Urea treatment reduced Heterobasidion annosum s.l. root rot in Picea abies after 15 years

+ Models

FORECO-10919; No of Pages 7

Urea treatment reduced Heterobasidion annosum s.l. root rot

in Picea abies after 15 years

J. Oliva a,b,*, N. Samils b, U. Johansson c, M. Bendz-Hellgren b, J. Stenlid b

a Area de Defensa del Bosc, Centre Tecnologic Forestal de Catalunya, Pujada del Seminari s/n, E-25280 Solsona, Spainb Department of Forest Mycology and Pathology, Swedish University of Agricultural Sciences, Box 7026, S-750 07 Uppsala, Sweden

c Tonnersjohedens and Skarhult Experimental Forests, Box 17, S-310 38 Simlangsdalen, Sweden

Received 30 October 2007; received in revised form 22 January 2008; accepted 25 January 2008

Abstract

Stump protection using chemical or biological agents is the main control measure against root and butt rot caused by Heterobasidion annosum

s.l. in northern and temperate conifer forests. Long-term effects of urea treatment of stumps are poorly known and here we describe a 15-year study

of urea treatment on the rot incidence on Norway spruce (Picea abies). We also tested the effect of urea protection on tree growth and on the

resistance of stands against strong winds. Four treatments were made in two replications in two first-rotation P. abies stands in southern Sweden;

after first-thinning stumps were (i) treated with urea 35% (w/v), (ii) artificially infected with H. annosum conidia, (iii) half urea treated and half

artificially conidia infected, (iv) untreated, therefore naturally infected. After 15 years, the trees were sampled at 20 cm above ground using an

increment borer and observed for presence of rot and, following incubation, presence of H. annosum conidia. Tree growth was calculated by

measuring the diameter before and after the treatment. Urea treated plots showed the lowest incidence of rot (3%) as well as of H. annosum

incidence (0%). Conidia treatment showed the highest incidence of rot (68%), its incidence was higher than that observed in natural infection

treatment (43%), but did not differ from that of the 50% conidia treatment (47%). On about 30% of the rotted trees we observed conspicuous H.

annosum fruiting. We did not observe growth reduction associated with tree rot. H. annosum was the only fungus observed associated with rotted

trees which suggest that it was responsible for most of the rot observed in the investigated plots. Urea treated plots showed the lowest incidence of

windthrown trees, and 59% of the windthrown tree incidence among the plots was explained by the incidence of H. annosum. Urea can be regarded

as a reliable long-term protection method against root and butt rot of Norway spruce.

# 2008 Elsevier B.V. All rights reserved.

Keywords: Heterobasidion annosum; Norway spruce; Butt rot; Stump protection; Chemical control

www.elsevier.com/locate/foreco

Available online at www.sciencedirect.com

Forest Ecology and Management xxx (2008) xxx–xxx

1. Introduction

Root and butt rot caused by Heterobasidion annosum (Fr.)

Bref. sensu lato is the most important tree pathogen in north and

temperate coniferous forests. In Europe, there are three inter-

sterility groups with marked host preferences (Korhonen et al.,

1998). Heterobasidion annosum sensu stricto usually affects

pine (Pinus spp.) and other conifers, H. parviporum is mostly

found affecting Norway spruce (Picea abies L.), H. abietinum

is found infecting silver fir (Abies alba Mill.) in southern

* Corresponding author at: Area de Defensa del Bosc, Centre Tecnologic

Forestal de Catalunya, Pujada del Seminari s/n, E-25280 Solsona, Spain.

Tel.: +34 973 481752.

E-mail addresses: [email protected] (J. Oliva),

[email protected] (N. Samils), [email protected]

(U. Johansson), [email protected] (J. Stenlid).

0378-1127/$ – see front matter # 2008 Elsevier B.V. All rights reserved.

doi:10.1016/j.foreco.2008.01.063

Please cite this article in press as: Oliva, J., et al., Urea treatment reduce

Forest Ecol. Manage. (2008), doi:10.1016/j.foreco.2008.01.063

Europe (Niemela and Korhonen, 1998). Norway spruce is one

of the most productive species in the Scandinavian countries

and it is very susceptible to H. annosum butt rot. Winter cuttings

instead of summer cuttings (Moykkynen and Miina, 2002), or

the promotion of mixed stands (Linden and Vollbrecht, 2002)

have been suggested as preventive measures for this disease,

however due to industry supply demands these conditions are

not always feasible.

In managed stands, newly created stumps are usually

colonized by airborne H. annosum basidiospores. The fungus

then colonizes neighbour trees via the connections existing

amongst root systems (Rishbeth, 1951; Redfern and Stenlid,

1998). Stump protection against airborne spore infection is one

of the main control strategies. It is economically viable (Thor

et al., 2006), and it has usually been achieved through spraying

stump surfaces either with spore suspensions of other more

competitive fungi or with chemicals such as urea or borate

d Heterobasidion annosum s.l. root rot in Picea abies after 15 years,

mailto:[email protected]




http://dx.doi.org/10.1016/j.foreco.2008.01.063


Table 1

Site characteristics and mean values of stem density and tree diameter in 1992

and 2007 at the two sites

Bertilstorp Christinehof

Coordinates

Latitude 5584505700N 5584201500NLongitude 148301500E 1480602500E

Elevation (m) 125 116

Site indexa (m) 32.9 34.9

Density (stems ha�1)

1992 1875 (1775–1975) 2167 (2046–2289)

2007 996 (853–1139) 986 (752–1191)

Diameterb (cm)

1992 14.0 (13.8–14.2) 13.3 (13.1–13.6)

2007 22.5 (22.0–23.0) 21.6 (21.1–22.1)

Confidence interval at 95% is shown in brackets.a Dominant tree height at an age of 100 years.b Diameter refers only to the trees still alive in 2007.

J. Oliva et al. / Forest Ecology and Management xxx (2008) xxx–xxx2

+ Models


(Pratt et al., 1998; Holdenrieder and Greig, 1998). Today, the

most widespread control method is based on the decay fungus

Phlebiopsis gigantea (Fr.) Jul (Pratt et al., 2000; Thor, 2003),

one of the most commonly used formulas is registered as

Rotstop1. Some claims regarding the potential danger of

spreading a single isolate (Johansson et al., 2002), and variable

results in stump protection (Berglund and Ronnberg, 2004;

Berglund et al., 2005; Thor and Stenlid, 2005; Ronnberg et al.,

2006) could make other less used methods to be re-considered.

Amongst chemicals, urea formulations are the most

commonly used (Thor, 2003). The hydrolysis of the urea

produces ammonia raising the pH in the surface of the stump

into toxic levels for H. annosum (Johansson et al., 2002).

Efficient control is achieved when enough quantity of urea for

keeping the pH 7 is supplied and provided that the infections

occur in the sapwood. In earlier experiments, urea generally

gave good results, but may have had some collateral effects,

like the shift in either the fungi community inhabiting the

spruce stumps (Vasiliauskas et al., 2004) or in the epixylic plant

species population (Westlund and Nohrstedt, 2000). The main

issue, though, is that urea must be registered as a fungicide for

its use and no revenues can be expected from its registration.

Short-term effects of the treatment are well described but

mainly focus on the H. annosum incidence in treated and

control stumps (Pratt and Redfern, 2001; Nicolotti and

Gonthier, 2005; Thor and Stenlid, 2005). Long-term effects

of stump treatments regarding the protection against tree rot are

not satisfactorily documented in the literature (Pratt et al.,

1998).

Growth reductions have been associated with H. annosum

(Bendz-Hellgren and Stenlid, 1995). Trees react against fungus

infection by producing a reaction zone, and it has been observed

that the theoretical cost for producing the reaction zone

compounds was similar to the growth reduction associated to

the butt rot presence in Norway spruce. Several studies have

shown that root rot may affect the growth of trees (Reviewed in

Stenlid and Redfern, 1998) but the effect of H. annosum butt rot

on the growth of Norway spruce needs to be experimentally

tested.

Spruce stands are regarded to be particularly sensitive to

windthrow. Several issues are associated with the spruce trees

low resistance against strong winds such as: shallow root

systems, changes in the root architecture and intensive

management practices (Nilsson et al., 2004). Besides its

intrinsic susceptibility, spruce trees with H. annosum-infected

root systems could be more sensitive to strong winds

(Bazzigher and Schmid, 1969) and as observed for black

spruce (Picea mariana Mill.) by Whitney et al. (2002). The

occurrence of two major storms within the time of the

experiment (2005 and 2007) allowed us to study whether urea

treated plots were more resistant to wind.

In this study we aimed to: (i) evaluate the long-term effects

of urea treatment on P. abies plots by comparing the root rot

incidence between treated, natural infected and artificially

infected plots, (ii) assess the effect of H. annosum on the tree

growth, (iii) assess the effect of root rot on windthrown and the

putative resistance of urea treated plots against storms.



Testing the effect of urea treatment on root and butt rot

incidence should ensure a similar level of urea amongst

replicates, but also should ensure a sufficient level of H.

annosum infection. Stumps can be artificially infected with

conidia (Bendz-Hellgren and Stenlid, 1998), so we performed

two levels of treatment entailing artificial infection of half of

the stumps and the artificial infection of all of the stumps, in

order to include diverse controlled levels of infection.

2. Material and methods

2.1. Site description and experimental design

The experiment was conducted in two first rotation Norway

spruce stands placed on former agricultural lands in Skane

(southern Sweden). Each stand contained two replicate plots of

each treatment in a randomized block design. Site character-

istics of both locations are shown in Table 1. Plots were

rectangular (on average 20 m � 20 m) and included an average

of 82 trees. The minimum distance between plots was 20 m.

Both stands were first thinned in 1992 at the age of 22 years,

with an average intensity (number of trees removed/number of

trees before the thinning) of 34.0% (CI: 28.1–39.9). Immedi-

ately after the thinning, in two randomly chosen plots within

each location, the following treatments were applied: (i)

treatment of all stumps with an aqueous urea solution at 35%

(w/v) (urea treatment hereafter), (ii) artificial infection of all the

stumps with a H. annosum conidia suspension (100% conidia

hereafter), (iii) urea treatment of half of the stumps and artificial

infection of the other half of the stumps (50% conidia hereafter)

and (iv) no stump treatment, thus subjected to natural airborne

spore infection. The conidial suspensions were prepared as

described by Bendz-Hellgren and Stenlid (1998) and applica-

tions were made from one 9-cm Petri dish, corresponding to

between 1 and 20 million spores, per stump. The conidia, for

the 100% and 50% conidia treatments, consisted of a total of 20

different H. annosum Swedish strains, 11 of these were H.

parviporum, and 9 H. annosum s.s. Conidia were transferred



Fig. 1. Tree losses due to thinning (white) and mortality (dashed) under

different infection and protection treatments. Root rot incidence of remaining

the trees in 2007 is shown in black. Equal letter imply not statistically different

medians between treatments by least squares difference method ( p < 0.05).

Letters followed by ‘‘*’’ consider both healthy (grey) and rotted (black) trees

together.

J. Oliva et al. / Forest Ecology and Management xxx (2008) xxx–xxx 3

+ Models


from cultures on Petri dishes onto the stump surface with a

syringe. Once conidia treated, each stump was covered with a

plastic bag which was removed 5 days post treatment. Two

plots, one replicate of each of the 50% and 100% conidia

treatments, had been completely blown down due to the storm

of 2005 and had to be excluded from the study. Half of one urea

treated plot was clear-cut, and this part was thus not considered

in the analyses. Following the storm of 2005, the stands were

thinned with an average thinning intensity of 40%. The percent

of trees removed in the thinning operations did not differ

between treatments ( p = 0.66) nor between locations

( p = 0.85) (Fig. 1). The stumps left in 2005 were not treated.

Uprooted trees during the storm of 2007 were still remaining as

windthrown in the stand in 2007.

2.2. Measurements

In 2007, all living trees (533 trees) were assessed for butt rot

by extracting inner wood cores, at 20 cm from the ground level,

using a Pressler borer which was sterilized in ethanol 70%

between the extractions. Recently dead and uprooted trees (50

trees) were also bored at the same location on the stem. A

second core was always extracted perpendicular to the first if

this did not reveal any rot. Wood cores with suspected rot were

stored in sterile plastic bottles in the dark at room temperature

and observed under a dissecting microscope for the presence of

H. annosum conidiophores. Conidia from the rotted wood cores

were picked with a needle and transferred to a Petri dish

containing Hagem agar (Stenlid, 1985) and later identified

whether H. annosum or not by culture morphological

characters. The diameter at 1.3 m (referred as diameter

hereafter) of trees was recorded twice in the year of the

treatments and also when extracting the wood cores. The point

of measurement was permanently marked. Living trees, dead

trees and stumps were observed for the presence of resin flow,



reaction zone and H. annosum fruiting bodies, for the presence

of biotic or mechanical damages, and if being uprooted. The

491 stumps left after the thinning operations in 2005 and 2007

were investigated regarding decay. If a stump was severely

decayed, we assumed that the tree from which it originated had

been subjected to rot before the thinning operations.

2.3. Statistical analysis

Presence–absence variables at tree level were considered as

percent variables at plot level. Mean comparison of percent

variables between treatments were performed by logistic

regression using the GENMOD procedure of SAS/STAT

Version 8.02 software (Schabenberger and Pierce, 2002). All

incidence analyses included the location, the treatment and the

interaction between the location and the treatment. Over-

dispersion was usually observed when analyzing incidence and

was corrected by the quotient between the deviance and the

degrees of freedom (Schabenberger and Pierce, 2002). Means

were compared by the protected least squares difference

method. The association of rot with the probability to be

windthrown or with the probability to have deer wounds was

calculated with the GENMOD procedure by means of the GEE

equations. The subject was assumed to be the plot thus

enclosing the correlation resulting of the treatment and the

location.

The treatment effect on the diameter was tested by means of

the MIXED procedure. We tested the differences of diameter in

1992, diameter in 2007 and growth (percent referred to the

diameter of 2007) between rotted and healthy trees. In these

analyses we included the treatment and the interaction between

the presence of rot and the treatment. All trees in the same plot

may not behave independently, so we included the plot as a

random factor in order to perform more reliable tests on the

fixed factors (Schabenberger and Pierce, 2002).

Mean logit values are shown back-transformed into median

percent values. All means and medians presented herein are

shown with its confidence interval at 95% (CI) in brackets.

Confidence limits of percent values were calculated using a

Bayesian approach of Clopper and Pearson (1934).

3. Results

In 2007, we observed that the mortality occurring since 1992

differed between treatments ( p = 0.031) and locations

( p = 0.036) (Fig. 1). The percent of trees found dead in both

100% conidia (17.4% CI: 9.0–30.8) and natural infection

treatments (12.9% CI: 7.1–22.3) was higher than those trees

found dead in the urea treated plots (3.3% CI: 1.0–10.7). No

mortality differences were observed between these two

treatments and 50% conidia treatment (7.1% CI: 2.6–17.7),

nor between 50% conidia treatment and urea treatment.

Mortality recorded in Christinehof (13.5% CI: 8.9–19.8) was

higher than that recorded in Bertilstorp (5.5% CI: 2.5–11.8).

When not including the location per treatment interaction in the

analysis ( p = 0.85), the percent of the initial trees found still

living in 2007 of both 100% conidia (37.9% CI: 27.3–49.9) and



Table 2

Incidence of butt rot and H. annosum in Picea abies plots under different infection and protection treatments

p < x2 100% conidia 50% conidia Natural infection Urea

Incidence (%) CI 95% Incidence (%) CI 95% Incidence (%) CI 95% Incidence (%) CI 95%

Living trees, dead trees and stumps

Rot <0.0001 73.0 a 58.2–84.1 54.3 ab 39.8–68.1 43.0 b 31.6–55.2 12.4 c 6.2–23.0

H. annosum <0.0001 26.7 a 17.8–38.1 11.5 b 6.2–20.2 11.1 b 6.4–18.5 1.0 c 0.1–6.5

Living and dead trees

Rot <0.0001 68.4 a 50.1–82.4 46.7 ab 31.2–62.9 43.2 b 29.5–58.0 2.7 c 0.3–18.9

H. annosum <0.0001 23.4 a 17.0–31.3 10.7 b 6.9–16.2 15.7 ab 11.5–21.2 0.0 c 0.0–0.0

Living trees

Rot <0.0001 60.6 a 40.3–77.7 41.1 ab 26.4–57.6 33.3 b 20.4–49.3 2.7 c 0.3–15.5

H. annosum 0.0567 13.2 a 4.8–31.5 6.9 a 2.4–18.5 9.8 a 4.3–20.6 0.0 b 0.0–0.0

Stumps of 2005

Rot 0.0007 82.7 a 55.9–94.7 70.3 ab 40.5–89.2 49.7 bc 30.9–68.5 22.2 c 9.2–44.5

H. annosum <0.0001 33.1 a 19.7–49.9 19.4 ab 9.3–36.2 9.9 b 3.9–23.1 0.0 c 0.0–0.0

Equal letter imply not statistically different medians between treatments by least squares difference method ( p < 0.05). Comparisons are within the same row.

Fig. 2. Correlation between windthrown tree incidence and H. annosum inci-

dence (A) and rot incidence (B) in Picea abies plots. Equation in A: Windthrown

incidence (%) = 0.97718 + 0.57523 � H. annosum incidence (%). Equation in B:

Windthrown incidence (%) = �1.35961 + 0.21622 � rot incidence (%).


+ Models


natural infection treatment (44.8% CI: 35.4–54.7) was smaller

than that of Urea (53.7% CI: 43.5–63.7) and 50% conidia

treatments (58.7% CI: 47.4–69.2). Natural infection and 50%

conidia treatments were found not different (Fig. 1).

Urea treated plots showed the lowest incidence of rotted

trees amongst all treatments (Table 2). The plots subjected to

the 100% conidia treatment showed the highest incidences of

rot and were in all cases higher than those of the plots subjected

to natural infection. No differences were observed between

100% conidia treatment and 50% conidia treatments. When

considering both living and dead trees, we observed differences

of rot incidence between 50% conidia treatment and natural

infection. However, in the other cases both treatments were not

found different. Only when considering the rot incidence in the

stumps from 2005, we found that urea treatment did not differ

from natural infection.

We identified H. annosum as the fungus infecting 24.1% (CI:

15.0–36.3) of the rotted living trees and 31.2% (CI: 26.6–36.3)

of the rotted dead trees. In 2007 we observed H. annosum

fruiting bodies on 16.7% (CI: 9.3–28.2) of the rotted stumps

that had been created in 2005. Urea treated plots were those

with the lowest incidence of H. annosum amongst all

treatments. When considering living trees, dead trees and

stumps altogether, the H. annosum incidence was highest in the

100% conidia treatment whilst no differences were observed

between 50% conidia and natural infection treatments.

On average, 6.6% (CI: 3.9–10.9) and 3.0% (CI: 1.2–7.5) of

trees were windthrown during the storms of 2005 and 2007

respectively. Rotted trees were found to be more likely to be

windthrown than those not rotted ( p = 0.013), no interaction

between the location and the rot presence on the probability of

being uprooted was identified. The median probability of a

rotted tree to be windthrown was of 12.8% (CI: 8.3–19.2) whilst

the probability of a non-rotted tree to be windthrown was of

3.5% (CI: 1.8–6.7). Windthrown incidence respectively

correlated with the severity of rot ( p = 0.009) and H. annosum

signs ( p = 0.001) in the plot (Fig. 2). We observed the incidence

of windthrown trees in 2005 differed between treatments



( p = 0.0005). Location was a significant factor ( p = 0.014) as

Bertilstorp windthrown incidence (0.01% CI: 0.00–0.03) was

( p < 0.0001) lower than that of Christinehof (7.0% CI: 4.5–

10.7). Location was found not to interact with the treatment




+ Models


( p = 0.28). Urea treated plots showed the lowest incidence of

windthrown trees 0.0% (CI: 0.0–0.0), whilst both 100% conidia

and natural infection showed the highest, 11.0% (CI: 6.2–18.9)

and 8.7% (5.1–14.5) respectively. The incidence in the 50%

conidia treated plots (2.8% CI: 1.0–8.0) was smaller than that of

the 100% conidia treated plots, but was not different than that of

the plots subjected to natural infection.

On average, 44.3% (CI: 40.2–48.4) of both living and dead

trees had been wounded by deer. We did not observe differences

in terms of deer wound incidence between treatments

( p = 0.73), but between locations ( p < 0.0001). The Christi-

nehof plots showed higher deer wound incidence (71.4% CI:

59–81.3) than the Bertilstorp plots (5.3% CI: 1.2–20.2). We

found an association between the deer wound presence and the

rot presence in trees ( p = 0.057). Deer wound incidence on

rotted trees was 35.3% (CI: 21.8–51.6) and on those not rotted

47.3% (CI: 28.5–67.0).

Rotted trees in 2007 had a larger diameter in 1992 than those

without rot ( p = 0.042), and the rotted trees were still those

larger in 2007 ( p = 0.038). Mean diameter of rotted trees in

2007 was 22.6 cm (CI: 22.0–23.2), these trees had in 1992 a

mean diameter of 13.9 cm (CI: 13.6–14.2). The mean diameter

of healthy trees in 2007 was 21.7 cm (CI: 21.3–22.2), these

trees had a mean diameter of 13.5 cm (CI: 13.3–13.7) in 1992.

Neither type of trees was different in terms of growth

( p = 0.42). In 12.7% of the rotted living trees we recorded

resin flow at the stem base and in 56% of the rotted trees we also

identified a reaction zone. No differences in the diameter of

2007 or in growth were observed between rotted trees with or

without reaction zone or with or without resin flow.

No differences in the diameter in 2007 were observed

between treatments ( p = 0.82). We identified differences in

terms of growth between rotted and healthy trees depending on

the treatment ( p = 0.035). The mean growth of rotted trees in

the 50% conidia treated plots (56.8% CI: 47.7–65.8) was lower

( p = 0.015) than that of healthy trees (65.5% CI: 56.7–74.3).

Other comparisons were not significant. The mean growth of

rotted trees in 100% conidia treated plots (68.0% CI: 58.8–

77.2) tended to be higher ( p = 0.099) than that of healthy trees

(60.1% CI: 50.1–70.9).

4. Discussion

Urea treatment of freshly cut stumps is a reliable protection

method against Heterobasidion root rot as confirmed by our

study. After 15 years, only 2.7% of the living trees, in urea

treated plots, were rotted whereas 33.3% of the trees were

rotted in the untreated plots. In a short-term perspective, the

effects of urea stump treatment have previously been reported

in several studies (reviewed by Pratt et al., 1998). Johansson

and Brandtberg (1994) and Brandtberg et al. (1996) showed an

85% of reduction in H. annosum incidence 3–24 months after

treatment with 30% urea, compared to that of untreated stumps

whose infection incidence was of 34%. Nicolotti and Gonthier

(2005) observed that 38% of the stumps were infected by H.

annosum after being treated with a 30% urea solution, whilst

the 100% of control stumps were infected. Thor and Stenlid



(2005) observed that manual and mechanical treatment of

stumps with a 35% urea solution resulted in infection successes

of 3% and 19%, respectively, whilst 90% of control stumps

were found infected. Pratt and Redfern (2001) observed in first

rotation Picea sitchensis stands that urea treatment at 17%

reduced the natural infection success of the stumps into two

thirds when compared with control stumps. However, long-

term effects (>2 years) have not been evaluated under strict

experimental conditions, although Vollbrecht and Jorgensen

(1995) reported a significant reduction of root rot in treated

stands compared to untreated. Our study showed, under

controlled conditions, a clear effect 15 years after applying 35%

urea on the stump surfaces against H. annosum on Norway

spruce.

In 24% of the rotted trees we identified signs of H. annosum,

either by means of core culture or by direct observation of

fruiting bodies at the base of the trunk. No other fungi but H.

annosum were isolated from the wood cores. This suggests that

the majority of rot had been caused by H. annosum. Previous

investigations have shown higher isolation success of H.

annosum at 1.3 m than at stump height (Stenlid and Wasterlund,

1986; Stenlid, 1987), probably due to a more active mycelium

closer to the advancing rot front in the trunks. It is therefore

highly probable that we would have detected higher incidences

of H. annosum if we had dissected the whole tree.

Artificial stump infection resulted in a higher rot incidence

than the natural infection treatment. At stump level, natural

infection usually results in a high infection success: 88% by

Berglund et al. (2005) and 89% by Thor and Stenlid (2005).

Bendz-Hellgren and Stenlid (1998) also showed how natural

and artificial infection resulted in similar infection success

under the same conditions (73% and 95%, respectively). At tree

level, the incidence after natural infection (33.3%) seems to be

lower than at stump level, and also about half of what we have

observed after artificial infection (60.6%). This disagreement

could be explained by a more uneven infection of stumps at

stand level after natural infection than after artificial infection,

resulting in more clustered stump infections, or due to a smaller

cover of the stump surface (% of stump area infected, Thor and

Stenlid (2005)) in naturally infected stumps than in artificially

infected stumps. The latter explanation is supported by a study

by Morrison and Johnson (1978) indicating that smallish

infections tended to be less effective in survival and transfer of

disease than larger ones.

Rotted trees were more likely to become windthrown than

the healthy trees. Thus, after the storm of 2005, urea treated

plots showed the lowest incidence of windthrown trees. Our

results suggest that H. annosum root rot increases the

susceptibility of P. abies to become windthrown. A higher

correlation was found between windthrown incidence and H.

annosum incidence (R2 = 0.59) than with only rot incidence

(R2 = 0.45). Economic losses due to storms have been observed

increasing in the latter part of the 20th century (Nilsson et al.,

2004). Urea stump protection can be used to prevent tree

uprooting as a result of strong winds.

Rotted trees in 2007 were those measured larger in 1992 and

these trees were still larger in 2007. A bigger diameter is




+ Models


associated with a bigger and more widespread root system,

probably implying higher chances of root contact between trees

and infected stumps. Rotted trees in the 50% conidia treatment

grew slower than healthy trees, contrarily; rotted trees in the

100% conidia treatment tended to grow faster than healthy

trees. In all treatments except for the 50% conidia treatment, the

trend was that the smaller the initial diameter, the smaller the

radial growth. We did not find any biological explanation for

this shift in the tree growth pattern. Tree removal, which may

unevenly affect the tree growth between treatments, was found

not to be different. Diameter reduction due to H. annosum

(Bendz-Hellgren and Stenlid, 1995), as well as due to other

pathogens (Mallett and Volney, 1999) and pests (Camarero

et al., 2003), is better explained when tracking the tree growth

during longer periods.

Diameter reduction due to H. annosum infection is regarded

to be connected to the formation of a reaction zone when the

pathogen begins to colonize the sapwood (Bendz-Hellgren and

Stenlid, 1995). We did not identify any differences in growth

related to the reaction zone presence. Neither was any

interaction observed, between the treatment and the association

of a reaction zone with the growth. The effect of a reaction zone

on tree growth should be tested comparing trees before and after

the reaction zone formation. In our experiment, it could be that

most of the rotted trees presented in 2007 were too decayed for

testing this association. The fact that in the 12.7% of the trees

the pathogen had reached the cambium, thus producing resin

flow, may support that theory. The low isolation success of H.

annosum from rotted cores could also relate to a very advanced

decay of the sampled trees. Therefore, it is likely that most of

the rotted trees, without a reaction zone, had one prior to our

sampling, but in 2007 the reaction zone was no longer present at

stump height.

Acknowledgements

We are grateful to the landowners of Christinehofs gods for

hosting the experiment. Nicklas Samils was funded by a grant

to Jan Stenlid from Swedish Research Council for Environ-

ment, Agricultural Sciences and Spatial Planning (FORMAS).

Jonas Oliva was funded by the scholarship 2006BE00500 from

the DURSI-GENCAT. Field assistance by Maria Falk is

acknowledged.

References

Bazzigher, G., Schmid, P., 1969. Sturmschaden und Faule. Schweiz. Z. For-

stwes. 120, 521–535.

Bendz-Hellgren, M., Stenlid, J., 1995. Long-term reduction in the diameter

growth of butt rot affected Norway spruce, Picea abies. Forest Ecol.

Manage. 74, 239–243.

Bendz-Hellgren, M., Stenlid, J., 1998. Effects of clear-cutting, thinning, and

wood moisture content on the susceptibility of Norway spruce stumps to

Heterobasidion annosum. Can. J. Forest Res. 28, 759–765.

Berglund, M., Ronnberg, J., 2004. Effectiveness of treatment of Norway spruce

stumps with Phlebiopsis gigantea at different rates of coverage for the

control of Heterobasidion. Forest Pathol. 34, 233–243.

Berglund, M., Ronnberg, J., Holmer, L., Stenlid, J., 2005. Comparison of five

strains of Phlebiopsis gigantea and two Trichoderma formulations for



treatment against natural Heterobasidion spore infections on Norway spruce

stumps. Scand. J. Forest Res. 20, 12–17.

Brandtberg, P.-O., Johansson, M., Seeger, P., 1996. Effects of season and urea

treatment on infection of stumps of Picea abies by Heterobasidion annosum

in stands on former arable land. Scand. J. Forest Res. 11, 261–268.

Camarero, J.J., Martın, E., Gil-Pelegrın, E., 2003. The impact of a needleminer

(Epinotia subsequana) outbreak on radial growth of silver fir (Abies alba) in

the Aragon Pyrenees: a dendrochronological assessment. Dendrochrono-

logia 21, 3–12.

Clopper, C.J., Pearson, E.S., 1934. The use of confidence or fiducial limits

illustrated in the case of the binomial. Biometrika 26, 404–413.

Holdenrieder, O., Greig, B.J.W., 1998. Biological methods of control. In:

Woodward, S., Stenlid, J., Karjalainen, R., Huttermann, A. (Eds.), Heter-obasidion annosum: Biology, Ecology, Impact and Control. CAB Interna-

tional, Wallingford, New York, pp. 235–258.

Johansson, M., Brandtberg, P.O., 1994. Environmental conditions influencing

infection of Norway spruce stumps by Heterobasidion annosum and effect

of urea treatment. In: Johansson, M., Stenlid, J. (Eds.), Proc. 8th Int. Conf.

Root and Butt Rots, Sweden and Finland, August 9–16, 1993. SLU,

Uppsala, pp. 668–674.

Johansson, S.M., Pratt, J.E., Asiegbu, F.O., 2002. Treatment of Norway spruce

and Scots pine stumps with urea against the root and butt rot fungus

Heterobasidion annosum - possible modes of action. Forest Ecol. Manage.

157, 87–100.

Korhonen, K., Capretti, P., Karjalainen, R., Stenlid, J., 1998. Distribution of

Heterobasidion annosum intersterility groups in Europe. In: Woodward,

S., Stenlid, J., Karjalainen, R., Huttermann, A. (Eds.), Heterobasidion

annosum: Biology, Ecology, Impact and Control. CAB International,

Wallingford, New York, pp. 93–104.

Linden, M., Vollbrecht, G., 2002. Sensitivity of Picea abies to butt rot in pure

stands and in mixed stands with Pinus sylvestris in southern Sweden. Silva

Fennica 36, 767–778.

Mallett, K.I., Volney, W.J.A., 1999. The effect of Armillaria root disease on

lodgepole pine tree growth. Can. J. Forest Res. 29, 252–259.

Morrison, D.J., Johnson, A.L.S., 1978. Stump colonization and spread of Fomes

annosus 5 years after thinning. Can. J. Forest Res. 8, 177–180.

Moykkynen, T., Miina, J., 2002. Optimizing the management of a butt-rotted

Picea abies stand infected by Heterobasidion annosum from the previous

rotation sensitivity of Picea abies to butt rot in pure stands and in mixed

stands with Pinus sylvestris in southern Sweden. Scand. J. Forest Res. 17,

47–52.

Nicolotti, G., Gonthier, P., 2005. Stump treatment against Heterobasidion with

Phlebiopsis gigantea and some chemicals in Picea abies stands in the

western Alps. Forest Pathol. 35, 365–374.

Niemela, T., Korhonen, K., 1998. Taxonomy of the genus Heterobasidion. In:

Woodward, S., Stenlid, J., Karjalainen, R., Huttermann, A. (Eds.), Heter-obasidion annosum : Biology, Ecology, Impact and Control. CAB Inter-

national, Wallingford, New York, pp. 27–33.

Nilsson, C., Stjernquist, I., Barring, L., Schlyter, P., Jonsson, A.M., Samuelsson,

H., 2004. Recorded storm damage in Swedish forests 1901–2000. Forest

Ecol. Manage. 199, 165–173.

Pratt, J.E., Johansson, M., Huttermann, A., 1998. Chemical control of

Heterobasidion annosum. In: Woodward, S., Stenlid, J., Karjalainen,

R., Huttermann, A. (Eds.), Heterobasidion annosum: Biology, Ecology,

Impact and Control. CAB International, Wallingford, New York, pp. 259–

282.

Pratt, J.E., Niemi, M., Sierota, Z.H., 2000. Comparison of three products based

on Phlebiopsis gigantea for the control of Heterobasidion annosum in

Europe. Biocont. Sci. Technol. 10, 467–477.

Pratt, J.E., Redfern, D.B., 2001. Infection of Sitka spruce stumps by spores

of Heterobasidion annosum: control by means of urea. Forestry 74, 73–

78.

Redfern, D.B., Stenlid, J., 1998. Spore dispersal and infection. In: Woodward,

S., Stenlid, J., Karjalainen, R., Huttermann, A. (Eds.), Heterobasidion

annosum: Biology, Ecology, Impact and Control. CAB International, Wall-

ingford, New York, pp. 105–124.

Rishbeth, J., 1951. Observations on the biology of Fomes annosus, with

particular reference to East Anglian pine plantations. III. Natural and




+ Models


experimental infection of pines, and some factors affecting severity of the

disease. Ann. Bot. 15, 221–246.

Ronnberg, J., Sidorov, E., Petrylaite, E., 2006. Efficacy of different concentra-

tions of Rotstop1 and Rotstop1S and imperfect coverage of Rotstop1S

against Heterobasidion spp. spore infections on Norway spruce stumps.

Forest Pathol. 36, 422–433.

Schabenberger, O., Pierce, F.J., 2002. Contemporary Statistical Models for the

Plant and Soil Sciences. CRC Press LLC, Boca Raton, FL.

Stenlid, J., 1985. Population structure of Heterobasidion annosum as deter-

mined by somatic incompatibility, sexual incompatibility, and isozyme

patterns. Can. J. Bot. 63, 2268–2273.

Stenlid, J., 1987. Controlling and predicting the spread of Heterobasidion

annosum from infected stumps and trees of Picea abies. Scand. J. Forest

Res. 2, 187–198.

Stenlid, J., Redfern, D.B., 1998. Spread within the Tree and Stand. In:

Woodward, S., Stenlid, J., Karjalainen, R., Huttermann, A. (Eds.),

Heterobasidion annosum: Biology, Ecology, Impact and Control. CAB

International, Wallingford, New York, pp. 125–141.

Stenlid, J., Wasterlund, I., 1986. Estimating the frequency of stem rot in Picea

abies using an increment borer. Scand. J. Forest Res. 1, 303–308.

Thor, M., 2003. Operational stump treatment against Heterobasidion annosum

in European forestry – Current situation. In: LaFlamme, G., Berube, J.,



Bussieres, G. (Eds.), Root and butt rot of forest trees. Proceedings of the

IUFRO Working Party 7.02.01, Quebec City, Canada, 16–22 September

2001. Canadian Forest Service, Information Report LAU-X-126, pp. 170–

175.

Thor, M., Arlinger, J.D., Stenlid, J., 2006. Heterobasidion annosum root rot in

Picea abies: Modelling economic outcomes of stump treatment in Scandi-

navian coniferous forests. Scand. J. Forest Res. 21, 414–423.

Thor, M., Stenlid, J., 2005. Heterobasidion annosum infection of Picea abies

following manual or mechanized stump treatment. Scand. J. Forest Res. 20,

154–164.

Westlund, A., Nohrstedt, H., 2000. Effects of stump-treatment substances for

root-rot control on ground vegetation and soil properties in a Picea abies

forest in Sweden. Scand. J. Forest Res. 15, 550–560.

Whitney, R.D., Fleming, R.L., Zhou, K., Mossa, D.S., 2002. Relationship of

root rot to black spruce windfall and mortality following strip clear-cutting.

Can. J. Forest Res. 32, 283–294.

Vasiliauskas, R., Lygis, V., Thor, M., Stenlid, J., 2004. Impact of biological

(Rotstop) and chemical (urea) treatments on fungal community structure in

freshly cut Picea abies stumps. Biol. Control 31, 405–413.

Vollbrecht, G., Jorgensen, B.B., 1995. Modelling the incidence of butt rot

in plantations of Picea abies in Denmark. Can. J. Forest Res. 25, 1887–

1896.



Documents

Urea treatment reduced Heterobasidion annosum s.l. root rot in Picea abies after 15 years