Butt rot incidence, causal fungi, and related yield loss in Picea abies stands of Latvia

Butt rot incidence, causal fungi, and related yieldloss in Picea abies stands of Latvia

N. Arhipova, T. Gaitnieks, J. Donis, J. Stenlid, and R. Vasaitis

Abstract: Root and butt rot is the most destructive disease of conifers in the Northern Hemisphere, but little is known aboutthe dynamics of yield loss in stands of different ages, site types, and species composition. This study aimed to estimate buttrot incidence, causal fungi, and related wood yield loss in Picea abies (L.) H. Karst. stands in Latvia. A total of 24 745stumps were examined on 318 forest sites, and 21.8% of them contained rot. There was a positive correlation between standage and butt rot frequency. Proportion of other tree species in a stand had no influence on incidence of the rot, but signifi-cant differences were observed among different forest site types. The length of decay columns in 114 stems analysed was6.6 ± 2.6 m on average. Based on the observed butt rot frequencies in Latvian P. abies stands of different age classes, vol-umes of decay-degraded wood in a fully stocked stand would comprise about 19.7 m3·ha–1 at the age of 40 years,57.4 m3·ha–1 at 60 years, 54.9 m3·ha–1 at 80 years, 63.1 m3·ha–1 at 100 years, and 91.8 m3·ha–1 at 120 years, correspondingto 6%–16% of a total standing volume.

Résumé : Le pourridié est la maladie la plus dommageable chez les conifères dans l’hémisphère nord mais la dynamiquedes pertes de rendement selon l’âge, le type de station et la composition en espèces est peu connue. Cette étude visait à dé-terminer l’incidence du pourridié, les champignons responsables et la perte de rendement en matière ligneuse dues à cettemaladie dans les peuplements de Picea abies (L.) H. Karst. en Lettonie. Au total, 24 745 souches ont été examinées dans318 stations et 21,8 % contenaient de la carie. Il y avait une corrélation positive entre l’âge du peuplement et la fréquencedu pourridié. La proportion d’espèces compagnes dans le peuplement n’avait pas d’influence sur l’incidence de la cariemais des différences significatives ont été observées entre les différents types de station. La colonne de carie avait une lon-gueur moyenne de 6,6 ± 2,6 m dans les 114 tiges qui ont été analysées. En se basant sur la fréquence observée du pourridiédans les peuplements de P. abies de différentes classes d’âge en Lettonie, le volume de bois carié dans un peuplement avecune densité relative adéquate serait respectivement d’environ 19,7, 57,4, 54,9, 63,1 et 91,8 m3·ha–1 à l’âge de 40, 60, 80,100 et 120 ans, ce qui correspond à 6–16 % du volume sur pied.

[Traduit par la Rédaction]

Introduction

Butt and stem rots are the most economically importantdiseases of Picea abies (L.) H. Karst. in Europe, especiallyin managed forests where cut stumps and wounds on livingstems are abundant. In particular, the most destructive patho-gens from the genus Heterobasidion spp. are favoured by for-est management (Woodward et al. 1998). So far, these fungiwere identified as the principal causal agents of butt rot ofP. abies in different parts of northern and central Europe(Pechmann and Aufsess 1971; Kallio and Tamminen 1974;Hallaksela 1984). As butt rot caused by Heterobasidion spp.is common, in some studies, butt rot of P. abies was attrib-uted to Heterobasidion based solely on visual stump assess-ment (Enerstvedt and Venn 1979; Nilsen 1983; Vasiliauskaset al. 2002). Yet, it is known that many other decay fungican cause butt rot in living P. abies, including Stereum san-guinolentum, Armillaria spp., Amylostereum spp., Porodae-dalea chrysoloma, Coniophora puteana, Resinicium bicolor,Postia spp., Sistotrema brinkmannii, and Climacocystis bor-

ealis (Pechmann and Aufsess 1971; Norokorpi 1979; Hallak-sela 1984). Moreover, butt rot pathogens of P. abies mightvary considerably even between neighbouring geographicalregions, depending on stand age, site characteristics, andmanagement history, as reported from Germany (Pechmannet al. 1973) and Finland (Kallio and Tamminen 1974; Noro-korpi 1979).Despite numerous studies on butt and stem rot causing

fungi, few published works have attempted to estimate thewood yield loss caused by the disease in P. abies stands.The results show that losses might be significant, dependingon infection frequency. For example, an inventory of P. abiesstands in southern Finland demonstrated that the decrease insawn timber volume due to butt rot varied from 0% to 37%and was 8.5% on average (Tamminen 1985). Earlier, more lo-cally conducted Finnish studies reported sawn timber volumereduction by 21.5% (Kallio and Tamminen 1974) and 30%(Kallio 1972). In stands where wounded trees are present,yield loss might also be significant, depending on a numberof wounded trees, time since the damage occurred, stand age,

Received 13 July 2011. Accepted 12 September 2011. Published at www.nrcresearchpress.com/cjfr on 15 November 2011.

N. Arhipova, T. Gaitnieks, and J. Donis. Latvian State Forest Research Institute “Silava”, P.O. Rigas 111, Salaspils, Latvia, LV 2169.J. Stenlid and R. Vasaitis. Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, P.O. Box7026, SE – 750 07 Uppsala, Sweden.

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

2337

Can. J. For. Res. 41: 2337–2345 (2011) doi:10.1139/X11-141 Published by NRC Research Press

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and productivity. For example, in a productive (bonität I),fully stocked (1.0), 80-year-old P. abies stand containing40% of stems with 30-years-old wounds, 10% of the volumewill be reduced from high quality (butt) sawlog to decayedfirewood (Vasiliauskas 2001).Apparently, in light of disease importance, available data

on root and butt rot dynamics are scarce, and little is knownon its dynamics and caused yield loss in stands of differentages, site types, and species composition and with differentfrequencies of infection. If made available, such informationcould be applied on a wide scale and used for optimizing ofmanagement of P. abies stands in Europe. The aims of thisstudy were (i) to estimate butt rot frequency in LatvianP. abies stands, (ii) to determine the extent to which diseaseis related to stand characteristics, e.g., age, site type, speciescomposition, (iii) to estimate related wood yield losses, and(iv) to identify fungi that cause butt rot and stem decay.

Materials and methods

FieldworkThe study was conducted in 2005 and 2006 in P. abies

stands throughout Latvia (Fig. 1). The fieldwork included (i)estimating the frequency of and measuring butt rot in stumpsof P. abies on thinned and clear-felled forest sites, (ii) fellingand dissecting decayed stems and measuring decay parame-ters, and (iii) sampling decayed stumps and living stems forthe subsequent isolation of fungi. The criteria for selectingforest sites were dominance of P. abies (>50% standing vol-ume) and recent wood harvesting, thinning, or clearcutting(≤3 years; the goal was to record butt rot present in a livingstem prior to felling). Information on the availability of suchP. abies stands in Latvia was obtained from the database ofLatvian State Forests (I. Brauners, personal communication,2005, 2006), and the most accessible sites in 23 Latvian re-gions were included into the present work. The inventory wascarried out in 149 thinned and 169 clear-felled sites. Thesites represented Oxalidosa (102), Hylocomiosa (86), Myrtil-losa (67), and Mercurialiosa (37) forest types on mediumrich mineral soil and Caricoso-phragmitosa, Oxalidosa turf.mel., and Myrtillosa turf. mel. (27) forest types on drainedpeat of poor fertility (Bušs 1997). Age of cut stands variedfrom 27 to 164 years, and area varied from 0.2 to 8.7 ha. Ofall evaluated stands, 82 (26%) were pure P. abies stands, 189(59%) were P. abies dominated stands with 10%–30% otherspecies, and 47 (15%) were stands with 40%–50% other spe-cies. The other species were P. sylvestris and deciduous spe-cies (mainly Betula spp., Populus tremula, Alnus glutinosa,Alnus incana, Fraxinus excelsior, and Quercus robur).In total, 24 745 P. abies stumps were examined during the

current study, 15 to 240 stumps per site, depending on standarea (Table 1). A randomly oriented transect ~10 m wide wasmade across each site over the centre (Bloomberg et al.1980). Within each transect, after examination of the firststump, the next closest stump was subjected to examination,and so on. All stumps were surveyed for presence or absenceof butt rot and their diameters were measured in one (pre-sumed average) direction using a ruler. In doubtful cases, thestump was double checked by cutting a piece of wood 3–5 cm deep out of a stump using an axe and evaluating woodcondition (decayed vs. nondecayed) in more detail. The di-

ameter of stumps examined varied from 5 to 120 cm. Stumpswere classed in two categories, “healthy” or “butt rot”. Foreach butt rot stump, the cross-sectional area of decay wasmeasured, and all butt rot stumps were divided into four cat-egories according to stage of wood decomposition: 1, discol-oration (colour change without changes in wood mechanicalproperties); 2, decay (colour change with moderate changesin wood mechanical properties); 3, advanced rot (strongchanges in wood mechanical properties; wood becomingvery soft, squeezable with fingers); and 4, hollow (wood iscompletely degraded in the centre of the decay column, form-ing a hollow). On each site, between one and 10 decayedstumps were randomly selected and bore cores were taken us-ing an increment borer. Cores were taken 2–4 cm below thestump surface and aimed at the centre of decay column forsubsequent isolations of decay-causing fungi from the cores.Each stump was sampled once, and a total of 1182 sampleswere taken from the same number of rotten stumps. The in-crement borer was sterilized by 70% ethanol before eachsampling.To estimate length of decay in stems, increment borer

cores were taken from the butt of randomly selected trees(without open wounds) on four forest sites and examined fordecay symptoms. A total of 114 trees containing decay werecut and dissected, and the following parameters were re-corded: tree height, tree diameter at stump level, tree DBH,decay diameter at stump level, decay diameter at DBH, andtotal length of decay. Discs were cut from these trees at thestem base (0.2–0.3 m), at breast height (1.3 m), at a heightof 2.3 m from the stump, and then continuing at 3 m inter-vals. The final length of the decay column was determinedto an accuracy of 10 cm using discs cut at shorter intervals.The discs from the tree base, middle, and top of the decaycolumn were numbered, placed into separate plastic bags,and brought to the laboratory for isolation of decay-causingfungi.

Isolation and identification of fungiImmediately after the sampling, bore cores were individu-

ally placed into sterile plastic Petri dishes and brought to thelaboratory. From the wood disks, small pieces of wood (ap-proximately 3 × 1 × 1 cm) were cut from the edge of thedecay column. Isolation was done on the day after the sam-

Fig. 1. Map of Latvia showing joint territory (in black) of adminis-trative forestry units investigated in the present study.

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pling, and the procedure closely followed those employed inour earlier studies (Vasiliauskas et al. 1996; Vasiliauskas andStenlid 1998). Each sample was flame-sterilized, placed onmalt agar medium (15 g bacto malt extract, 12 g agar,1000 mL distilled H2O), and incubated in the dark at 19 °C.For species identification, all isolates were individually sub-cultured on Hagem agar media (5 g glucose, 0.5 g NH4NO3,0.5 g KH2PO4, 0.5 g MgSO4·7H2O, 5 g malt extract, 20 gagar, 1000 mL distilled H2O at pH 5.5) in separate Petridishes. All pure cultures were examined under the micro-scope and grouped into mycelial morphotypes (219 groupsin total). From those, 11 species or genera were identifiedmicroscopically: Ascocoryne sarcoides, Aspergillus spp.,Cosmospora vilior, Cylindrocarpon dydimum, Gibberellaavenacea, Hormonema demantioides, Ophiostoma piceae,Penicillium spp., Trichoderma spp., Umbelopsis isabellina,and U. rammaniana. For identification of Heterobasidionspecies, intersterility tests were performed (Korhonen 1978)using homokariotic test cultures 96119 (H. parviporum),98036 (H. parviporum), 03013 (H. annosum senso stricto),and 03015 (H. annosum senso stricto) (courtesy Dr. Kari Ko-rhonen, Finnish Forest Research Institute).One to three representatives from the remaining mycelial

morphotypes were subjected to molecular identification fol-lowing modified procedures from previous studies (Vasiliaus-kas et al. 2004, 2005). In brief, DNA extraction and PCRamplification were done accordingly to established protocols(Kåren et al. 1997). The ready PCR products were purifiedusing Calf Intestine Alkaline Phosphate (CIAP) and Escheri-chia coli exonuclease I. After purification, PCR products

were Sanger sequenced by Macrogen (Seoul, Republic ofKorea) using the primer ITS4 for every specimen. Sequenc-ing was performed on one direction. All sequences weremanually edited using the Lasergene software package Seq-Man (version 5.07, DNASTAR, Madison, Wisconsin).BLAST searches were performed using two reference se-quence databases, one at GenBank (http://www.ncbi.nlm.nih.gov/blast) and one at the Department of Forest Mycologyand Pathology, Swedish University of Agricultural Sciences.The ITS sequence homology was set at 98%–100% for delim-iting fungal taxon (presumed species) and at 94%–97% fordelimiting at the genus level. Internal Transcribed Spacer(ITS) sequences of each sequenced mycelial morphotypewere deposited in GenBank (for GenBank Accession num-bers, see Table 4).

Volume calculations and statistical analysesStand characteristics (species composition, age, and site

type) were estimated 1–5 years prior to harvesting and takenfrom stand inventory data in the Forest State Register. Vol-ume calculations of decayed logs in individual stems werebased on actual decay length in analysed trees and done ac-cording to formulas in Ozoliņš (2002). Calculations of decayvolume in the stand were based on the volume of decayedlog and the number of butt rot infected stems and applyingthose data in the context of regional forest yield models andtables (Kuliesis 1993). The calculations were arranged in thefollowing order: (i) the results of the present work gave ac-tual data on average lengths of decay for mature spruce treesin relation to stump diameter, DBH, and tree height (Table 2);

Table 1. Picea abies sites and stumps investigated.

Age of harvested stands, minimum–maximum (mean) in years

Parameters 27–49 (39) 50–69 (61) 70–89 (82) 90–109 (99) 110–164 (127) All (72)SitesNo. of clear-felled sites 17 18 47 55 32 169No. of thinned sites 86 31 14 11 7 149Total no. of sites 103 49 61 66 39 318Mean (minimum–maximum)butt rot incidence (%)*

16.7 (0–60) 21.5 (2–62) 22.1 (0–68) 25.7 (3–83) 30.4 (6–56) 21.8 (0–83)

Stumps†

No. examined 8789 3835 4362 4791 2968 24745No. containing butt rot 1471 825 963 1229 903 5391Diameter of butt rot infectedstumps, mean ± SD (cm)

21.4±8.7a 29.6±9.7a 34.7±12.3a 38.0±14.1a 40.9±15.2a 32.3±14.1a

Diameter of healthy stumps,mean ± SD (cm)

20.3±8.4b 27.5±12.1b 31.9±12.5b 35.5±14.0b 36.6±14.5b 28.1±13.2b

Diameter of all stumps, mean ±SD (cm)

20.5±8.5 28.0±11.6 32.5±12.5 36.2±14.1 37.9±14.9 28.9±13.6

Butt rot‡

Diameter at stump, mean ± SD(cm)

8.3±6.8a 9.9±8.0a 10.5±9.4b 13.0±10.5c 12.9±11.7c 11.9±10.3

No. classed as discoloration (%) 588 (40)a 126 (15)b 170 (18)b 213 (17)b 133 (15)b 1230 (23)No. classed as decay (%) 513 (35)a 372 (45)b 441 (46)b 460 (37)a 322 (36)a 2108 (39)No. classed as advanced rot (%) 161 (11)a 143 (17)b 163 (17)b 225 (18)b 178 (20)b 870 (16)No. classed as hollow (%) 209 (14)a 184 (22)bd 189 (20)b 331 (27)cd 270 (30)c 1183 (22)

*Correlation between average stand age and average butt-rot incidence: r = 0.984, p < 0.05.†Values within a column followed by a different letter differ significantly (t test, p < 0.001).‡Values within a row followed by a different letter differ significantly (diameter means compared using a t test, p < 0.001; proportions of stumps containing

the given butt rot category at each stand age compared using c2 tests, p < 0.001).

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(ii) the lengths of decay were assumed to correspond to ac-tual lengths of “decayed log” in respective age classes withcorresponding stem parameters; (iii) the volumes of “decayedlog” were calculated by standard formulas for P. abies(Ozoliņš 2002), based on log diameter and length (the lattercorresponding to respective lengths of decay); (iv) from re-gional forest yield models and tables (Kuliesis 1993), the ap-propriate category of stand age – height ratio of P. abies wasselected based on its closest proximity to age and DBH tothose of analysed trees (Table 2); (v) from the models foreach given category, tree number and volume per hectare infully stocked (1.0) stands at a given age are available andwere projected on actual levels on decay incidence in LatvianP. abies stands; and (vi) the number of decayed stems andtheir decayed volume were calculated based on volumes ofdecay-containing logs (Table 2).The analysis of proportions (c2 tests), correlations, and t

tests were estimated using Minitab 15 software and Excel,and their significances were evaluated according to Fowler etal. (2001). Analysis of similarity between fungal commun-ities in all sampling categories was performed by calculatingthe qualitative Sorensen similarity index (Magurran 1988).

Results

Butt rot incidence varied strongly between individual forestsites, from 0% to 83%, and was 21.8% on average (Table 1).There was a positive correlation between stand age and buttrot frequency (r = 0.317, p < 0.001) (Fig. 2). The level ofmixture with other tree species in the composition of P. abiesstand had no influence on incidence of the rot (r = 0.007,p < 0.001). Forest site type had a significant impact on buttrot incidence: it was highest on Hylocomiosa (27.2%) sites,followed by Oxalidosa (23.7%), Mercurialiosa (18.7%), andwas lowest on Myrtillosa forest site type (15.6%) and drainedpeat soils (15.8%) (c2 test, p < 0.001). The interaction ofstand age and forest site type on butt rot frequency was notsignificant (test of between-subject effects, p = 0.4).Larger stumps were more likely to contain decay, both in

each tree age class and in the whole sample (Table 1).Among the 5391 butt rot containing stumps examined, 1230(23%) showed discoloration, 2108 (39%) showed decay, 870(16%) showed advanced rot, and 1183 (22%) were hollow.

The proportion of stumps with advanced rot and that werehollow tended to increase in older stands (Table 1). The di-ameter of the rot at stump height varied from 0.5 to 80 cm(mean 9.7 ± 4.7 cm) and was positively correlated with standage (r = 0.411, p < 0.001).The parameters of felled stems are presented in Table 2.

The length of decay columns in the felled stems varied from0.5 to 12.4 m and was 6.6 ± 2.6 m on average. There was aweak positive correlation between stem DBH and length ofdecay (Fig. 3). The diameter of rot at stump height was 1.6–65.6 cm (average 29.4 ± 12.0 cm) and at breast height was0–44.3 cm (21.0 ± 8.5 cm). The length of decay correlatedpositively with stump diameter (r = 0.39, p < 0.01), stemDBH (r = 0.26, p < 0.01), tree height (r = 0.37, p < 0.01),and diameter of decay at stump level (r = 0.62, p < 0.001).The average volume of decayed logs in relation to stem DBHand length of decay is presented in Table 2. Based on ac-tually observed butt rot frequencies in Latvian P. abies standsof different age classes (Table 1), volumes of decay-degradedwood in a fully stocked stand would comprise about19.7 m3·ha–1 at the age of 40 years, 57.4 m3·ha–1 at 60 years,54.9 m3·ha–1 at 80 years, 63.1 m3·ha–1 at 100 years, and91.8 m3·ha–1 at 120 years, corresponding to 6%–16% of a to-tal standing volume (Table 3).From a total of 1182 samples from stumps, 655 (54.9%)

resulted in fungal growth and yielded 866 strains, represent-ing 76 fungal taxa. Among 300 samples from felled trees,196 (65.3%) resulted in fungal growth and yielded 323 fun-gal strains, representing 52 fungal taxa (Table 4). The rest ofthe samples remained sterile, gave only bacterial growth, orwere contaminated. Heterobasidion parviporum was mostcommon among decay-causing fungi (basidiomycetes), iso-lated from 131 stumps (11.1%) and 63 stems (55.3%) (Ta-ble 4). Its identity in each case was confirmed byintersterility tests. Stereum sanguinolentum was the secondmost common basidiomycete in both stumps (3%) and stemcolumns (3.5%). The maximum heights of decay column atwhich the two species were isolated were 11.4 m and12.4 m, respectively.The most characteristic ascomycetes–anamorphic fungi

identified were Ophiostoma piceae, Cytospora spp., Chalaraspp., Ascocoryne cylichnium, and Neonectria fuckeliana (Ta-ble 4). Species richness of fungi was higher on clearcut (67

Table 2. Mean (± SD) stem and decay parameters of analysed trees.

Stem DBH, mean ± SD (cm)

Parameter 12–19 (16.2 ± 2.8) 20–26 (23.3 ± 2.1) 27–32 (30.4 ± 1.6) 33–54 (40.7 ± 5.7) AllTree height, m 14.3±3.1 22.2±3.2 26.7±2.3 28.6±2.5 24.5±5.1Tree age,* years 40 65 95 120 85Butt diameter, cm 21.7±4.7 31.8±5.7 43.0±5.4 53.7±9.3 40.0

±12.2Decay length,† m 3.4±2.5 6.7±2.4 7.2±2.0 7.0±2.3 6.6±2.6Stem volume,‡ m3 0.1639 0.4674 0.9204 1.7953 0.9165Volume of a log with decay present, m3 0.0662 0.2444 0.4508 0.8124 0.4387No. of trees 11 39 36 28 114

Note: DBH, diameter at breast height. The volume of decayed logs was calculated according to Ozoliņš (2002), based on log butt diameter and length ofdecay.*Taken from stand growth tables using closest proximity of tree height / tree DBH from parameters of fully stocked (1.0) P. abies stands of age–height ratio

100 years / 27 m (Kuliesis 1993).†Mean decay length observed in examined stems with respect to mean DBH (Fig. 3).‡Stem volume of a tree from stump to top.

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species) than on thinned (48 species) sites. Yet, Sorensensimilarity index between those communities was rather high(0.68), indicating that in most cases the same species weredetected.

Discussion

The present study shows that about one-fifth of P. abiestrees in Latvian forests are infected by butt rot and stem de-cay and that infection frequency among individual standsvaries greatly. The results are comparable with 10%–30% rotfrequency (Enerstvedt and Venn 1979; Norokorpi 1979; Nil-sen 1983; Vasiliauskas 1989; Huse et al. 1994; Vasiliauskaset al. 2002) and 8%–30% of yield loss (Kallio 1972; Kallioand Tamminen 1974; Tamminen 1985) detected during pre-vious inventories in Nordic and Baltic countries.The significant influence of stand age and forest site type

on rot incidence and intensity also agrees with the previousreports, although in a Lithuanian study, a correlation betweenstand age and butt rot incidence was not detected (Vasiliaus-kas et al. 2002). However, earlier in Latvia, Mangalis (1975)determined that in Oxalidosa and Hylocomiosa forest sitetypes, the occurrence of butt rot increased with stand ageand varied from 1% to 63.8%. In a Norwegian study, in soilswith good drainage capacity, butt rot was more common thanit was in soils with less drainage capacity, but there was no

obvious relationship between rot frequency and site class(Nilsen 1983). In another Norwegian study, butt rot fre-quency was positively correlated with increasing stump diam-eter (Enerstvedt and Venn 1979), as it was observed in thepresent work (Table 1). These observations could be attrib-uted to the fact that decayed trees increase their butt diame-ters to compensate for the decay, or in case ofHeterobasidion infections, larger trees are infected morereadily because they are faster growing and contact inoculumfrom adjacent infected stumps more quickly. Several studiesreported that butt rot frequency in P. abies stands tends todecrease with an increased fraction of deciduous trees andpine (Huse et al. 1994; Linden and Vollbrecht 2002, Gait-nieks et al. 2008), but this was not the case in the presentstudy.The major problem in interpreting the results obtained in

our trial is that the history of the stands is unknown andmanagement is the most likely cause determining the highvariation observed. It is known that butt rot frequency in astand is influenced by different factors such as site history,site management, previous tree rotation, and stem damage bygame (Isomäki and Kallio 1974; Swedjemark and Stenlid1993; Piri 2003). Felling in warmer seasons during thegrowth period creates a higher risk of infecting the treeswith pathogens by both fresh stumps, which are known asthe main Heterobasidion spp. infection source, and mechani-

Table 3. Decay-caused volume losses in relation to actual butt rot incidence in Latvian Picea abies stands.

Stand age, yearsStand and decay parameters 40 60 80 100 120

Stand DBH, cm 15.8 20.6 25.8 29.8 36.3Stand height, m 17.1 20.9 24.7 27.0 31.4Stand volume, m3·ha–1 311 386 458 501 577No. of stems in stand, ha–1 1779 1093 713 543 371Actual no. (%) of butt rot infected trees(Table 1)

297 (16.7) 235 (21.5) 158 (22.1) 140 (25.7) 113 (30.4)

Actual volume of decayed logs,*m3·ha–1 (% of stand volume)

19.7 (6.3) 57.4 (14.9) 54.9 (12.0) 63.1 (12.5) 91.8 (15.9)

Note: Stand parameters represent fully stocked (1.0) stands (Kuliesis 1993), with closest estimate in age and mean DBH to those ofanalysed trees (Table 2).*Calculated based on assumption that average volumes of a decayed log at age classes 60 and 100 years correspond to actual decayed

log volumes at 65 and 95 years, respectively (Table 2), and that average volume of a decayed log in the 80-year age class is a mean ofthose two, or 0.3476 m3. Decayed log volumes for 40- and 120-year age classes correspond to those actually observed (Table 2).

Fig. 2. Butt rot incidence in Picea abies stands of Latvia in relationto stand age (r = 0.317, p < 0.001).

Fig. 3. Correlation between stem DBH and length of decay in Piceaabies stems. (r = 0.27, p < 0.01).



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Table 4. Fungi isolated from wood samples from Picea abies stumps and stems in Latvia.

Fungi (% of substrates colonized / % among isolated)

Fungal taxaGenBankAccession No.

Thinned stumpson sites

Clear-felled stumpson sites Living stems

BasidiomycetesAmylostereum areolatum (Chaillet ex Fr.) Boidin FJ903375 — 0.2/0.6 0.9/1.3Amylostereum chailletii (Pers.) Boidin FJ903304 0.5/2.4 0.5/1.8 —Armillaria cepistipes Velen. FJ903313 — 0.3/1.2 —Basidiomycete sp. A16 FJ903287 — 0.2/0.6 —Basidiomycete sp. B14 FJ903300 — 0.3/1.2 —Basidiomycete sp. B33 FJ903305 — 0.2/0.6 —Basidiomycete sp. E21 FJ903338 — — 0.9/1.3Basidiomycete sp. L61 FJ903368 — — 0.9/1.3Basidiomycete sp. N42 FJ903378 — 0.3/1.2 —Bjerkandera adusta (Willd.) P. Karst. FJ903311 1.6/7.3 2.4/9.0 1.7/2.5Bjerkandera fumosa (Pers.) P. Karst. FJ903376 0.2/0.8 — —Climacocystis borealis (Fr.) Kotl. & Pouzar FJ903302 0.4/1.6 0.7/2.4 —Coprinellus sp. 222 FJ903332 — — 1.7/2.5Cylindrobasidium evolvens (Fr.) Jülich FJ903309 0.5/2.4 1.0/3.6 —Flammulina velutipes (Curtis) Singer FJ903296 0.2/0.8 — —Fomitopsis pinicola (Sw.) P. Karst. FJ903310 — 0.2/0.6 —Gloeophyllum odoratum (Wulfen) Imazeki FJ903299 — 0.2/0.6 —Gloeophyllum sepiarium (Wulfen) P. Karst. FJ903356 — — 1.8/2.5Heterobasidion parviporum Niemelä & Korhonen FJ903330 12.3/56.1 9.8/37.1 55.3/78.8Oxyporus corticola (Fr.) Ryvarden FJ903327 — 0.2/0.6 —Peniophora incarnata (Pers.) P. Karst. FJ903308 — 0.3/1.2 —Phlebia radiata Fr. FJ903348 — — 0.9/1.3Phlebia tremellosa (Schrad.) Nakasone & Burds. FJ903298 — 0.2/0.6 —Phlebiopsis gigantea (Fr.) Jülich FJ903306 0.7/3.3 1.0/3.6 —Polyporus brumalis (Pers.) Fr. FJ903349 — — 0.9/1.3Porodaedalea chrysoloma (Fr.) Fiasson & Niemelä FJ903363 — — 0.9/1.3Schizophyllum commune Fr. FJ903301 0.7/3.3 1.6/6.0 —Sistotrema brinkmannii (Bres.) J. Erikss. FJ903297 1.8/8.1 2.7/10.2 —Skeletocutis odora (Peck ex Sacc.) Ginns FJ903307 0.2/0.8 — —Stereum sanguinolentum (Alb. & Schwein.) Fr. FJ903322 2.7/12.2 3.2/12.0 3.5/5.0Trametes hirsuta (Wulfen) Lloyd FJ903351 — — —Trametes ochracea (Pers.) Gilb. & Ryvarden FJ903281 0.2/0.8 0.8/3.0 —Trametes versicolor (L.) Lloyd FJ903303 — 0.6/2.4 —Anamorphic fungi and ascomycetesAlternaria alternata (Fr.) Keissl. FJ903288 0.2/0.4 — —Apiospora montagnei Sacc. FJ903318 0.5/1.6 0.3/0.6 —Arthrographis pinicola Sigler & Yamaoka FJ903328 0.2/0.4 0.2/0.3 —Ascocoryne cylichnium (Tul.) Korf FJ903373 3.0/6.7 4.4/8.8 17.4/11.2Ascocoryne sarcoides (Jacq.) J.W. Groves & D.E. Wilson — 1.2/2.8 2.7/5.3 5.2/3.4Ascocoryne sp. A34 FJ903292 0.2/0.4 — 2.6/1.7Ascomycete sp. B29 — — 0.6/1.3 —Ascomycete sp. C49 FJ903323 — 0.2/0.3 —Ascomycete sp. L19 FJ903346 — — 0.9/0.6Ascomycete sp. L32 — — — 0.9/0.6Ascomycete sp. L51 FJ903364 — — 0.9/0.6Ascomycete sp. N6 FJ903369 — 0.2/0.3 —Ascomycete sp. N8 — — 0.3/0.6 —Ascomycete sp. N43 FJ903379 0.2/0.4 — —Aspergillus spp. — — — 2.6/1.7Botryotinia fuckeliana (de Bary) Whetzel FJ903283 — 0.6/1.3 —Cadophora malorum (Kidd & Beaumont) W. Gams FJ903289 2.3/5.1 2.5/5.0 —Capronia sp. C51 FJ903324 0.9/2.0 0.3/0.6 —Chaetomium sp. E11 FJ903333 — — 0.9/0.6Chaetomium sp. L16 FJ903344 — — 1.7/1.1

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Chaetomium sp. T6 FJ903382 — — 0.9/0.6Chalara sp. 400 FJ903320 3.4/7.5 1.9/3.8 1.8/1.1Cladosporium tenuissimum Cooke FJ903350 — — 6.1/3.9Cosmospora vilior (Starbäck) Rossman & Samuels — 0.7/1.6 0.2/0.3 —Cylindrocarpon didymum (Harting) Wollenw. — — 0.2/0.3 —Cytospora sp. A11 FJ903284 4.8/10.7 4.3/8.5 0.9/0.6Epicoccum nigrum Link FJ903352 — — 1.8/1.1Eutypa lata (Pers.) Tul. & C. Tul. FJ903370 — 0.2/0.3 —Fusarium sp. E19 FJ903337 — — 0.9/0.6Gibberella avenacea R.J. Cook — 0.2/0.4 1.1/2.2 —Gnomonia sp. A36 FJ903293 — 0.3/0.6 —Haematonectria haematococca (Berk. & Broome) Samuels& Nirenberg

FJ903374 — 0.2/0.3 —

Hypoxylon serpens (Pers.) J. Kickx f. FJ903321 0.2/0.4 0.2/0.3 —Lecythophora hoffmannii (J.F.H. Beyma) W. Gams &McGinnis

FJ903377 2.5/5.5 3.7/7.2 —

Lecythophora sp. A14 FJ903286 0.9/2.0 1.1/2.2 —Lecythophora sp. A29 FJ903291 1.1/2.4 1.0/1.9 —Leptodontium elatius (F. Mangenot) de Hoog FJ903294 0.7/1.6 0.3/0.6 0.9/0.6Lewia infectoria (Fuckel) M.E. Barr & E.G. Simmons FJ903347 — — 1.8/1.1Nectria cinnabarina (Tode) Fr. FJ903339 — — 0.9/0.6Neonectria fuckeliana (C. Booth) Castl. & Rossman FJ903380 3.2/7.1 3.3/6.6 15.7/10.1Ophiostoma olivaceum Math.-Käärik FJ903282 — 0.3/0.6 —Ophiostoma piceae (Münch) Syd. & P. Syd. — 8.5/19.0 5.1/10.0 0.9/0.6Ophiostoma piceaperdum (Rumbold) Arx FJ903319 0.2/0.4 0.5/0.9 —Ophiostoma sp. C59 FJ903325 0.2/0.4 0.2/0.3 —Penicillium spp. — 2.3/5.1 2.7/5.3 12.2/7.9Periconia sp. L12 FJ903341 — — 0.9/0.6Phaeoacremonium sp. A27 FJ903290 0.2/0.4 — —Paraphoma sp. L13 FJ903342 — — 0.9/0.6Phialocephala sp. C4 FJ903312 0.9/2.0 0.2/0.3 —Phialocephala sp. C8 FJ903314 — 0.3/0.6 —Phialocephala sp. L12 FJ903362 — — 5.2/3.4Phialophora fastigiata (Lagerb. & Melin) Conant FJ903336 — — 0.9/0.6Phialophora sp. C16 FJ903315 0.4/0.8 — —Phialophora sp. L5 FJ903340 — — 1.8/1.1Phialophora sp. N21 FJ903372 0.2/0.4 — —Phoma exigua Sacc. FJ903360 — — 1.8/1.1Phoma sp. E16 FJ903335 — — 1.8/1.1Phoma sp. N20 FJ903371 — 0.2/0.3 —Preussia sp. L34 FJ903358 — — 0.9/0.6Pseudeurotium bakeri C. Booth FJ903285 — 0.3/0.6 —Pycnidiophora sp. L15 FJ903343 — — 2.6/1.7Sarea difformis (Fr.) Fr. FJ903295 0.4/0.8 0.3/0.6 —Sarea resinae (Fr.) Kuntze FJ903329 — — 0.9/0.6Sarea sp. C65 FJ903326 — 0.3/0.6 —Scytalidium lignicola Pesante FJ903317 0.4/0.8 1.4/2.8 1.8/1.1Spadicoides bina (Corda) S. Hughes FJ903316 0.4/0.8 0.2/0.3 3.5/2.2Sydowia polyspora (Bref. & Tavel) E. Müll. — 0.9/2.0 0.8/1.6 —Thysanophora penicillioides (Roum.) W.B. Kendr. FJ903357 — — 0.9/0.6Trichocladium opacum (Corda) S. Hughes FJ903366 — — 0.9/0.6Trichoderma spp. — 2.7/5.9 5.7/11.3 7.8/5.1Valsa sordida Nitschke FJ903354 — — 0.9/0.6Unidentified fungi — 0.2/0.4 0.3/0.6 7.8/5.1



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cal wounds (Rönnberg 2000; Vasiliauskas 2001; Mäkinen etal. 2007).Moreover, the results of this work demonstrated that yield

loss due to butt rot in Latvian P. abies stands is rather low atthe relatively young age of 40 years but increases more thantwofold at age classes of 60–100 years and threefold in over-mature stands of 120–160 years of age. This is an additionalargument for considering assigning overmature P. abies for-ests with protective status, as yield loss due to decay there isalready high and, on the other hand, such stands are likely toharbour vulnerable and threatened species (Nitare 2000).However, more research is needed to assess best options forharvesting younger P. abies stands.This study shows that H. parviporum is the main cause of

butt rot in Latvian P. abies stands, which indicates that suchforest sites are permanently infested and that the disease willpersist over future forest generations. Therefore, on suchsites, planting Heterobasidion-resistant tree species should beconsidered, in particular using short-rotation, fast-growing,native Alnus and Populus. For example, in recent extensivepathogen inventories of Latvian Alnus incana and A. gluti-nosa stands, Heterobasidion infections were not detected (Ar-hipova et al. 2011; N. Arhipova, T. Gaitnieks, J. Donis,J. Stenlid, and R. Vasaitis, unpublished). On the other hand,on heavily Heterobasidion-infested sites, stump removal islikely to reduce butt rot (Vasaitis et al. 2008), and this shouldalso be considered under Latvian conditions.Heterobasidion parviporum, S. sanguinolentum, and Amy-

lostereum spp. are known as common butt and stem rotagents in living P. abies (Pechmann et al. 1973; Woodwardet al. 1998; Vasiliauskas 1999, and references therein). How-ever, this study has revealed the presence of the basidiomy-cetes Bjerkandera adusta, Polyporus brumalis, andGloeophyllum sepiarium in active decay columns in livingP. abies stems. These species are known as saprophytes, ordecomposers of dead wood. Interestingly, B. adusta and P.brumalis have been previously reported as occasional buttrot agents of P. abies in southern Germany (Pechmann andAufsess 1971; Pechmann et al. 1973) and G. sepiarium innorthern Finland (Norokorpi 1979).In conclusion, the present study provides relevant informa-

tion on current and future wood yield loss in P. abies stands,indicating that both preventive and combative control meas-

ures against butt rot should be undertaken to sustain continu-ous wood production in the forests of Latvia.

AcknowledgmentsThis study was supported by the JSC “Latvian State For-

ests”, the Latvian State Forest Research Institute “Silava”,the Swedish Energy Agency (STEM), the Faculty of NaturalResources and Agricultural Sciences (research programTEMA), and the Swedish University of Agricultural Scien-ces. We thank Anna Hopkins for language revision.

ReferencesArhipova, N., Gaitnieks, T., Donis, J., Stenlid, J., and Vasaitis, R.

2011. Decay, yield loss and associated fungi in stands of grey alder(Alnus incana) in Latvia. Forestry, 84(4): 337–348. doi:10.1093/forestry/cpr018.

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Bušs, K. 1997. Forest ecosystem classification in Latvia. InProceedings of Latvian Academy of Sciences, Section B. Vol.51. Riga, Latvia. pp. 204–218. [ISSN 1407-009X.]

Enerstvedt, L.I., and Venn, K. 1979. Decay in mature Picea abies (L.)Karst. stands. A study on clear-cuttings in Øvre Eiker. Medd. Nor.Inst. Skogforsk. 35: 237–264. [In Norwegian with Englishsummary.]

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Table 4 (concluded).





ZygomycetesMortierella spp. — 0.5/1.2 0.3/0.6 14.8/9.6Mucor spp. — 0.4/0.8 0.6/1.3 18.3/11.8Umbelopsis isabellina (Oudem.) W. Gams — — 0.5/0.9 —Umbelopsis ramanniana (Möller) W. Gams — — 0.3/0.6 3.5/2.2

No. of forest sites 169 149 4No. of sampled stumps or stems 552 630 114No. of isolated species 48 67 52No. of isolated strains 380 486 323No. of wood samples 552 630 300

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Butt rot incidence, causal fungi, and related yield loss in Picea abies stands of Latvia