Susceptibility of Abies pinsapo and its tree cohort species to Heterobasidion abietinum

Abies pinsapo, a rare fir found in the southernmost mountain region of Spain, is severely affected by Heterobasidion abietinum. It was hypothesized that spread of the disease might be favoured by woody species growing in the same habitat. In order to evaluate this hypothesis, artificial inoculation tests were performed on other potential hosts forming the tree cohort species with A. pinsapo. Inoculation test on seedlings demonstrated that H. abietinum was able to colonize stems of Pinus halepensis, P. pinaster and Quercus ilex subsp. rotundifolia, but failed on Q. faginea. Both Pinus species were colonized to a similar extent as the natural host, but Q. ilex subsp. rotundifolia showed a significantly lower susceptibility than conifers. These results suggest that Pinus spp. growing in mixed stands with A. pinsapo might favour spread of H. abietinum. As a consequence, natural replacement of pure A. pinsapo stands by mixed forest Abies‐Quercus should be facilitated.     

Heterobasidion on Abies nordmanniana in north‐eastern Turkey

Occurrence of Heterobasidion annosum s.l. was investigated in 15 coniferous stands in the Giresun and Pontic Mountains in north‐eastern Turkey. Basidiocarps of the fungus were found in 11 stands. Fifty‐two basidiocarp specimens of Heterobasidion were collected from stumps of Abies nordmanniana ssp. nordmanniana and two from stumps of Picea orientalis. Pure cultures were isolated from the basidiocarps and identified with the aid of mating tests. Forty‐five (90%) of the specimens collected from A. nordmanniana were identified as H. abietinum and five (10%) as H. annosum s.s. The former species was also found twice on P. orientalis. This is the first report of H. annosum s.s. for Turkey and the first report of H. abietinum on P. orientalis. Heterobasidion abietinum seems to be mostly a saprotroph on A. nordmanniana.     

Heterobasidion abietinum on Abies species in western Turkey

Forty‐five basidiocarp specimens of Heterobasidion were collected from native Abies species in three locations in western Turkey: A. nordmanniana ssp. bornmülleriana in Bolu province, A. nordmanniana ssp. equi‐trojani in Balikesir province and A. cilicica in Antalya province. Pure cultures were isolated from the basidiocarps and identified to the species level with the aid of mating tests. All the specimens proved to belong to the species Heterobasidion abietinum. This root rot fungus is common in the forests investigated and appears to be relatively virulent on Abies in Turkey. This is the first report of H. abietinum outside Europe.     

The distribution of closely related large genets of Heterobasidion parviporum in a Todo fir (Abies sachalinensis) stand in Hokkaido,Japan

The distribution of genets of a root and butt rot pathogen Heterobasidion parviporum was studied in a 68‐year‐old Abies sachalinensis plantation in Japan. A total of 33 pure cultures of H. parviporum were isolated from diseased Todo fir stumps after clear‐felling. Individual genets of the fungus were identified by three different methods: somatic incompatibility test, random amplified polymorphic DNA, and DNA microsatellite analyses. The combined results of the three analyses identified at least eight genets within a 60 × 100 m plot. One genet, consisting of only one isolate, was genetically differentiated from the other genets by all three methods; the other 32 isolates, however, were grouped with minor discrepancies, into seven genetically close genets. The genetic differentiation was lower than that recorded previously in Europe. A single genet infected 1–15 trees in the plot. The longest distance of the two most isolated trees of a single genet was 51 m. The close genetic relationship between genets and their large sizes suggest that basidiospores from restricted sources (just a few fruiting bodies) infected the site before establishment of the present Todo fir stand and that the disease has spread mainly by vegetative growth of the mycelia through root contact. Absence of fruiting bodies of the fungus in the study plot also suggests the greater importance of vegetative growth than spore dispersal for the spread of this fungus.     

Spatial distribution and persistence of Heterobasidion parviporum genets on a Norway spruce site

Spatial distribution of Heterobasidion genets over a period of ca 50 years in two successive generations of Norway spruce (Picea abies) was unravelled. The genets were first identified in 1993 in a naturally regenerated 43‐year‐old spruce stand that had been thinned the previous winter. Heterobasidion parviporum was found in 17.5% of the old stumps of the previous spruce generation. Nine genets were identified on the study plot; seven of them were present in old stumps of the previous tree generation and two only in the new spruce generation. Eighteen spruce trees of the new generation were infected, 15 of them by vegetative growth of genets originating from the old stumps. The study plot was investigated again in 2005. No new genets had been established after thinning, and three old genets had died out. The remaining genets had infected five new trees, most likely from the thinning stumps of diseased trees. At the age of 56 years, 16.1% of the residual spruces were infected by Heterobasidion. The results of this study suggest that if spore infection to stumps of spruce can be prevented, the decay frequency caused by H. parviporum will not necessarily increase in successive generations.     

Genetic variation of Heterobasidion abietinum in Southern Europe and the Mediterranean Basin

Heterobasidion abietinum causes root and butt rot on Abies species occurring in central Europe and the Mediterranean Basin in a distribution extending from Spain in the west to Turkey and Caucasia in the east. To investigate the genetic diversity within H. abietinum, 95 isolates from different regions were analysed with 61 polymorphic molecular markers. The markers showed genetic differentiation amongst the H. abietinum populations. The most diversified population is that on A. pinsapo in southern Spain, which is isolated from gene flow with other populations. Lower but still significant differences were found amongst other European populations. Isolates from Turkey showed little diversification compared with the south European isolates from east of the Alps. The genetic structure of the H. abietinum populations in relation to postglacial recolonization of Abies is discussed.     

Epidemiology of Heterobasidion abietinum and Viscum album on silver fir (Abies alba) stands of the Pyrenees

In the last two decades, stand decline and increased mortality has affected silver fir (Abies alba) forests in the Spanish Pyrenees. Simultaneously severe occurrences of the root rot fungus Heterobasidion annosum s.l. and of the mistletoe Viscum album have been reported. We aimed to improve the understanding of the epidemiology of both pathogens in our region. All H. annosum isolates found on silver fir were typed as H. abietinum. H. abietinum was more frequently observed where cuttings had targeted fir trees rather than other species. H. abietinum fruiting bodies were observed in the most recently cut stumps. V. album was more abundant on more dominant fir trees, and in southern aspect stands. The number of V. album colonies in the stand correlated (R² = 0.40) with silver fir mortality. Stands with a high level of V. album infection tended to have a smaller percentage of basal area in species other than silver fir, and they tended to be located on more south‐facing slopes. H. abietinum was widespread in silver fir forests of the Pyrenees. Our data suggest that, in the Pyrenees, the observed H. abietinum incidence may represent a combination of both primary and secondary spread of the pathogen. Favouring mixed forests should be tested as a potential control method for V. album. The correlation between silver fir mortality and V. album infection warrants further study, as the observed tree mortality could have occurred due to other factors than V. album, such as drought damage.     

New records of Heterobasidion parviporum in China

Twenty‐one basidiocarp specimens of Heterobasidion annosum s.l. were collected in six forest areas in western and central China, from host trees Picea schrenkiana, Abies fabri, Abies fargesii and Larix griffithii. Single‐spore cultures were isolated from the basidiocarps and identified by mating tests. All the specimens proved to belong to the species Heterobasidion parviporum. The results show that this fungus has a wide distribution in China. It seems to be a less aggressive pathogen in China than in Europe, although reliable data on the occurrence of Heterobasidion root rot in coniferous forests of China are so far lacking.     

Can habitat prediction models contribute to the restoration and conservation of the threatened tree Abies pinsapo Boiss. in Southern Spain?

We examined the association between habitat variables and the relative impacts of topographic microclimates as a valuable tool for restoration and conservation of Abies pinsapo in southern Spain. We used presence–absence data from A. pinsapo and 79 environmental variables and biomod species distribution models to describe the current and future species habitat across the Sierra de las Nieves Natural Park (southern Spain). A. pinsapo habitat was most strongly associated with microtopographic (solar incidence) and temperature variables, indicating climate-driven changes in microhabitat use. Most of the temperature variation among the study site was attributable to topographic microclimates rather than regional temperature differences, such that differences in microhabitat associations occurred principally between north- and south-facing slopes within the same region. The current potential distribution suggests that around 8.7% (56.44 km²) of the study area is highly suitable for A. pinsapo, with 9.7% (62.84 km²) being moderately suitable. Under different global circulation models and climate change scenarios, the net decrease in suitable habitat is predicted to be 93% of the current distribution by 2040, disappearing altogether by 2099. Our findings also show a sharp reduction of potential restoration areas (1.8% of the current areas). Microclimatic variation generated by the topography offers the microclimate-driven locations of habitat suitability which could shape species’ distribution restoration actions and their responses to environmental change. The approach presented here can provide a rapid assessment of the future conservation status of other important forest tree species in Spain, improving our understanding of the vulnerability of endangered species under climate change, and can be an effective tool for biodiversity conservation, restoration, and management.

     

Two studies to assess the risk to Pinus sylvestris from Heterobasidion spp. in southern Sweden

Abstract

Pine stumps are not being treated against Heterobasidion spp. in Sweden. To determine whether they should be, the frequency of stump infections and the species of Heterobasidion involved were investigated in nine newly thinned pure Scots pine (Pinus sylvestris L.) stands in southern Sweden. The incidence of Heterobasidion was measured in roots of standing Scots pine in another 15 stands. Infections by both H. annosum (Fr.) Bref. s.s. and H. parviporum Niemelä & Korhonen were numerous in stumps six months after a summer thinning. The pathogen, mostly H. annosum, was found in 44 of 60 sampled root systems, from 14 of the 15 stands. Twenty of the infected pines were assessed as healthy on the basis of crown symptoms while 24 trees had defoliated crowns. Infected root systems were most frequent among trees with thin crowns in stands on former agricultural land, where previous thinnings had been carried out during the growing season when airborne spores are plentiful. The study suggests that stump treatment may be a profitable way to reduce disease development in Scots pine monocultures on sandy soils as well as in mixtures with Norway spruce [Picea abies (L.) Karst.] on any soil.     

Changes to relative stand composition after almost 50 years of Heterobasidion root disease in California true fir and pine forests

The Agaricomycete Heterobasidion annosum sensu lato (s.l.), a species complex of fungal pathogens, causes root and butt rot on conifers throughout the northern hemisphere, thereby shaping structure, composition, and evolution of vast and diverse forest ecosystems. We analyze forest change 48–49 years following Heterobasidion root disease emergence in 63 permanent plots first established in 1970–1972 and measured at least once every decade through 2020. We use this dataset to infer the long-term consequences of Heterobasidion root disease in a set of common forest types that reflect some of the most important hosts for this set of diseases in western North America. We contrasted three host–pathogen systems located within the Sierra Nevada, southern Cascades Mountain Range and the Modoc Plateau: (1) H. irregulare in host communities dominated by several Pinus (pine) species and Calocedrus decurrens (incense cedar) in Yosemite Valley, on the Sierra Nevada Range western slope; (2) H. irregulare in a largely single species (Pinus jeffreyi) host disease system on the eastern slopes of the Sierra Nevada and southern Cascades as well as the Modoc Plateau; and (3) H. occidentale—also on the western slope of the Sierra Nevada—in stands with a mixture of susceptible Abies (true fir) and a diversity of non-hosts for this Heterobasidion species. Approximately 50 years after disease emergence, relative basal area and stem density were significantly reduced within disease centres in all three pathosystems, but changes to forest composition and relative species dominance were determined by pre-disease host and non-host diversity. In the western-slope H. occidentale system, the disease increased the dominance of non-susceptible species, Pinus species and C. decurrens. In the multi-genus Yosemite pathosystem, H. irregulare did not significantly shift species dominance, and as expected, species shifts did not occur in the largely single-genus eastern-slope forests. In these widespread California forest ecosystems, two factors appeared to determine forest conditions almost 50 years after Heterobasidion root disease monitoring: the size of the disease centre and the initial diversity of non-hosts. Along with pathogen species, these factors appear to affect the local severity of disease as well as the degree of species shifts relative to initial plot compositions, reaffirming host susceptibility classifications associated with these forest types.     

Differences in virulence of genets of Heterobasidion annosum and susceptibility of young plants of different conifer species and origins

Heterobasidion species are the most important pathogens causing root and stem rot on conifers in northern hemisphere forests. The host list of this complex is very wide and includes over 200 species of trees and shrubs. Among the members of this complex, Heterobasidion annosum s. s. has the largest host range. In this study, young plants of Pinus sylvestris, Picea orientalis, Abies nordmanniana, Cedrus libani and Pinus brutia (three different origins) were inoculated on the lower stem with known genets of Heterobasidion annosum s.s. collected from Pinus brutia stands in south-western Türkiye. Infection frequency, assessed as presence of the conidial stage in stem discs following incubation, in the inoculated seedlings was 100%. The Heterobasidion annosum s. s. isolates were re-isolated from all inoculated host species. Control seedlings showed no symptoms of disease. Mortality in inoculated plants was 11.5% of the 735 inoculated plants, which died over an 8-weeks incubation period. The isolates showed greater growth on Cedrus libani, Pinus sylvestris and Picea orientalis seedlings compared to other species tested. On the other hand, it was found that the least affected seedlings were Pinus brutia TB12 and Abies nordmanniana. This study proved that differences occur in aggressiveness of Heterobasidion annosum s. s. to host species. A striking point in the results is that, despite being the host species from which the isolates were obtained, Pinus brutia seedlings showed lower sensitivity to Heterobasidion annosum s. s. than the other conifer species tested. Inoculations of three different Pinus brutia provenances suggested there was no significant difference in mean lesion lengths and fungal growth values in Pinus brutia plants, except in Pinus brutia TB14, which was more susceptible to extension growth of the pathogen.     

Effect of planting Scots pine around Norway spruce stumps on the spread of Heterobasidion coll.

Management of a Norway spruce stand planted on a site infected by Heterobasidion coll. is problematic because the fungus spreads vegetatively from the colonized stumps of the previous generation to the new seedlings. Growing of mixed stand with more resistant tree species has been suggested to decrease the economic losses caused by butt rot in Norway spruce trees. The mechanistic simulation model Rotstand describing the spread of Heterobasidion coll. in coniferous stands of southern Finland was used to study the effect of planting Scots pines around colonized clear‐felling stumps of Norway spruce of the previous generation. Planting of Scots pines in clusters around colonized stumps markedly decreased the butt rot of Norway spruce trees at the age of 20 years and at clear felling. If the same number of Scots pines were planted randomly, the effect was weak. When the average diameter of colonized clear‐felling stumps was 30 cm, a Scots pine circle with a radius of 3 m resulted in the highest soil expectation value (SEV) at 2% discounting rate, whereas with 40‐cm stump diameter, a 4‐m radius produced the highest SEV. When the proportion of Heterobasidion parviporum in the old colonized stumps was 50% instead of 95%, planting pines around colonized stumps still clearly decreased the butt rot at the age of 20 years and in final felling.     

Cedrus libani: the most susceptible Turkish conifer species to local Heterobasidion isolates in spring inoculations

Five‐year‐old seedlings of Pinus nigra, Pinus brutia, Abies nordmanniana ssp. bornmülleriana and Cedrus libani, 3‐year‐old seedlings of Pinus sylvestris, and 2‐year‐old seedlings of Juniperus excelsa were inoculated on the lower stem with Turkish Heterobasidion abietinum and Heterobasidion annosum s.s. isolates. In total, 300 seedlings were inoculated in April 2007 with five isolates of each Heterobasidion species and incubated in a glasshouse for 12 weeks. The daily maximum temperature increased gradually from 13°C to 31°C by the end of the incubation period. Infection incidence, mortality, lesion length in the inner bark and fungal growth in the xylem were examined. For H. abietinum, infection incidence ranged from 0% to 36%, and for H. annosum s.s. from 0% to 60%. Mortality was low; only 1% of the inoculated seedlings died. Mean lesion lengths varied between 7.6 and 11.9 mm for H. abietinum and 8.0 and 15.7 for H. annosum s.s. in all species apart from C. libani, in which the corresponding values were 42.2 and 42.6 mm respectively. Similarly, mean fungal growth in sapwood of C. libani was approximately 25 mm for both Heterobasidion species, in contrast to 0–3.2 mm in the other tree species. The H. abietinum isolates were not reisolated from P. nigra, P. sylvestris or J. excelsa. The H. annosum s.s. isolates did not infect Abies seedlings. Only P. brutia and C. libani were susceptible to both pathogens. Control seedlings showed no symptoms. The results indicated that C. libani is highly susceptible to Turkish isolates of Heterobasidion.     

Terpene response of Picea abies and Abies alba to infection with Heterobasidion s.l.

The monoterpene composition of Picea abies and Abies alba resin was analysed in relation to growth by Heterobasidion spp. Fifteen‐year‐old P. abies and A. alba trees were inoculated on branches with three species of Heterobasidion annosum s.l. After 4 months of incubation, each host was colonized to a significantly greater degree by the pathogen specific to that host (H. parviporum on P. abies, H. abietinum on A. alba) than by the other fungi. Analysis of the enantiomeric monoterpene profiles in the spruce and fir showed that the response in terms of the relative proportions of the monoterpene compounds in the resin differed between tree species. Following challenge with Heterobasidion spp., A. alba trees did not show changes in monoterpene composition in addition to those in the wounding response (increase in (−)‐α‐pinene and (−)‐camphene, and decrease in β‐phellandrene). In P.abies, (−)‐α‐pinene, (+)‐α‐pinene and δ‐3‐carene increased following Heterobasidion attack but not after wounding alone.     

Susceptibility of red fir and white fir to fir dwarf mistletoe (Arceuthobium abietinum) in California

Fir dwarf mistletoe (Arceuthobium abietinum, Viscaceae) is a damaging parasite of true firs (Abies spp.) in California. In the Sierra Nevada Mountains, fir dwarf mistletoe consists of two special forms (formae speciales, f. sp.) which are morphologically similar, but exhibit a high degree of host specificity: A. abietinum f. sp. concoloris whose principal host is Sierra white fir (Abies lowiana) and A. abietinum f. sp. magnificae which only parasitizes red fir (Abies magnifica). Although field observations and cross‐inoculation studies have consistently supported the extreme host specialization demonstrated by these special forms of fir dwarf mistletoe, little quantitative data from mixed red fir/white fir stands infested with fir dwarf mistletoe have been available. Therefore, I sampled 20 mixed conifer stands dominated by red and white fir and infested with f. sp. concoloris (8 stands) or f. sp. magnificae (12 stands) from near Mount Shasta to the southern Sierra Nevada Mountains near Sherman Pass. Infection of red and white fir was evaluated using temporary circular plots (0.012 ha) established around large, severely infected trees and with rectangular transects placed within fir dwarf mistletoe‐infested stands. In each plot and transect, live trees >5 cm in diameter at breast height were assigned a dwarf mistletoe rating (6‐class system). A total of 55 plots and 51 transects were established in the 20 stands, and over 1,900 red firs and 1,700 white firs were sampled. Ninety‐nine per cent of the red firs and 98% of the white firs were infected in stands infested with f. sp. magnificae or f. sp. concoloris, respectively. In contrast, no infection of red fir was observed in stands infested with f. sp. concoloris and no infected white firs were observed in stands infested with f. sp. magnificae. These data provide further support that the special forms of fir dwarf mistletoe are extremely host specific in California.     

Effect of Thinning and Phlebiopsis gigantea Stump Treatment on the Growth of Heterobasidion parviporum Inoculated in Picea abies

The spread of Heterobasidion parviporum Niemelä & Korhonen in roots of Norway spruce was studied in three unthinned first rotation stands of Norway spruce [Picea abies (L.) Karst.] on former agricultural land in south-western Sweden. Heterobasidion parviporum was inoculated at stump height into the trunk of 135 standing trees in a randomized block design. One year after inoculation, two-thirds of the trees were thinned out and one-third was left standing. Half of the stumps left by thinning were treated with spores of Phlebiopsis gigantea (Fr.) Jül and half were left untreated. The spread of H. parviporum was examined both 3 and 5 yrs after inoculation. The rate of spread of H. parviporum and the proportion of infected roots were found to be significantly higher in the root systems of the stumps than in those of the standing trees. Treatment with P. gigantea had no significant effect on the development of H. parviporum in the stumps. There was a tendency 5 yrs after inoculation, however, for a lower proportion of H. parviporum-infected roots in the stumps treated with P. gigantea than in the untreated stumps. In conclusion, thinning of infected Norway spruce was found to increase the rate of spread of H. parviporum in the root systems of the infected trees, which could increase the risk of a rapid build-up of infection in the remaining stand.     

Mortality and growth of dwarf mistletoe‐infected red and white fir and the efficacy of thinning for reducing associated losses

In managed forests dominated by true fir (Abies) species, stands are often restocked using understory trees retained during timber harvest, making the effects of dwarf mistletoe (Arceuthobium spp.) infestation on small true fir a concern. This study examined the response of small red (A. magnifica) and white (A. concolor) fir and their dwarf mistletoes (A. abietinum f.sp. magnificae and A. abietinum f.sp. concoloris, respectively) to precommercial thinning treatments in fir‐dominated stands in the Sierra Nevada Mountains of California. Tree diameters and dwarf mistletoe ratings were monitored from 1981 to 2001, and mortality was observed from 1981 to 2006. Red and white fir survival and radial growth decreased significantly with greater mistletoe ratings and increased with larger diameters and live crown ratios. Thinning significantly increased survival and growth of white, but not red fir. Over the course of the study, mistletoe ratings for both fir species did not change significantly in unthinned stands, but increased in thinned stands. However, while statistically significant, increases in mistletoe ratings in thinned stands were gradual and mistletoe ratings did not statistically differ between treatments 20 years post‐thinning. Additionally, thinning did not significantly influence mistletoe spread to uninfected trees, indicating that precommercial thinning in lightly infested red and white fir stands will not likely result in substantial increases in dwarf mistletoe abundance over typical harvesting intervals. Overall, while severe dwarf mistletoe infection ratings reduced tree survival and growth, because ratings remained low, actual losses resulting from mistletoes during this study were minor and will not likely result in substantial economic losses over normal harvesting intervals. This finding indicates that precommercial thinning treatments designed specifically to compensate for mistletoe‐associated losses may not be necessary when managing red and white fir for timber production.     

Occurrence of Heterobasidion basidiocarps on cull pieces of Norway spruce left on cutting areas and in mature spruce stands

Fruiting of Heterobasidion on cull pieces and stumps of Norway spruce was investigated in cutting areas and mature spruce stands located in southern Finland. Cull pieces of variable size and showing butt rot were left on three clear‐cut areas and in one thinned stand. Additionally, a part of the cull pieces was transported to mature forest sites with closed canopy. During the succeeding 3–4 years the cull pieces were investigated annually for sporocarps of Heterobasidion, and the area of actively sporulating pore layer of each sporocarp was measured. Root bases of spruce stumps in the logging areas were excavated and sporocarps found on the stumps also measured. At the onset of the experiment, Heterobasidion spp. were isolated from 76% of the cull pieces showing butt rot; 85% of the isolates were identified as H. parviporum and 15% as H. annosum s.s. During the following 3–4 years sporocarps were found on 20% of the 1938 cull pieces where Heterobasidion butt rot was initially detected visually. Sporocarp formation was promoted by advancement of butt rot, increasing cull piece diameter and end‐to‐end ground contact, but restricted by the colonization of the cull piece by Stereum sanguinolentum. Between‐site differences were significant but could not be explained by differences in tree cover. At the end of the investigation period the average sporulating area of Heterobasidion sporocarp per metre of cull piece was higher than the average sporulating area per stump at three of four logging sites. Hence, leaving cull pieces containing Heterobasidion butt rot at logging areas in southern Finland can considerably increase local production of Heterobasidion spores.