Full text of DOI:10.1093/forestry/73.5.457

Receptivity of Picea sitchensis
stum ps to infection by
Heterobasidion annosum
basidiospores
C.M. WOODS1, S. WOODWARD1 AND D.B. REDFERN2
1
Department of Forestry, University of Aberdeen, MacRobert Building, 581 King Street, Aberdeen AB24 5UA,
Scotland
2
Forest Research, Northern Research Station, Roslin, Midlothian EH25 9SY, Scotland
Summary
Picea sitchensis stumps were inoculated with Heterobasidion annosum basidiospores either
immediately or 24 h, 7 days or 28 days after cutting, in order to determine the length of time they
remained susceptible to infection. Control stumps were inoculated with sterile water; those that
became colonized were presumed to have been infected by natural inoculum. The degree of
colonization of inoculated stumps declined when spores were applied more than 24 h after cutting
but was still greater than in the control stumps at 7 days. Spores applied at 28 days did not result in
stump infection. These data indicate that stump protection measures applied after felling must
remain effective for at least 7 days, and that if stump treatment is not applied immediately after
cutting, it could still have some protective value up to 7 days later.
Hallaksela, 1979; Brandtberg et al., 1996) and
the number of spores available at the stump
surface (Redfern et al., 1997). In Sitka spruce
(Picea sitchensis (Bong.) Carr), stump moisture
content is an important factor influencing the
success of infection (Redfern, 1993). In addition,
Redfern (1993) found a positive correlation
between infection in the heartwood and
sapwood, which suggests there are also intrinsic
differences in stump susceptibility.
Research on control measures has led to stump
treatment with chemicals such as creosote,
sodium nitrite and currently urea (Rishbeth,
1959a, b; Phillips and Greig, 1970) and to bio-
logical control on pine (Pinus spp.) using the
Introduction
Heterobasidion annosum (Fr.) Bref. (Fomes
annosus (Fr.) Cke) causes a serious root and butt
rot of conifers in the North Temperate region
(Hodges, 1969). It becomes established in first
rotation plantations principally by basidiospore-
infection of fresh stump surfaces (Rishbeth,
1951a, b). Following spore germination, H.
annosum grows from the stump surface into the
body of the stump and roots and infects neigh-
bouring trees through root contacts. The success
of stump colonization is affected by factors such
as temperature (Yde-Andersen, 1962; Driver
and Ginns, 1964, 1969; Ross, 1973; Kallio and
© Institute of Chartered Foresters, 2000
Forestry, Vol. 73, No. 5, 2000

458
FO R EST RY
fungus Phlebiopsis gigantea (Fr.) Jülich [Penio- Aberdeenshire. The spore deposits were collected
phora gigantea (Fr.) Massee] (Rishbeth, 1963). after 24 h, air-dried for 1 h at room temperature,
Recently, in Scandinavia, a commercial formu- and stored at 2°C for up to 7 days. Basidiospore
lation of P. gigantea, ‘Rotstop’, has also been used suspensions were made up 5 min before inocula-
successfully on Norway spruce (Picea abies (L.) tion by immersing the slides in a flask containing
Karst.) (Korhonen et al., 1994).
1 l of sterile distilled water and gently agitating
Chemical or biological control agents are the dry spores with a small paintbrush. Sufficient
applied to stumps immediately after cutting and basidiospores were used to form a cloudy sus-
must remain effective for at least the time during pension.
which stumps are susceptible to infection (Pratt
and Redfern, 1989). This period can vary with
tree species. In North America, Ross (1968)
Experimental procedure
reported that Loblolly pine (Pinus taeda L.) The experiment was set up in an unthinned first
stumps were susceptible to H. annosum for up to rotation stand of 24-year-old Sitka spruce in Bun-
12 days after cutting, after which time a rapid zeach Forest, Aberdeenshire, Scotland (57°11ꢁ N,
increase in P. gigantea appeared to limit coloniz- 3°01ꢁ W). On 12 August 1994, 120 trees were
ation. Cobb and Schmidt (1964) found that felled leaving stumps 40–45 cm tall. Stumps were
stumps of white pine (Pinus strobus L.) inocu- in four rows with four rows of trees between each
lated with conidia were highly susceptible to H. treatment row. Two days later, at the start of the
annosum infection for only 3 days, whereas Cobb experiment, stumps were all re-cut to a height of
and Barber (1968) found that Redwood (Sequoia 20 cm above the level of the buttress roots.
sempervirens (D. Don.) Endl.), Douglas fir Stumps were inoculated with either a basidio-
(Pseudotsuga menziesii (Mirb.) Franco) and spore suspension of H. annosum or with sterile
Ponderosa pine (Pinus ponderosa Laws.) were distilled water, applied immediately, 1 day, 7 days
susceptible for at least 4 weeks. In Europe, Yde- or 28 days after re-cutting. The eight treatments
Andersen (1962) suggested that Norway spruce were allocated at random in 15 replicate blocks,
stumps were susceptible to natural infection for with each block consisting of eight consecutive
no more than 1 month and Schönhar (1979) stumps along a row. For each time treatment,
found that they were only receptive to conidial control stumps were treated first, followed by the
infection for 28 days, with most infection occur- stumps to be inoculated with the basidiospore
ring the day after felling. Rishbeth (1951a) sug- suspension.
gested that competition from fungi, such as P.
A new pair of latex medical gloves was worn
gigantea, limited to only 2–3 weeks the period for each treatment and swabbed down with 75
during which Scots pine (Pinus sylvestris L.) per cent ethanol before use. Spore suspensions
stumps were susceptible. No equivalent data are were shaken vigorously prior to inoculation and
available for Sitka spruce and this paper reports agitated at regular intervals. Stumps were inocu-
the results of an experiment to determine the lated by applying water or a freshly made
receptivity of stumps of this species within basidiospore suspension dropwise using different
28 days of cutting.
sterile pipettes. The volume of suspension
required to wet the stump surface was recorded,
together with the under-bark diameter of the
stump.
Each stump was covered with a polythene sheet
for 24 h after inoculation to prevent spores being
washed off by rain. Contact between the poly-
thene and the stump surface was prevented by
placing a piece of 15 mm diameter plastic tubing
across the stump surface and stapling the poly-
thene to the stump sides.
Materials and methods
Basidiospore inoculum
Heterobasidion annosum basidiospores were col-
lected on glass slides placed horizontally in the
bottom of 10 ꢀ 10 cm glass staining dishes
beneath basidiocarps growing on Douglas fir
stumps and fallen trees in Kirkhill Forest,
Immediately after inoculation, the viability of

H E T E R O BASI D I O N AN N O SU M IN FEC T IO N O F SIT KA SPR UC E ST UM PS
459
the spore suspension was assessed by plating colonies were transferred to tracing paper and
aliquots (1 ml) of each of six successive 10-fold photocopied. The boundary between heartwood
dilutions of each suspension onto a selective and sapwood was identified on the basis of wood
medium (Kuhlman and Hendrix, 1962). There colour and moisture content. For the purposes of
were three replicate dishes per dilution. Cultures this study the heartwood was considered to be the
were incubated at 22°C in the dark and examined dry inner area of the stump including the lighter
daily from 3 until 7 days after inoculation for H. coloured transition zone that surrounds it, and
annosum colonies. The concentration of viable the sapwood was the wetter outer area. The
spores was calculated from the dilution that difference between these tissues is clearly defined
yielded no more than 25 colonies per Petri dish, in freshly cut stump discs. The stump outline was
and a haemocytometer count of the total number cut out and weighed, followed by the heartwood
of spores. Spore concentration data were com- and sapwood areas and finally the H. annosum
bined with data on the volume of spore suspen- colonies in the heartwood and sapwood separ-
sion applied to produce a figure for the number ately. From these data the percentage of the cross-
of basidiospores applied to each stump.
sectional area of heartwood and sapwood
occupied by H. annosum was calculated.
Sampling and assessment of colonization by H.
annosum
Ancillary observations
Stumps were sampled 7–9 months after inocula-
tion by cutting two 3 cm-thick discs from the top
with a chain saw. Discs were placed in individual
plastic bags after cutting and transported to the
laboratory. Within 24 h of sampling, the bark was
removed and discs were washed with running tap
water in order to remove any sawdust that might
impede the subsequent observation of fungal
colonies and be a possible source of contami-
nation (Morrison and Redfern, 1994). After
drying for 2 h in a vertical position, discs were
wrapped individually in newspaper (Rishbeth,
1957) and placed vertically in clean plastic dust-
bins that had been swabbed out with 70 per cent
ethanol prior to use. Each bin was covered by a
lid and aeration was provided by seven evenly
spaced 1 cm diameter holes drilled 7 cm below the
rim. The bins were incubated for 7–10 days out-
doors, where the ambient temperature did not
exceed 10°C. If the temperature remained around
0°C for several days, the bins were transferred to
room temperature 3 days prior to observing the
discs under a dissecting microscope for conidio-
In P. sitchensis, some stumps remain alive due to
the formation of root grafts with neighbouring
trees, and previous observations (Redfern, 1982,
1993) have suggested that these stumps may be
more susceptible to H. annosum than those that
die quickly. The incidence of living stumps was
therefore determined at the end of the experiment
by examining the condition of the phloem and
vascular cambium tissues on the lowest sample
disc. When the stump dies, these tissues deterio-
rate, causing the bark to loosen.
The incidence of other stump fungi was also
noted, particularly Melanotus proteus (Kalchbr.)
Singer, a small crepitoid hymenomycete common
on Sitka spruce stumps, with a distinctive white
mycelium (Redfern, 1991, 1993; Woods, 1996).
The area occupied by this fungus on incubated
discs was outlined and measured in the same way
as for H. annosum.
Statistical analysis
phores of H. annosum. Colonies were outlined The figures for the percentage of cross-sectional
with an indelible felt tip pen. area colonized by the fungi were transformed to
The cross-sectional area of heartwood and the arcsine scale prior to conducting an analysis
sapwood occupied by H. annosum on the upper of variance (ANOVA) to determine whether
surface of the lower disc (i.e. at a depth of c. treatment differences were significant at the 95
38 mm) from each stump was measured in the per cent level. Tukey’s test was used to determine
following manner. The outline of the stump disc, which treatment differences were significant at
heartwood and sapwood areas and H. annosum the 95 per cent level.

460
FO R EST RY
Results
heartwood than in the sapwood, in which
colonization was negligible by day 7.
The mean number of viable spores applied to
Period of stump susceptibility
The incidence of infection for each treatment is the stumps is shown in Table 1. No viable spores
given in Table 1. Up to 7 days after cutting, the were detected in the water used to inoculate
proportion of stumps infected by H. annosum control stumps.
was much greater among those that were inocu-
lated than among the controls, whereas at
28 days the proportions were little different.
Pattern of stump colonization
The area occupied by H. annosum in the In stumps inoculated both immediately and 1 day
stumps is shown in Table 2. It was significantly after cutting, H. annosum either occupied large
greater in stumps inoculated with basidiospores irregular areas within the heartwood and
than in the controls for up to 7 days after cutting. sapwood (Figure 1a) or occupied a single exten-
However, in stumps inoculated at day 7, the area sive area within the heartwood (Figure 1b). In
was smaller than in those inoculated at earlier stumps inoculated after
7 days, heartwood
times. Colonization was much greater in the colonization was less extensive and occurred in
Table 1: Infection of Sitka spruce stumps by H. annosum following inoculation with basidiospores at various
times after cutting
Inoculation with H. annosum
Inoculated with
sterile water
————————————————————
Mean no. of viable
Delay after cutting
(days)
H. annosum spores
cm–2 stump surface
No. of stumps
infected*
No. of stumps
infected*
0
1
7
6.6 ꢀ 103
92.7 ꢀ 103
87.1 ꢀ 103
350.4 ꢀ 103
15
15
13
3
2
1
1
0
28
*Out of 15.
Table 2: Colonization of Sitka spruce stumps by H. annosum following inoculation with basidiospores or sterile
water at various times after cutting
Mean percentage cross-sectional area occupied
—————————————————————————————————————————–
Heartwood
Sapwood
Total
—————————————– ————————————— ——————————————
Delay after
cutting (days) H. annosum
Sterile
water
Sterile
water
Sterile
water
H. annosum
H. annosum
0
1
7
37.2a
50.4a
15.6b
0.0*c
0.0*
0.0*
0.0*
0.0
4.4a
0.0
0.0
0.0
0.0
15.8a
15.6a
4.3b
0.0*
0.0*
0.0*
0.0
2.3ab
0.5ab
0.0*b
28
0.0*c
Mean values for the heartwood, sapwood and total areas inoculated with H. annosum or sterile water followed
by dissimilar letters differ significantly (P < 0.05). Comparisons should not be made between columns.
*Trace = not measurable.

H E T E R O BASI D I O N AN N O SU M IN FEC T IO N O F SIT KA SPR UC E ST UM PS
461
Figure 1. Distribution of H. annosum in representative P. sitchensis stumps 7 months after inoculating the
stump surface with H. annosum basidiospores applied (a) immediately, (b) 1 day after cutting, (c, d) 7 days
after cutting and (e) 28 days after cutting. Areas occupied by H. annosum are outlined. The dotted line indi-
cates the boundary between heartwood and sapwood. Bar represents 25 mm.

462
FO R EST RY
discrete areas (Figure 1c, d). In some stumps it
Broadly similar results have been obtained for
was absent entirely. Colonization of the sapwood other conifers, but the reported rate of decline in
was rare in stumps inoculated 28 days after receptivity has varied (Rishbeth, 1951a; Cobb and
cutting, and most colonies occupied small areas Schmidt, 1964; Yde-Anderson, 1962; Cobb and
within the heartwood (Figure 1e).
Barber, 1968; Ross, 1968; Schönhar, 1979). Apart
from the effects of environmental factors (Yde-
Anderson, 1962; Driver and Ginns, 1964, 1969;
Ross, 1973; Kallio and Hallaksela, 1979; Brandt-
Colonization by other fungi
M. proteus was found on 68.3 per cent of inocu- berg et al., 1996; Redfern, 1993; Redfern et al.,
lated stumps and on only 46.7 per cent of stumps 1997), some variation may result from the degree
treated with sterile distilled water. Colonization of host specificity shown by the different species
was most extensive in stumps inoculated with H. of Heterobasidion (previously referred to as inter-
annosum 1 day after cutting (Table 3), and was sterility groups; see Niemelä and Korhonen, 1998)
greater than in stumps inoculated with sterile present in Europe, and the relative abundance of
water for three out of the four inoculation times, inoculum of these species in different forest types.
but the differences were not significant. No other Some degree of host specificity in living trees has
Basidiomycotina were observed on the discs.
been suggested (Stenlid and Swedjemark, 1988;
Capretti et al., 1994), but there is conflicting evi-
dence on the importance of this factor in stump
infection (Harrington et al., 1989; Otrosina et al.,
Stump condition
At the time of sampling 29 out of 120 stumps 1992; Korhonen and Piri, 1994; Hanso et al.,
were alive. H. annosum was present in 28 per cent 1994). The basidiospore inoculum used in this
of these stumps whereas M. proteus was observed study originated from H. annosum sensu stricto
in only 10 per cent. By contrast the respective (Niemelä and Korhonen, 1998), as confirmed in
figures for dead stumps were 53 per cent and 72 molecular studies (Kasuga et al., 1993).
per cent.
It has been suggested that pine stumps become
less receptive to H. annosum with increasing age
because they are colonized by competing fungi
(Rishbeth 1951a; Ross, 1968). However, in this
study, in which M. proteus was the only other
Discussion
Sitka spruce stumps were highly susceptible to fungal colonist recorded, there was no evidence
colonization by H. annosum basidiospores up to from the frequency of colonization by the two
7 days after cutting but susceptibility declined to fungi in live and dead stumps that M. proteus
almost zero between 7 and 28 days. These results restricted infection by H. annosum. Both fungi
indicate that stump treatment must remain effec- were more common in dead stumps than live ones
tive for at least 7 days after felling and that if and M. proteus was no more common in stumps
treatment is delayed it could still have some pro- in which inoculation was delayed than in those
tective value if applied up to 7 days later.
inoculated earlier.
Table 3: Colonization of Sitka spruce stumps by M. proteus following inoculation with H. annosum
basidiospores at various times after cutting
Mean percentage cross-sectional area occupied by M. proteus
Delay after
——————————————————————————————
cutting (days)
Inoculation with H. annosum
Inoculation with sterile water
0
1
7
3.6
5.6
3.4
2.7
4.7
1.6
1.1
2.4
28

H E T E R O BASI D I O N AN N O SU M IN FEC T IO N O F SIT KA SPR UC E ST UM PS
463
Although the frequency of stump infection is a by the huge numbers of H. annosum spores
major determinant in the development of the applied.
disease within a stand, the ability of H. annosum
The low level of infection (8.3 per cent) in the
to survive within colonized stumps is also import- control stumps suggests that the risk of natural
ant. Several authors have reported a rapid decline infection in P. sitchensis was extremely low in this
in the survival of H. annosum in stumps, whether forest at the time the work was done. Similarly
inoculated or infected naturally (Dimitri et al., low levels (4.2 and 13.3 per cent) have been found
1971; Morrison and Johnson, 1978; Shaw, 1989; elsewhere in Scotland by Redfern (1993) and
Morrison and Redfern, 1994). The last authors Redfern et al. (1997). Nevertheless, the response
observed that H. annosum was absent from to inoculation suggests that if spore loads
stumps that 6 years previously had been infected increase, levels of infection could become much
only in the heartwood, whereas it was still present higher.
in those infected in the sapwood. In these latter
stumps the fungus had entered the roots and
infected neighbouring trees (Morrison and
Acknowledgements
Redfern, 1994). In the experiment reported here,
although there was little difference in the number
of stumps infected up to 7 days, the proportion in
which the sapwood was colonized declined from
53 per cent and 73 per cent in the immediate and
day 1 inoculations, respectively, to 20 per cent at
7 days. A consequence of this could be that
stumps colonized within 1 day of felling are more
likely to cause infections in surrounding trees
than those colonized later.
Unfortunately the number of viable spores
applied to stumps varied (more than 10-fold)
between inoculation times. The greatest number
was used on the oldest stumps (28 days) and it is
arguable that the reduced colonization resulting
from inoculation at this time was due to intra-
specific competition between genets rather than
to a decline in stump receptivity. However, this
seems unlikely as, although Redfern et al. (1997)
detected such an effect of competition, it was rela-
tively small. Furthermore the greater number of
spores applied at day 1 compared with the im-
mediate treatment was associated with increased
heartwood colonization.
Although the effect was not significant, M.
proteus was generally more common on stumps
inoculated with basidiospores than on those that
received only sterile water. Redfern et al. (1997)
observed that stumps inoculated with higher con-
centrations of H. annosum basidiospores were
colonized by a greater abundance of fungi such as
R. bicolor, H. fasciculare and M. proteus than
those inoculated with lower numbers of spores.
They suggested that colonization by these fungi
might have been favoured by the effect of mutual
C.M.W. gratefully acknowledges the Forestry Commis-
sion for funding this research and Buchan Forest Dis-
trict for providing a suitable field site. Thanks to Jim
Pratt for his advice on field work, Douglas Proudfoot
and George Walker for assistance in the field and Jean
Cooper for statistical advice.
References
Brandtberg, P.O., Johansson, M. and 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. For. Res. 11,
261–268.
Capretti, P., Gogglioli, V. and Mugnai, L. 1994 Inter-
sterility groups of Heterobasidion annosum in Italy:
distribution, hosts and pathogenicity tests. In Pro-
ceedings of the Eighth IUFRO Conference on Root
and Butt Rots. M. Johansson and J. Stenlid (eds).
Swedish University of Agricultural Sciences, Uppsala,
Sweden, pp. 218–226.
Cobb, F.W. and Barber, H.W. 1968 Susceptibility of
freshly cut stumps of Redwood, Douglas fir, and Pon-
derosa pine to Fomes annosus. Phytopathology 58,
1551–1557.
Cobb, F.W. and Schmidt, R.A. 1964 Duration of sus-
ceptibility of Eastern White pine stumps to Fomes
annosus. Phytopathology 54, 1216–1218.
Dimitri, L., Zycha, H. and Kliefoth, R. 1971 Unter-
suchungen über die bedeutung der stuben infektion
durch Fomes annosus für ausbreitung der rötfaule
der fichte. Forstwiss. Centralblatt 90, 104–107.
Driver, C.H. and Ginns, J.H., Jr. 1964 The effect of
climate on occurrence of Annosus root rot in thinned
slash pine plantations. Plant Dis. Rep. 48, 509–511.
Driver, C.H. and Ginns, J.H., Jr. 1969 Ecology of slash
pine stumps: fungal colonization and infection by
Fomes annosus. For. Sci. 15, 2–10.
inhibition between H. annosum genets or simply Hanso, S., Korhonen, K. and Hanso, M. 1994 Attack

464
FO R EST RY
of spruce and pine by S and P groups of Heteroba-
the western United States. Phytopathology 82,
540–545.
Phillips, D.H. and Greig, B.J.W. 1970 Some chemicals
to prevent stump colonization by Fomes annosus (Fr.)
Cooke. Ann. App. Biol. 66, 441–452.
Pratt, J.E. and Redfern, D.B. 1989 Stump treatment
against Fomes is vital in UK. Forestry and British
Timber 18, 33–34.
sidion annosum on forest and former agricultural
soils in Estonia. In Proceedings of the Eighth IUFRO
Conference on Root and Butt Rots. M. Johansson
and J. Stenlid (eds). Swedish University of Agri-
cultural Sciences, Uppsala, Sweden, pp. 254–259.
Harrington, T.C., Worrall, J.J. and Rizzo, D.M. 1989
Compatibility among host-specialised isolates of
Heterobasidion annosum from western North Redfern, D.B. 1982 Infection of Picea sitchensis and
America. Phytopathology 79, 290–296.
Hodges, C.S. 1969 Modes of infection and spread of
Pinus contorta stumps by Heterobasidion annosum.
Eur. J. For. Pathol. 12, 11–25.
Fomes annosus. Annu. Rev. Phytopathol. 7, Redfern, D.B. 1991 Melanotus proteus:
247–266.
a
newly
recorded colonist of Sitka spruce stumps in Britain
and potential competitor for Heterobasidion
Kallio, T. and Hallaksela, A-M. 1979 Biological control
of Heterobasidion annosum Fr. Bref. (Fomes
annosus) in Finland. Eur. J. For. Path. 9, 298–308.
Kasuga, T., Woods, C., Woodward, S. and Mitchelson,
K.R. 1993 Heterobasidion annosum 5.8S ribosomal
DNA and internal transcriber spacer sequence: rapid
a
annosum. Plant Pathol. 40, 483–486.
Redfern, D.B. 1993 The effect of moisture on infec-
tion of Sitka spruce stumps by basidiospores of
Heterobasidion annosum. Eur. J. For. Path. 23,
218–235.
identification of European intersterility groups by Redfern, D.B., Gregory, S.C. and Macaskill, G.A. 1997
ribosomal DNA restriction polymorphism. Curr.
Genetics 24, 433–436.
Korhonen, K. and Piri, T. 1994 The main hosts and
Inoculum concentration and the colonization of
Picea sitchensis stumps by basidiospores of Heter-
obasidion annosum. Scand. J. For. Res. 12, 41–49.
distribution of the S and P groups of Heterobasidion Rishbeth, J. 1951a Observations on the biology of
annosum in Finland. In Proceedings of the Eighth
IUFRO Conference on Root and Butt Rots. M.
Johansson and J. Stenlid (eds). Swedish University of
Agricultural Sciences, Uppsala, Sweden, pp.
260–267.
Korhonen, K., Lipponen, K., Bendz, M., Johansson, M.,
Ryen, I., Venn, K., Seiskari, P. and Niemi, M. 1994
Control of Heterobasidion annosum by stump treat-
ment with ‘Rotstop’, a new commercial formulation
Fomes annosus, with particular reference to East
Anglian Pine plantations. II. Spore production,
stump infection and saprophytic activity in stumps.
Ann. Bot. N.S. 15, 1–21.
Rishbeth, J. 1951b Observations on the biology of
Fomes annosus, with particular reference to East
Anglian Pine plantations. III. Natural and experi-
mental infection of pines, and some factors affecting
severity of the disease. Ann. Bot. N.S. 15, 221–246.
of Phlebiopsis gigantea. In Proceedings of the Eighth Rishbeth, J. 1957 Some further observations on Fomes
International Conference on Root and Butt Rots. M. annosus Fr. Forestry 30, 69–89.
Johansson and J. Stenlid (eds). Swedish University of Rishbeth, J. 1959a Stump protection against Fomes
Agricultural Sciences, Uppsala, Sweden, pp.
675–683.
annosus. I. Treatment with creosote. Ann. App. Biol.
47, 519–528.
Kuhlman, E.G. and Hendrix, F.F. 1962 A selective Rishbeth, J. 1959b Stump protection against Fomes
medium for the isolation of Fomes annosus. Phyto-
pathology 52, 1310–1312.
annosus. II. Treatment with substances other than
creosote. Ann. App. Biol. 47, 529–541.
Morrison, D.J. and Johnson, A.L.S. 1978 Stump Rishbeth, J. 1963 Stump protection against Fomes
colonization and spread of Fomes annosus 5 years
after thinning. Can. J. For. Res. 8, 177–180.
annosus. III. Inoculation with Peniophora gigantea.
Ann. App. Biol. 52, 63–77.
Morrison, D.J. and Redfern, D.B. 1994 Long-term Ross, E.W. 1968 Duration of stump susceptibility of
development of Heterobasidion annosum in
basidiospore-infected Sitka spruce stumps. Plant
Pathol. 43, 897–906.
Niemelä, T. and Korhonen, K. 1998 Taxonomy of the
genus Heterobasidion. In Heterobasidion annosum:
Biology, Ecology, Impact and Control. S. Woodward,
J. Stenlid, R. Karjalainen and A. Hüttermann (eds).
CAB International, Wallingford, pp. 27–33.
Loblolly pine to infection by Fomes annosus. For. Sci.
14, 206–211.
Ross, E.W. 1973 Fomes annosus in the southeastern
United States: relation of environmental and biotic
factors to stump colonisation and losses in the resid-
ual stand. USDA, Forest Service, Tech. Bull. 1459,
26 pp.
Schönhar, S. 1979 Susceptible period of the freshly-cut
surface of spruce stumps to infection by Fomes
annosus spores. Allg. Forst- Jagdz. 150, 162–163.
Otrosina, W.J., Chase, T.E. and Cobb, F.W. 1992
Allozyme differentiation of intersterility groups of
Heterobasidion annosum isolated from conifers in Shaw, C.G., III 1989 Root disease threat minimal in

H E T E R O BASI D I O N AN N O SU M IN FEC T IO N O F SIT KA SPR UC E ST UM PS
465
young stands of Western Hemlock and Sitka spruce Yde-Andersen, A. 1962 Seasonal incidence of stump
in Southeastern Alaska. Plant Dis. 73, 573–577.
Stenlid, J. and Swedjemark, G. 1988 Differential
growth of S- and P-isolates of Heterobasidion
annosum in Picea abies and Pinus sylvestris. Trans.
Brit. Mycol. Soc. 90, 209–213.
infection in Norway spruce by air-borne Fomes
annosus spores. For. Sci. 8, 98–103.
Woods, C.M. 1996 The fungal ecology of Sitka spruce
stumps. Ph.D. thesis. University of Aberdeen.
Received 15 April 1999