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Keywords:

  • Betula pubescens;
  • Betula pendula;
  • birch dieback;
  • canker;
  • field survey

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Betula pendula and B. pubescens were surveyed at nine Scottish Woodland Grant Scheme (WGS) sites in 2004 to assess the incidence and severity of two fungal pathogens, Anisogramma virgultorum and Marssonina betulae, and their association with crown dieback. Of the surveyed trees, 47% had at least 40% crown dieback, with B. pendula more severely affected than B. pubescens at most sites. Overall, 57% of surveyed birch trees had A. virgultorum and 28% had M. betulae, with the incidence of trees infected with both species varying among sites. Incidence and severity of A. virgultorum were greater on B. pubescens than on B. pendula, whereas the reverse was true for M. betulae. The relationship between incidence of M. betulae foliar disease and sunken cankers was significant, with 83% of M. betulae-infected trees having these cankers. The presence of M. betulae foliar disease resulted in a greater percentage of crown dieback compared with non-infected trees in both birch species, whereas the presence of A. virgultorum caused greater crown dieback in B. pubescens only. Across all sites and both birch species, as severity of infection with either A. virgultorum or sunken cankers increased, so did the severity of crown dieback. This study showed that A. virgultorum and M. betulae appear to contribute significantly to birch dieback at the nine sites surveyed.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

In Scotland, Betula pendula (silver birch) and B. pubescens (downy birch) are the most commonly found native broadleaf species (Forestry Commission, 2004). During the 1990s, about 73 000 ha of new native woodland was created in Scotland under the Woodland Grant Scheme (WGS), primarily aimed at improving the landscape and enhancing biodiversity and quality of life for people through natural regeneration or planting of new woodlands. Both Betula spp. are major broadleaved components in WGS plantings (Forestry Commission, 2001). In recent years, over 20 WGS sites in Scotland have reported dieback of young birch trees approximately 5–10 years old (Green & MacAskill, 2007). Following planting, the trees tend to grow well for a few years before crown dieback begins, typically starting from the lower crown upwards and the outer crown inwards (Green, 2005). Specific symptoms include sunken cankers and fissures on older stems and branches, and discrete lesions and tip dieback on young shoots. In a preliminary survey of several WGS sites in Scotland, a number of fungi were isolated from affected trees, two of which were found to be pathogenic and suspected causal agents of shoot dieback: Anisogramma virgultorum and Marssonina betulae (Green, 2005).

Anisogramma virgultorum is a pathogenic ascomycete belonging to the order Diaporthales. Ascospores of the fungus infect young shoots of Betula spp. to cause black, elongated stromatal cankers, which extend through the cortex causing malformation of the branch (Massee, 1914; Froidevaux & Müller, 1972). Stromata contain numerous flask-shaped perithecia in which asci and ascospores develop (Dennis, 1968). Only limited information is available on the distribution and impact of A. virgultorum on birch in Britain and reports are conflicting. Massee (1914) suggested that the fungus was probably widely distributed in Scotland and occurred on trees throughout Great Britain. However, Dennis (1968) and Ellis & Ellis (1985) described the occurrence of A. virgultorum as rare. The fungus has also been reported on birch in Europe (Vleugel, 1917; Karlsson & Albrektson, 2001; Witzell & Karlsson, 2002) and North America (Theissen & Sydow, 1916; Froidevaux & Müller, 1972). Reports on the pathogenicity of this fungus are conflicting (Vleugel, 1917; Peace, 1962). Artificial inoculation of ascospores of A. virgultorum onto B. pendula and B. pubescens seedlings resulted in the formation of dark brown-black, erumpent cankers on a small number of young, expanding shoots (Green, unpublished data). In an experiment in which 30 healthy seedlings of both birch species were placed around the base of trees naturally infected with A. virgultorum at a field site during early to mid-spring, 68% of exposed seedlings developed stromatal cankers typical of the fungus on current-season shoots during late summer of the same season (Green, unpublished data). One year later, 60% of shoots with A. virgultorum cankers had died back (Green, unpublished data). Seedlings from the same provenance not exposed to the fungus remained unaffected.

Marssonina betulae is a common foliar pathogen on birch throughout Europe, causing characteristic leaf spots as well as lesions on young shoots. This deuteromycete fungus, for which a sexual state is unknown, infects leaves and young shoots in spring and summer via conidia. Previously, damage caused by M. betulae was thought to be limited to leaves and young, small shoots, and its degree of aggressiveness was considered to be weak (Peace, 1962; Bäucker & Eisenhauer, 2001). However, inoculation studies conducted with M. betulae on B. pendula found that it caused sunken cankers on shoots and branches leading to progressive dieback (Green & MacAskill, 2007).

Detailed information is lacking on the extent of the birch dieback problem at WGS sites in Scotland, the frequency of occurrence of these two fungal pathogens, and the degree to which these fungi are responsible for the observed symptoms of crown dieback of Betula spp. at these sites. To address this, a survey of nine Scottish WGS sites at which birch dieback had been reported and both A. virgultorum and M. betulae were known to be present was undertaken in August and September 2004 with the following objectives: (i) to evaluate the frequency and severity of crown dieback, (ii) to record the incidence of A. virgultorum and M. betulae, (iii) to correlate the incidence of M. betulae foliar infection with the incidence of sunken cankers (not associated with A. virgultorum), (iv) to determine the severity of A. virgultorum and sunken cankers, and their relationship with severity of crown dieback, and (v) to compare the incidence and severity of A. virgultorum and M. betulae on B. pendula and B. pubescens.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Study sites and sampling design

In August and September 2004, a survey was conducted of B. pendula and B. pubescens at nine WGS sites in Scotland, at which dieback of birch had been reported by woodland owners. From previous enquiries, A. virgultorum was known to be present at seven of the nine sites, while M. betulae had not previously been reported at these sites (Table 1, Fig. 1). Within each site, five plots were selected based on areas where birch had been planted. The nine survey sites varied greatly in size and plots were chosen to ensure as wide an area as possible was surveyed on each site so that the survey was representative of each site as a whole. The locations of survey plots within a site were therefore very variable from site to site. In each plot, a central point (tree) was marked with flagging tape and its precise location recorded using a GPS. From this centre point, a transect was laid out along each of the four cardinal points of the compass. The first five living birch trees located either directly on each transect, or closest to it, were selected for surveying. At some sites transect layout varied from this design according to birch tree density, size of the planting and planting pattern. At all sites, 20 trees within each of the five plots were surveyed, giving a total of 100 surveyed trees per site.

Table 1.  Characteristics of the nine sites surveyed in this study
Site nameRegion and GPS co-ordinatesYear(s) of plantingBirch species present (number of trees surveyed per species)ProvenanceAspect and slopeSoil typeAltitude (m a.s.l.)
Site 1Dumfriesshire 55°20′N 03°57′W1989/90 (B. pendula)B. pendula (6); B. pubescens (94)Unknown for B. pendula; B. pubescens naturally regeneratedN/NW shallowPeat on mineral soil290–295
Site 2Dumfriesshire 55°07′N 03°44′W1994B. pubescens (100)UnknownN/NW Shallow/moderate/moderate to steepMineral soil160–180
Site 3Dumfriesshire 55°14′N 04°07′W1991 beat-ups in 1996/97 and 2001B. pendula (27); B. pubescens (73)UnknownE/SE Shallow/Shallow to moderateFree draining stony brown earth/Mineral soil, fairly free draining brown earth300–350
Site 4Dumfriesshire 55°12′N 04°04′W1995B. pubescens (100)UnknownSE moderateBrown earth/peaty gleys280–330
Site 5Perthshire 56°18′N 04°07′W1994B. pendula (61); B. pubescens (39)UnknownNW moderatePeat and gravel250–270
Site 6Inverness-shire 57°22′N 03°11′W1993B. pendula (11); B. pubescens (89)Local provenanceN/NW Shallow to moderateGleys, peat and peaty gleys330–390
Site 7Banffshire 57°23′N 03°36′W1991B. pendula (90); B. pubescens (10)Local provenanceE/SE Shallow to moderatePeat320–410
Site 8Inverness-shire 57°49′N 04°09′W1989, 1990, 1991B. pendula (63); B. pubescens (37)Genetically improved Scottish stock; Black Isle provenance; some unknownN/NW moderateBrown earth at lower elevation, shallow podzol, peaty soils and peaty iron pan, indurated at higher altitude100–200
Site 9Ross & Cromarty 57°43′N 04°53′W1993/94B. pendula (34); B. pubescens (66)UnknownN/NE ShallowPeat260–330
image

Figure 1. Map of Scotland indicating the location of nine Woodland Grant Scheme sites surveyed in this study.

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Site and plot information

For each WGS site the following general information was recorded: other tree species present, birch provenance (where known), planting year and total area planted with birch. Plot-specific data such as aspect, altitude and soil type were also noted (Table 1). At sites 2 and 4, only B. pubescens had been planted, while a mixture of both birch species was present at all other sites. Birch trees in all plots had been planted, except for site 1, where B. pubescens had regenerated naturally and only B. pendula had been planted, and one plot at site 6, where naturally regenerated birch was assessed.

Tree assessments

For each individual survey tree the following parameters were assessed. Stem diameter at breast height (DBH) was measured at 1·3 m above ground, while stem diameter for trees less than 1·5 m high was measured 50 cm above ground. Tree height in metres was estimated visually. A crown dieback score was given by assessing the reduction in living crown density caused by shoot dieback in 5% classes using the following rating system: 0 = no shoot dieback; 5 = 1–5% shoot dieback; 10 = 6–10% shoot dieback, and so on until 100% reduction/dieback indicating tree death (Innes, 1990). Stage of crown dieback was recorded as 0 = no dieback, 1 = dieback restricted to relatively thin branches, 2 = several large branches involved, or 3 = main stem involved in the lower and middle part of the crown. Location of dieback was recorded as 1 = lower part of the crown affected, 2 = lower and middle parts of the crown, or 3 = whole crown affected.

The presence or absence of A. virgultorum infection was recorded by observation of characteristic stromatal lesions and/or old stromatal cankers, which were clearly identifiable in the field (Fig. 2a,b). Although M. betulae is known to cause sunken cankers (Green & MacAskill, 2007) the presence of M. betulae foliar disease in the field could only be confirmed by microscopic analysis of infected leaves since the fungus has not been observed fruiting on sunken cankers. All 512 survey trees with symptoms were sampled by removing several current-season shoots bearing characteristic leaf lesions. Diseased shoots and leaves were maintained at 4°C for 1–4 weeks before being assessed under dissecting and compound microscopes to confirm the presence of M. betulae acervuli and conidia. Single-conidial isolates of M. betulae were obtained from at least one tree at each site by spreading conidia on 2% malt agar. The cultures were kept at room temperature overnight. Germinated single conidia were then transferred onto fresh culture plates containing 2% malt agar.

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Figure 2. (a) Stromatal canker of Anisogramma virgultorum on a young, living shoot of Betula pubescens and (b) old cankers of A. virgultorum leading to malformations of a dead branch of B. pendula.

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The severity of A. virgultorum infection was assessed by two surveyors, visually estimating the percentage area covered in lesions and old cankers characteristic of this fungus on three main branch systems located immediately above and immediately below 1·3 m on the main stem. On trees smaller than 1·5 m, three branches immediately above and immediately below the 50-cm mark on the main stem were assessed. In cases where trees exhibited severe dieback and branch loss, the three living branches closest to the 1·3-m/50-cm mark were assessed. The severity of sunken cankers (non-A. virgultorum) was also assessed using this method.

Statistical analysis

A total of 292 B. pendula (32% of all survey trees) and 608 B. pubescens (68% of survey trees) were assessed in this study (n = 900). The percentage incidence (i.e. frequency of occurrence) of A. virgultorum and M. betulae, and the percentage of trees having 40% or greater crown dieback, were summarized for each WGS site. Statistical analyses were performed using sas version 9·1 (SAS Institute Inc., 2000), treating plot within a WGS site as an experimental unit. An analysis of variance (anova) using a generalized linear mixed model (proc glimmix) was performed to assess the effects of birch species and site on percentage crown dieback, excluding data for sites 2 and 4 at which only B. pubescens was present. Differences between species within a site were determined using the lsmeans statement. proc glimmix was used to test the pair-wise relationships between (i) incidence of A. virgultorum or M. betulae and birch species, (ii) incidence of sunken cankers and birch species, and (iii) incidence of A. virgultorum or M. betulae and incidence of sunken cankers (excluding data for trees infected with both fungi). proc glimmix was then conducted to (i) test the effects of birch species on severity of infection with either A. virgultorum or sunken cankers, (ii) analyse the combined effects of birch species and incidence of either A. virgultorum or M. betulae on crown dieback, (iii) analyse the effects of incidence of A. virgultorum and site on crown dieback, and (iv) test the overall effects of severity of either A. virgultorum infection or severity of sunken cankers on severity of crown dieback. Fisher's exact chi-squared test for independence (proc freq) was conducted to test the pair-wise relationship between absence or presence of A. virgultorum and absence or presence of M. betulae. Overall mean percentage crown dieback and standard errors were calculated using proc glimmix for B. pendula and B. pubescens which were either (i) non-infected, (ii) infected with either A. virgultorum or M. betulae, or (iii) infected with both fungi.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Incidence and severity of crown dieback

Overall, 97% of surveyed birch trees (n = 900) had between 5 and 95% crown dieback. To simplify the reporting of crown dieback data, trees with 40% or greater crown dieback were considered to have ‘severe’ dieback. At six of the nine WGS sites, at least half of all birches surveyed had severe crown dieback, with an overall mean of 48% of trees affected by this level of dieback (Table 2). In 49% of these severely affected trees, dieback was recorded on several larger branches of the crown, while in the remaining trees dieback had also affected the main stem. In 36% of trees with severe crown dieback, the lower and middle sections of the crown were affected, while in 63% of these trees the whole crown was affected (data not shown). Overall, 61% of B. pendula and 41% of B. pubescens exhibited severe crown dieback. At the seven sites where both birch species were present, crown dieback was significantly influenced by an interaction between site and birch species (F6,20 = 7·02; P = 0·0004). Mean percentage crown dieback was significantly higher in B. pendula than B. pubescens at sites 3, 5, 6 and 8, but not at site 9, where B. pubescens was significantly more affected. There was no significant difference in mean percentage crown dieback between the two birch species at sites 1 and 7 (Fig. 3).

Table 2.  Percentage of trees with 40% or greater crown dieback and percentage of trees infected by Anisogramma virgultorum and Marssonina betulae (n = 100 for each variable) at nine woodland Grant Scheme sites in Scotland
SiteIncidence (%)
≥ 40% diebackA. virgultorumM. betulae
1255615
25396 8
36243 8
42782 5
5641946
6503247
7585060
8336035
9577228
Overall mean485728
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Figure 3. Mean percentage crown dieback of Betula pendula and B. pubescens at seven Woodland Grant Scheme (WGS) sites in Scotland. Data for sites 2 and 4 were not included, since only B. pubescens had been planted at those two sites. Bars represent one standard error of the mean.

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Incidence of A. virgultorum and M. betulae

Anisogramma virgultorum is easily recognized in the field by characteristic dark brown to black stromatal cankers on young shoots (Fig. 2a). Infections on older shoots are also easily visible as long deep fissures, which remain once the stromatal tissues have dried up and fallen out (Fig. 2b). At most sites, A. virgultorum stromata occurred on shoots that were 2–3 years old, with infections on 2004 shoots recorded only at four of the nine sites. The presence of M. betulae was confirmed by microscopic analysis of diseased leaves and shoots, and all single-conidial isolations grew into sporulating colonies which were morphologically typical of M. betulae (Sutton, 1980), i.e. slow-growing, greyish-brown colonies, with acervuli and spores produced relatively quickly.

Anisogramma virgultorum and M. betulae were present on birch trees at all nine WGS sites. Overall, 57% of the 900 trees surveyed had A. virgultorum and 28% had M. betulae foliar disease, with the incidence of both pathogens among sites varying from 19 to 96% for A. virgultorum and from 5 to 60% for M. betulae (Table 2). proc glimmix revealed that the incidence of A. virgultorum was significantly greater (F1,26 = 6·36; P < 0·02) on B. pubescens (65% of trees infected) than on B. pendula (41% infected), whereas M. betulae foliar disease occurred more frequently (F1,26 = 14·91; P = 0·0007) on B. pendula (39% of trees infected) than on B. pubescens (9% infected).

Incidence of sunken cankers

Overall, 41% of the 900 birch trees surveyed had sunken cankers (non-A. virgultorum). These were visible as darkened, sunken areas of dead tissue on young shoots, older branches and main stems, and were often centred around the base of a dead side shoot (Green & MacAskill, 2007). proc glimmix showed that the incidence of sunken cankers was significantly greater (F1,26 = 20·58; P < 0·0001) on B. pendula (63% affected) than on B. pubescens (23% affected). Presence of sunken cankers on trees with M. betulae foliar disease alone (83%) was also highly significant (F1,60 = 41·87; P < 0·0001). In comparison, only 59% of trees infected with A. virgultorum alone had sunken cankers (F1,60 = 1·81; P = 0·1835).

Effect of A. virgultorum on crown dieback

Overall, the severity of A. virgultorum infection was significantly influenced by birch species (F1,26 = 16·35; P < 0·0005). The mean percentage of infected shoot tissue on B. pubescens was 7 ± 2·1% (estimated mean ± one standard error) compared with 2 ± 0·7% (estimated mean ± one standard error) on B. pendula. Over all sites and both birch species there was a significant positive relationship between severity of A. virgultorum infection and severity of crown dieback (F109,746 = 1·47; P < 0·003). A significant interaction effect between absence or presence of A. virgultorum and birch species on severity of crown dieback was evident (F1,78 = 9·12; P < 0·004). Overall mean percentage crown dieback in infected B. pubescens was 42% compared to 20% in non-infected B. pubescens. Mean percentage crown dieback did not differ between infected and non-infected B. pendula trees (49% and 48%, respectively). When data were combined for both birch species, crown dieback was significantly influenced by the interaction between WGS site and absence or presence of A. virgultorum (F8,846 = 3·05, P < 0·003). Anisogramma virgultorum infection resulted in a higher percentage of crown dieback at sites 1, 8 and 9, while there was no difference in crown dieback between infected and non-infected trees at all other sites (Fig. 4).

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Figure 4. Mean percentage crown dieback of birch with Anisogramma virgultorum (Av) present or absent at nine Woodland Grant Scheme (WGS) sites in Scotland. Bars represent one standard error of the mean.

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Effect of sunken cankers and M. betulae on crown dieback

There was a significant positive relationship between the severity of sunken cankers and severity of crown dieback (F1,850 = 76·73; P < 0·0001) and this was true for both birch species and across all sites, as there were no significant interactions among the main effects. However, birch species had an effect on the severity of sunken cankers, as B. pendula had a significantly greater (F1,26 = 14·15; P = 0·0009) percentage of shoot tissue affected by sunken cankers (1·8%) than B. pubescens (0·6%).

There was no significant interaction effect between site and absence or presence of M. betulae foliar disease on the severity of crown dieback (F8,28 = 0·42; P = 0·8961). Over all sites, the effect of absence or presence of M. betulae foliar disease (F1,66 = 31·99; P < 0·0001) and birch species (F1,66 = 5·57; P = 0·0212) on severity of crown dieback was significant. Overall, trees infected with M. betulae foliar disease had 58% crown dieback, while non-infected trees had 34% crown dieback. Crown dieback was greater in B. pendula (52%) than B. pubescens (40%).

The combined effects of A. virgultorum and M. betulae on crown dieback

Only 150 of the 900 surveyed birch trees were infected with both fungi. A Fisher's exact chi-squared test on the overall incidence of these two pathogens for all plots within a WGS site conducted showed no significant interaction between these two fungi. Betula pendula and B. pubescens infected with both pathogens had mean crown dieback values of 59 ± 7% (estimated mean ± one standard error) and 56 ± 6%, respectively. This was significantly greater than for B. pendula and B. pubescens infected with A. virgultorum alone (41 ± 6% and 40 ± 5% crown dieback, respectively). Betula pubescens and B. pendula infected with M. betulae alone had mean percentage crown dieback of 42% (± 10%) and 64% (± 6%), respectively. These values did not differ significantly from the mean percentage crown dieback for B. pendula and B. pubescens infected with both fungi.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

This study is the first to show the high degree of crown dieback and the abundance of the two fungal pathogens A. virgultorum and M. betulae on birch at planted sites across Scotland. This study also indicates that both pathogens contribute to dieback, probably in conjunction with other factors.

At six of the nine sites at least 50% of all survey trees were severely affected by crown dieback. This quantifies the extent of the problem at these planted sites in Scotland where birch is evidently in poor health. Although other factors may contribute to the dieback of birch, the aim of this study was to focus on the role of two birch pathogens suspected of causing crown dieback. Anisogramma virgultorum has been described as a minor pathogen of birch as its occurrence was considered to be rare (Dennis, 1968; Froidevaux & Müller, 1972; Ellis & Ellis, 1985). However, in this survey, the first to assess its incidence in planted birch in Scotland, A. virgultorum was found to be abundant at most sites, infecting at least 50% of all surveyed trees at six of the nine sites. Witzell & Karlsson (2002) surveyed B. pendula and B. pubescens saplings in stands in northern Sweden and also found that the fungus was abundant, being present on 55% of the birch saplings.

This survey found that over all sites severity of crown dieback increased with increasing severity of A. virgultorum infection, which supports evidence from previous artificial- and natural-inoculation studies which showed that birch shoots infected with A. virgultorum often die back (Green, unpublished). Similarly, Vleugel (1917) reported that A. virgultorum caused the death of young birch trees in a nursery in Sweden. Almost all the trees with A. virgultorum in this study had older infections (pre-2004), with fresh stromata on the current season's (2004) shoot growth observed only infrequently at four sites. These observations suggest that a peak in A. virgultorum infection levels, possibly as a result of climatic factors, had occurred several years previously. Infection of young birch shoots by A. virgultorum can occur in successive years in Scotland, causing repeated damage to the shoot systems. It is, however, not clear whether new stromatal cankers on already infected trees develop as a result of a systemic infection which allows the fungus to spread within a tree, or by means of new infection loci caused by ascospores.

Marssonina betulae was previously thought to be primarily a leaf spot pathogen of only minor importance on birch (Peace, 1962). However, a recent study showed that M. betulae causes discrete, sunken cankers on young and old shoots and main stems which continue to expand over several years, causing dieback (Green & MacAskill, 2007). In the present study, birch trees which were infected with M. betulae foliar disease had a greater degree of crown dieback than non-infected trees, and the incidence of M. betulae foliar disease correlated highly with the incidence of sunken cankers on young shoots and older branches. There was a significant relationship between the severity of sunken cankers and the severity of crown dieback, even though the mean overall percentage of infected shoot tissue in affected trees was low (1·8% for B. pendula). It is thought that young, current-season shoots which are infected by M. betulae die back, forming a conduit for the fungus to grow into the older branches and stems over subsequent years (Green & MacAskill, 2007). Although M. betulae fruits readily on lesions on leaves and young shoots, it has not been observed fruiting on older sunken cankers in the field. Several shoot and stem sections were collected, but isolation of M. betulae from sunken cankers found on birch during this field survey was unsuccessful. Previous studies found that it is very difficult to culture this fungus from older cankers, since it is very slow growing and is easily overgrown on agar by faster-growing fungi (Green & MacAskill, 2007).

Both diseases evaluated in this survey were associated with similar patterns of dieback in affected trees. Green (2005) observed that crown dieback of birch begins in the lower part of the crown, then gradually moves upwards as dieback becomes more severe. This was confirmed in the current study, in which it was also noted that in trees with low percentages of dieback (less than 20%) it was mainly thin branches which were affected, with dieback gradually spreading into scaffolding branches and affecting the whole crown.

At the time of this study, only 20% of all trees surveyed were infected with both A. virgultorum and M. betulae, with the diseases generally occurring independently of each other. Incidence and severity of A. virgultorum were greater on B. pubescens, whereas M. betulae foliar disease occurred more frequently on B. pendula. The incidence and severity of sunken cankers associated with M. betulae (Green & MacAskill, 2007) were also greater on B. pendula than on B. pubescens. Since only one third of the birches surveyed were B. pendula, this partly explains the lower overall frequency of M. betulae (28%) compared with A. virgultorum (57%). The incidence of each disease varied across sites, reflecting the predominance of each birch species; for example, the highest incidence of M. betulae (60%) occurred at site 7, which comprised 90%B. pendula, whereas the highest incidences of A. virgultorum occurred at sites 2 and 4, which consisted solely of B. pubescens. However, there were anomalies in this trend. For example, site 7 also had a high incidence (58%) of A. virgultorum and site 6, which had only 11%B. pendula, had 47% incidence of M. betulae. Attempts to induce disease on B. pubescens by artificially inoculating seedlings with conidia or mycelium of M. betulae have consistently failed (Green, 2004; Green & MacAskill, 2007). However, this survey found that M. betulae can infect B. pubescens in the field to cause foliar lesions and associated sunken cankers. This indicates that B. pubescens does have a degree of susceptibility to M. betulae, although apparently less so than B. pendula. Provenances of birch may vary in susceptibility to these diseases and this may be responsible for some of the site-by-site variation in disease incidence, as well as the disparity in disease responses of inoculated B. pubescens and trees naturally infected with M. betulae in the field survey. However, the influence of provenance was difficult to assess in this survey since planting stock origin could not be determined accurately for most sites.

The majority of birch trees surveyed had been planted. At site 6, a plot consisting of naturally regenerated local B. pubescens was disease-free, despite the prevalence of both fungi at this site. It cannot be assumed, however, that all naturally regenerated stock is more resistant to infection: at site 1, many naturally regenerated B. pubescens trees were heavily diseased with A. virgultorum. One form of planted birch, present at a number of sites, appeared to be healthy despite having the same growth conditions as adjacent, heavily diseased birch trees. These scattered individual trees (both B. pendula and B. pubescens) were phenotypically distinct with a particularly dense, bushy growth form, small, round leaves and glabrous shoots.

Generally, crown dieback was greater in B. pendula than B. pubescens. Eight of the nine sites surveyed were exposed sites with moderately wet acidic soils, and seven of these sites lay above 250 m a.s.l. These conditions are considered to be suitable for B. pubescens (Low, 1986; White, 1995). Birch trees planted on poor quality, exposed sites such as these might generally be regarded as having increased susceptibility to fungal infection. However, this survey indicated that the poorest site conditions do not necessarily result in the highest levels of disease. For example, the greatest incidence of A. virgultorum was at site 2, the only sheltered, brown-earth site in the survey. It is possible that variations in the frequency of these diseases across sites could be partially explained by varying degrees of exposure to natural inoculum from surrounding areas, together with local climatic variables, these being two important factors influencing the establishment and spread of disease on a site. Factors other than disease also appeared to be causing crown dieback on a number of trees at these sites, since mean percentage crown dieback in non-infected B. pubescens and B. pendula was 18% and 37%, respectively. Some affected trees showed desiccation of scattered shoots, or entire branch systems, which was not associated with any visible disease symptoms. Such damage could be the result of climatic factors (Strouts & Winter, 1994; Braathe, 1995), such as late spring or early autumn frosts, or the formation of winter xylem embolism in shoots caused by freeze-thaw cycles, which may cause dieback in birch (Strati et al., 2003). The use of continental or southern UK provenances of birch in Scotland might also render the trees more susceptible to climate-induced dieback (Worrell, 1998). An interesting area for further study would be the interactions between abiotic stresses caused by climate, birch provenance and susceptibility to fungal disease. Such information could lead to the identification of less disease-susceptible stock for use in future planting schemes in Scotland.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Heike De Silva is supported by a postgraduate grant from the Scottish Forestry Trust, Edinburgh. We thank Andrew Peace for assistance with the statistical analysis and Dr Mike Perks for helpful comments on the manuscript.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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