from 0 to 85% (Table 4).In total, we found five distinct mycorrhizal morphotypes,which for this study were named type A to type E (see Ta-ble 4 for description). Type D was most common and wasfound on 57 of the 137 surviving seedlings (i.e., 42%), while21 (i.e., 15%) of the seedlings had no EM at all. Type A wassignificantly more abundant on seedlings at low comparedwith high levels of Kalmia cover, while the opposite patternwas observed for type B (Fig. 6a, Table 3). The insertion ofroot exclusion tubes interacted with the charcoal treatmentfor the proportion of type B (Fig. 6b, Table 3). There was nocorrelation between the PPFD incident of the seedlings andthe proportion of EM roots.

Discussion

At low levels of Kalmia cover, root competition appearedto be an important factor controlling black spruce seedling

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2026 Can. J. For. Res. Vol. 32, 2002

Fig. 2. The effect of Kalmia cover class on total K (ppm of soildry mass) in the H horizon. The values are least-square meansand error bars are ±SE. Means with the same letter do not differat p ≤ 0.05 according to Fisher’s least significant difference test.

Fig. 3. The effect of the charcoal treatment (activated charcoalwas spread on the soil surfaces while nontreated soils were keptas controls) on the concentration of water-soluble phenols(µg gallic acid equivalents·g–1 dry mass soil) in the F and Hhorizons. The values are least-square means and error bars are±SE. For each soil horizon, means with the same letter do notdiffer at p ≤ 0.05 according to Fisher’s least significant differ-ence test.

Fig. 4. The effect of Kalmia cover class on black spruce seed-ling dry mass (mg) when growing inside root exclusion tubes orin soil without tubes. The values are least-square means anderror bars are ±SE. Means with the same letter do not differ atp ≤ 0.05 according to Fisher’s least significant difference test.



growth (Fig. 4). The fact that the shoot/root ratio was not af-fected (Table 3) suggests that the relative resource allocationto shoots and roots was not influenced by this treatment. It isnot surprising that Kalmia was found to be an effectivebelowground competitor, since this is generally the case forother ericaceous species, at least on nutrient-poor sites (e.g.,Mallik 1995; Titus et al. 1995; Prescott et al. 1996; Alonsoand Hartley 1998; Hartley and Amos 1999). In addition,Kalmia has a very extensive system of fine roots, virtuallyforming a felt in the H horizon. The organic horizon of aKalmia heath may contain as much as 13 600 kg/ha of rootsand rhizomes less than 1 cm in diameter (Damman 1971).Smith et al. (2000) also found that Kalmia roots largelydominated the organic horizon in recently burnt or harvestedblack spruce forests in central Quebec. However, since re-ducing belowground competition did not increase seedling

biomass at the two higher levels of Kalmia cover class, thereseems to be some additional factor(s) that also suppressedblack spruce seedling growth. The lack of a true control(i.e., microcosms with no Kalmia cover) may also contributeto the weak relationships observed in the study.

Zhu and Mallik (1994) found several phenolic compoundsin aqueous extracts of fresh Kalmia leaves and demonstratedin a bioassay that these compounds have the potential toprevent normal root formation of black spruce germinants.However, it is uncertain whether these phenolic compoundsever reach inhibitory concentrations in the soil. In an earlierstudy, Inderjit and Mallik (1999) determined that the totalconcentration of water-soluble phenols was approximately140 µg·g–1 soil dry mass in the organic layer from a blackspruce forest with a Kalmia-dominated understory. This is inthe same range as the concentration of water-soluble phenolsthat we found in the F horizon not treated with charcoal(Fig. 3). Our hypothesis was that at least part of the ex-tracted phenolic compounds originated from Kalmia, and asa consequence, their concentration should be related to Kal-mia cover. However, this was not the case (Table 1), perhapsbecause degradation (or immobilization) of the phenolicswas not proportional to their rate of input at different levelsof Kalmia cover (cf. Dalton et al. 1983; Blum et al. 1999).

It is not clear why the addition of charcoal to soil de-creased spruce seedling biomass (Fig. 5), even though it de-creased the concentration of water-soluble phenols in soilby as much as 70%. The preliminary bioassay using aspenseeds confirmed that the charcoal itself was not inhibitoryto seed germination and growth and that it adsorbedphytotoxins (data not shown). The fact that seedlings incharcoal-treated microcosms allocated relatively more bio-mass to roots might indicate that they were under higher nu-trient stress than seedlings in the nontreated microcosms(Ericsson 1995). Pietikäinen et al. (2000) suggested thatcharcoal adsorbs not only dissolved phenolic compounds butalso other organic compounds (e.g., carbohydrates, aminoacids, and organic acids), although this has not been demon-strated in the field. By adding charcoal, we thus might haveremoved some of the C available to soil microorganisms, as

© 2002 NRC Canada


Seedling dry mass Mycorrhiza short roots

Source df PPFDa Totalb Shootb RootaShoot/rootratioa Totala

TypeAa

TypeBa

TypeCa

TypeDa

TypeEa

Block 3 0.002* 0.341 0.308 0.611 0.739 0.823 0.647 0.090 0.088 0.812 0.129Cover 2 0.042* 0.000 0.000 0.001 0.173 0.206 0.042* 0.045* 0.528 0.262 0.116Charcoal 1 0.846 0.002* 0.002* 0.097 0.015* 0.052 0.242 0.551 0.152 0.987 0.769Tube 1 0.974 0.390 0.530 0.122 0.334 0.864 0.678 0.888 0.781 0.795 0.439Cover × charcoal 2 0.277 0.119 0.144 0.207 0.747 0.421 0.394 0.668 0.663 0.406 0.371Cover × tube 2 0.739 <0.001* 0.001* 0.003* 0.385 0.341 0.794 0.336 0.475 0.511 0.608Charcoal × tube 1 0.509 0.852 0.701 0.564 0.245 0.763 0.424 0.005* 0.432 0.625 0.651Cover × charcoal × tube 2 0.984 0.920 0.884 0.833 0.561 0.683 0.731 0.012 0.622 0.346 0.791Error 33Total 47

Note: Asterisks indicate significant p values. Main effects, p ≤ 0.05; first-order interactions, p ≤ 0.01; second-order interactions, p ≤ 0.001. See Table 4for definition of mycorrhiza morphotypes.

aData were transformed using the square root.bData were transformed using the natural logarithm.

Table 3. Degrees of freedom and p values from ANOVA on the amount of incident light (PPFD) reaching black spruce seedlings,seedling dry mass, and the proportion of EM roots.

Fig. 5. The effect of the charcoal treatment (activated charcoalwas spread on the soil surfaces while non-treated soils were keptas controls) on black spruce seedling shoot and total dry mass(mg). The values are least-square means and error bars are ±SE.For each plant part, means with the same letter do not differ atp ≤ 0.05 according to Fisher’s least significant difference test.



well as organic nutrients used directly by spruce seedlings(Näsholm et al. 1998). Soil microorganisms in Kalmia hu-mus can be C limited (Bradley et al. 1997a), and a furtherdecrease in available C might have negatively influenced themicrobial biota. This might explain why the microbial Cbiomass was lower in the charcoal-treated H horizon than inthe nontreated soil.

The addition of activated charcoal may have affected thesoil microbial communities in other ways. Analysis of thecharcoal used in this study showed that it contained 2270 ±103 ppm total N, 117 ± 19 ppm total P, and 70 ± 26 ppmtotal K (mean ± SE, n = 3) of which only trace amountswere released when the powder was shaken in water (datanot shown). If bacteria can access these mineral nutrients,then both microbial biomass and activity (not measured)could have been altered by the addition of nutrients (cf.Bååth et al. 1981; Söderström et al. 1983; Smolander et al.

1994; Insam and Palojärvi 1995; Hart and Stark 1997). Thecharcoal itself may also support microbial communities andinduce changes in the microbial communities of the sur-rounding humus (Zackrisson et al. 1996; Pietikäinen et al.2000).

We therefore suggest that the charcoal treatment may haveinhibited black spruce seedling growth, either directly, bylimiting available organic nutrients in soil by adsorption onthe charcoal, or indirectly, via an effect on soil microorgan-isms. Foliar nutrient data could have confirmed the nutritioneffect, but unfortunately tissue samples were insufficient foranalyses. As a consequence, the charcoal treatment failed toevaluate the effect of water-soluble phenols in soil on blackspruce seedling growth. If the decrease in free phenoliccompounds in soil did have a positive effect on seedling bio-mass, this effect was masked by the negative effect of theadded charcoal itself.

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2028 Can. J. For. Res. Vol. 32, 2002

Type CharacteristicsOverall meanproportion*

No. ofplants

Meanproportion†

A Ascomycete, purplish black, 2–4 mm, unbranched, mantle 18 µm, hyphae 3–4 µm, netto felt prosenchyma, rhizomorphs 100 µm

0.067±0.012 41 0.225±0.027

B Ascomycete, light brown, 1.5–2 mm, club-shaped, unbranched, mantle 12 µm, hyphae4 µm, net prosenchyma

0.034±0.008 28 0.177±0.032

C Ascomycete, brown, 3–4 mm, unbranched, mantle 24 µm, hyphae 6–8 µm, netsynenchyma

0.014±0.005 12 0.155±0.047

D Ascomycete, reddish brown, 4–5 mm, unbranched, mantle 18 µm, hyphae 3 µm,irregular synenchyma (interlocking)

0.066±0.011 57 0.159±0.020

E Basidiomycete, greyish brown, 3–4.5 mm, unbranched, mantle uniform and slightlywaxy in appearance with occasional cystidia, hyphae 2.5–4 µm, clamp connections,irregular synenchyma

0.009±0.003 10 0.122±0.028

Total 0.190±0.016

Note: Treatment effects are shown in Figs. 6a and 6b.*Twenty-one of the 137 surviving plants had no ectomycorrhizas.†Ratio of EM short roots to total number of short roots.

Table 4. Characteristics, overall mean proportion (mean ± SE, n = 137), number of plants with, and mean proportion (mean ± SE, n =number of plants) of the five different ectomycorrhiza morphotypes identified on black spruce seedling roots.

Fig. 6. The effect on black spruce seedling ectomycorrhiza of (a) type A and B when grown in three different classes of Kalmia coverand (b) type B when growing inside root exclusion tubes or in intact soil and either treated with charcoal or left non-treated. The val-ues are least-square means and error bars are ±SE. For each ectomycorrhiza type, means with the same letter do not differ at p ≤ 0.05according to Fisher’s least significant difference test.



Investigation is needed to better understand the unantici-pated effects caused by charcoal addition to soil. Whenchoosing a suitable activated charcoal, we found that somecharcoals released significant amounts of minerals such asCa, Mg, and K when extracted with water and also signifi-cantly altered the pH of the solution. In this study, we ad-justed the pH of the charcoal slurry with HCl before addingit to the soil. If not, soil pH would have increased by aboutone unit. If charcoal is to be used in similar studies, cautionneeds to be taken to minimize possible secondary effects ofthe treatment.

The proportion of PPFD incident on the seedlings de-creased with increasing cover of Kalmia. However, the de-crease had little effect on seedling biomass. Instead, in thehigh Kalmia cover class, it is possible that black spruceseedling growth was inhibited by the immobilization of N inthe organic layer, resulting in higher total N concentration(Fig. 1). Ericaceous species are rich in polyphenols (e.g.,tannins) (Iason et al. 1993; Titus et al. 1993; Northup et al.1998; Gallet et al. 1999), which may function as generalmicrobial inhibitors (Schimel et al. 1996) and shift the domi-nant pathway of soil N cycling from mineral to organicforms by forming recalcitrant complexes with proteins(Hobbie 1992; Northup et al. 1995, 1998; Schimel at al.1998; Hättenschwiler and Vitousek 2000). Since tannins arebelieved to complex-bind proteins in senescent tissue(Kuiters 1990, 1991; Hernes and Hedges 1999) and alsoappear to adsorb tightly to soil (Schofield et al. 1998;Preston 1999), it is possible that this nonextractable fractionof tannins caused immobilization of N in the soil. Bradley etal. (2000) found that the leaching of NH4-N and NO3-Nfrom black spruce humus decreased after the addition ofcondensed tannins isolated from Kalmia foliage. However,no tannins were detected in soil leachates, and only 1% ofthe added tannins was recovered from the humus at the endof the incubation period, suggesting that the tannins hadbecome immobilized in soil or were metabolized by soilmicrobiota (Bradley et al. 2000). Free tannins are usuallyeffectively adsorbed on activated charcoal (Mohan andKarthikeyan 1997) and may also constitute a large part ofthe fraction we quantified as water-soluble phenols (cf.Waterman and Mole 1994). However, the charcoal treatmentdid affect the concentration of total N in soil. We did not ob-serve an accompanying decrease in extractable N, but thissingle measure of mineral N may not provide an optimumindication of N availability over the duration of the experi-ment.

Kalmia would likely gain a competitive advantage overspruce seedlings by immobilizing N in the organic layer,since ericoid mycorrhizas (which colonize Kalmia roots) areconsidered to have a greater capacity to make use of organicN than EM fungi (Bending and Read 1996; Michelsen et al.1996). This advantage would further increase if Kalmia, assuggested for Calluna vulgaris L., another ericaceous plant,secretes substances that are toxic to EM fungi but not to itsown mycorrhizas (Robinson 1972). Yamasaki et al. (1998)found that black spruce seedlings growing close to Kalmiavegetation (<1 m away) not only had a lower proportion ofEM roots, but also were more frequently associated withPhialocephala dimorphospora Kendrick, a potential rootpathogen, than seedlings growing further away from Kalmia.

Furthermore, Mallik and Zhu (1995) found that aqueousKalmia leaf extracts (containing phenolic acids) were toxicto several EM isolates. In our study, the overall mean pro-portion of EM roots on black spruce seedlings was very low(see Table 4), possibly because of the small biomass of theseedlings (McAfee and Fortin 1989). However, there arestudies that show that even roots from small seedlings maybe quickly colonized by EM in natural soils (cf. Smith et al.1995; Zackrisson et al. 1997). We were unable to determinewhat caused the observed difference in the proportion oftype A and type B EM on spruce roots with different classesof Kalmia cover (Fig. 6a). The difference does not seem tobe related to the concentration of water-soluble phenols insoil, since the concentration itself was not influenced by theKalmia cover (Table 1) and the charcoal treatment did notinteract with Kalmia cover on the proportion of EM roots(Table 3).

Lower concentrations of total K in the H horizon at highlevels of Kalmia cover (versus low and medium cover) maybe related to immobilization of K in the vegetative biomassof Kalmia. Damman (1971) found that the raw humus ofboth fir and spruce forests contained more K than the rawhumus from a Kalmia heath. On the other hand, Mallik(2001) found that black spruce from Kalmia sites containedhigher quantities of K in the needles than seedlings fromnon-Kalmia sites.

Conclusion

We found that belowground competition was an importantfactor contributing to suppression of black spruce seedlingbiomass at low levels of Kalmia cover, while other factor(s)seemed to be more important at high levels of Kalmia cover.The effect of water-soluble phenols in soil on black spruceseedling growth remains uncertain. The charcoal treatmentreduced the level of water-soluble phenols in soil but, con-trary to our hypothesis, also inhibited black spruce seedlingbiomass. It is possible that Kalmia influenced nutrient acqui-sition and seedling growth by immobilizing N in the organiclayer and also by influencing the composition of EM fungion black spruce seedling roots.

Acknowledgments

We thank Chantal Morin, Alain Brousseau, andRéal Mercier for help with the soil analyses. We also thankAndré Beaumont for help in the field, Hélène Crépeau forhelp with the statistical analysis, and Christiane Gallet formany valuable comments. Two anonymous reviewers pro-vided valuable comments to improve the quality of themanuscript. This work was made possible by the financialsupport from the ministère de l’Éducation du Québec (post-doctoral fellowship to Anna Wallstedt) and the Network ofCentres of Excellence in Sustainable Forest Management(project of Alison Munson).

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