Sphaeropsis sapinea
(Sphaeropsis blight)

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Identity

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Preferred Scientific Name

• Sphaeropsis sapinea (Fr.) Dyko & B. Sutton 1980

Preferred Common Name

• Sphaeropsis blight

Other Scientific Names

• Botryodiplodia pinea (Desm.) Petr. 1922
• Diplodia conigena Desm. 1846
• Diplodia pinastri Grove 1916
• Diplodia pinea (Desm.) J. Kickx F. 1867
• Granulodiplodia sapinea (Fr.) M. Morelet & Lanier 1973
• Macrophoma pinea (Desm.) Petr. & Syd. 1926
• Macrophoma sapinea (Fr.) Petr. 1962
• Phoma pinastri Lév.
• Sphaeria pinea Desm. 1842
• Sphaeropsis ellisii Sacc. 1884
• Sphaeropsis pinastri (Lév.) Sacc. 1884

International Common Names

• English: dieback: pine; Diplodia blight; Diplodia canker; Diplodia shoot blight; Diplodia tip blight; shoot blight: conifers; shoot dieback: conifers; Sphaeropsis canker; Sphaeropsis shoot blight; Sphaeropsis tip blight; tip blight: conifers; twig blight: conifers; whorl canker: pine
• Spanish: marchitez de los brotes del pino
• French: deperissement des pousses du pin

Local Common Names

• Germany: Triebspitzenkrankheit: Kiefer

EPPO code

• DIPDPI (Diplodia pinea)

Summary of Invasiveness

Top of page Detailed studies of invasion are lacking, but disease has developed rapidly and resulted in severe damage where the fungus was presumably introduced with pines into the southern hemisphere. Relatively recent reports of severe damage in areas of the north-central USA may also be indicative of invasion and proliferation there. Distribution on cones, seed, diseased seedlings or colonized tree stems after harvest, on or in asymptomatic tree parts, and by insects, could facilitate expansion of geographic range.

Taxonomic Tree

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• Domain: Eukaryota
•     Kingdom: Fungi
•         Phylum: Ascomycota
•             Subphylum: Pezizomycotina
•                 Class: Lecanoromycetes
•                     Subclass: Lecanoromycetidae
•                         Order: Lecanorales
•                             Family: Acarosporaceae
•                                 Genus: Sphaeropsis
•                                     Species: Sphaeropsis sapinea

Notes on Taxonomy and Nomenclature

Top of page Additional synonymy of the genus and/or species are presented in Petrak (1961), Punithalingam and Waterston (1970) and Sutton (1980). Denman et al. (2000) proposed that Diplodia should be used instead of Sphaeropsis. Phylogenetic studies have placed Sphaeropsis sapinea among Botryosphaeria species and related anamorphic fungi (Diplodia, Sphaeropsis, Lasiodiplodia) having pigmented conidia (Jacobs and Rehner, 1998; Denman et al., 2000; Zhou and Stanosz, 2001). Analyses of molecular markers allow differentiation of distinct groups that were first referred to as A and B morphotypes (Palmer et al., 1987) within S. sapinea sensu lato (Stanosz et al., 1999; Zhou and Stanosz, 2001; Zhou et al., 2001). Burgess et al. (2001) also differentiated a third group (referred to as the C morphotype), and De Wet et al. (2003) subsequently treated the B group as a discrete taxon, naming it Diplodia scrobiculata. It has been similarly demonstrated that the fungus referred to as Diplodia pinea f.sp. cupressi (or Sphaeropsis sapinea f.sp. cupressi) is also quite distinct from S. sapinea (Swart et al., 1993; Stanosz et al., 1998; Zhou and Stanosz, 2001; Zhou et al., 2001).

Description

Top of page Features of S. sapinea have been described and illustrated by Punithalingam and Waterston (1970) and Sutton (1980). Pycnidial conidiomata are dark, solitary or aggregated, immersed to erumpent, ovoid (up to approximately 250 µm diam.), and ostiolate. When produced on autoclaved needles placed on culture media, conidiomata may be superficial. Necks of conidiomata may be elongated when produced on such needles or produced on or in media. Conidiogenous cells are 15-20 µm long. Conidia are ovoid to obovoid, rounded at the apex and may be blunt or truncate at the base, initially hyaline to yellowish becoming dark brown, usually 0-1 (but may be 3 or more) septate, thick-walled and approximately 30-45 x 10-16 µm. Conidia may be smooth or exhibit pits in conidial walls, a character that is highly variable (Swart et al., 1993). Microconidia that are hyaline, cylindrical with rounded ends, aseptate, 2.5-6 x 1-2 µm may also be produced (Wingfield and Knox-Davies, 1980).

Distribution

Top of page S. sapinea (under this name or its numerous synonyms) has been reported from many areas within the natural ranges of its hosts and the regions into which they have been introduced and are cultivated. However, many occurrences probably have not been reported in readily available literature. Other reports do not clearly indicate the location(s) of collection. In addition, identifications are sometimes poorly documented and it is possible that other fungi with similar pigmented conidia have been identified as S. sapinea. In other cases, identification is made only to genus (Sphaeropsis or Diplodia) level. Although the origin of S. sapinea is unknown, it was probably introduced to many regions with the movement of host material. It is probable that the known distribution of the fungus will continue to expand as it is further spread or detected in areas where it is not yet confirmed.

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Risk of Introduction

Top of page S. sapinea is not listed as a quarantine organism by the European and Mediterranean Plant Protection Organization (EPPO).

Hosts/Species Affected

Top of page The host range is compiled from numerous sources reporting anecdotal observations, field surveys, indexes, checklists, as well as those describing experimental studies in detail. Reports may not be supported by careful characterization or isolation of the pathogen, and therefore erroneous information could be included. Sources also often do not provide information about the incidence or severity of disease symptoms on the host(s) mentioned. In addition, because differentiation of Sphaeropsis scrobiculata and the fungus referred to as Diplodia pinea f.sp. cupressi or S. sapinea f.sp. cupressi have been relatively recent, these two fungi have probably been included in some reports of hosts of S. sapinea.

High incidence and severity of disease have been reported on native Pinus banksiana, P. ponderosa and P. resinosa in nurseries, plantations, windbreaks, and some natural stands in the north-eastern, north-central and plains states of the USA and adjacent Canada. When grown as ornamentals, in windbreaks, or for Christmas trees, the exotic species Pinus mugo, P. nigra and P. sylvestris may also be severely damaged in the same regions. In Europe, P. nigra may be severely damaged. Economic damage has occurred in exotic plantings of Pinus radiata and P. patula in the southern hemisphere.

Growth Stages

Top of page Flowering stage, Fruiting stage, Post-harvest, Pre-emergence, Seedling stage, Vegetative growing stage

Symptoms

Top of page A variety of symptoms are exhibited by cones, seed and young seedlings in response to colonization by S. sapinea. Female cones may be killed before full development, becoming dark, shrunken and deformed. Symptoms resulting from in vitro inoculation range from reduced germination to death of seed of several Central American pine species (Rees and Webber, 1988). Radicles of germinants were shortened, thickened and discoloured, and if killed became flaccid and brown. Similarly, Fisher (1941) noted reduced germination and radicle decay for Pinus resinosa and P. ponderosa.

Palmer and Nicholls (1985) noted shoot blight of 1-year-old red pine seedlings evidenced by dead terminal buds and upper needles and symptoms on older seedlings including death of new shoots during shoot expansion and needle elongation. Exudation of resin droplets may be the first symptom of infection on either needles or succulent stems. Needles become discoloured and are often killed without elongating beyond fascicle sheaths. Water-soaked, purplish-brown stem lesions may expand as stems become stunted, curled, hardened, resin-encrusted and necrotic (Chou, 1976). Seedlings in nurseries and recently planted seedlings and saplings may be killed by Sphaeropsis collar rot (Palmer and Nicholls, 1985; Stanosz and Cummings Carlson, 1996), characterized by discoloured, necrotic bark and dark discoloration of wood in the lower stem and root collar. Foliage on the entire seedling or sapling becomes chlorotic, desiccated and brown as the stem is girdled.

Initial symptoms of shoot blight on established trees resemble those on seedlings, but symptoms become more severe as colonization progresses. The fungus proceeds from killed shoot tips or diseased cones into woody stems to cause cankers (Waterman, 1943; Chou, 1976). Exudation of resin may be copious and dead needles are often retained. On younger stems, smooth bark may be depressed and turn brown as it dies. The underlying wood may be stained green to brown to blue to black and be resin-soaked. Older cankers may be bounded by callus. Entire branches or whorls of branches may be killed as the pathogen progressively invades, and substantial dieback or dead tops can result. Subsequent forking or branching of diseased leaders may result in substantial defect (Currie and Toes, 1978).

Severe crown symptoms and tree death may follow hailstorms, drought or pruning. Zwolinski et al. (1990b) estimated loss of as much as half the live foliage, death of 50-80% of leaders, and up to almost 20% tree mortality in Pinus radiata plantations in South Africa in the months after a hail event. Chou (1987) described crown wilt of P. radiata associated with the colonization and killing of inner bark, the extensive invasion and blue staining of wood, and subsequent desiccation. Grey to blue to black staining of wood may occur in freshly cut logs and green lumber (Young, 1937; Kreber et al., 2001) and also in roots colonized by S. sapinea (Wingfield and Knox-Davies, 1980).

List of Symptoms/Signs

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Biology and Ecology

Top of page S. sapinea overwinters as conidia in pycnidia or mycelium in needles, shoots, branches and cones. Debris can be a source of inoculum for long periods (Zhou et al., 1997) and conidia release is common whenever the weather is moist (Brookhouser and Peterson, 1971; Swart et al., 1987a; Palmer et al., 1988) and they are distributed by rain or insects. Germination is rapid and penetration can occur through stomata on elongating needles (Brookhouser and Peterson, 1971) and directly through intact surfaces of succulent, expanding shoot tips (Chou, 1978). Penetration can also occur through wounds, including those produced by pruning branches from large trees (Chou and MacKenzie, 1988). Symptom development on young needles and succulent shoots is rapid, with visible lesions and wilting of affected organs within days to weeks of infection.

Altered host condition strongly influences the incidence and severity of disease. Field observations include long association of outbreaks with drought (Nicholls and Ostry, 1990). Experimental data from studies of potted trees (Bachi and Peterson, 1985; Chou, 1987; Blodgett et al., 1997a) and established plantation trees (Blodgett et al., 1997b) for which water status has been manipulated, support the importance of low host water potential in the induction of susceptibility. Outbreaks have also been associated with altered host nutrition (De Kam et al., 1991; Van Dijk et al., 1992; Stanosz and Trobaugh, 1996). The effects of tree age and seasonal conditioning on host susceptibility have also been observed (Chou, 1977, 1982).

The often sudden development of disease can in part be explained by the discovery that S. sapinea can persist on or in its hosts in the absence of any obvious symptoms. Virulent isolates of the pathogen have been obtained from various organs of naturally infected but asymptomatic pines including Pinus banksiana, P. nigra, P. patula, P. resinosa, P. sylvestris and P. radiata (Smith et al., 1996; Stanosz et al., 1997; Flowers et al., 2001). The fungus has also been re-isolated from wounded and inoculated seedlings of several other conifer species on which symptoms were not produced (Blodgett and Stanosz, 1999). Using naturally infected, potted P. resinosa seedlings, Stanosz et al. (2001) demonstrated that water stress can release S. sapinea from quiescence to result in rapid disease development and seedling mortality, thus proving the potential of S. sapinea to act as a latent pathogen sensu Mussell (1980).

Natural enemies

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Means of Movement and Dispersal

Top of page Natural Dispersal

Conidia of S. sapinea are released under moist conditions and disseminated by rainsplash or wind-driven rain. Thick-walled conidia are very durable and could remain not germinated but viable for long periods on seed, debris, other plants, wood products, etc. Feci et al. (2002) demonstrated that conidia are carried by the cone bug Gastrodes grossipes, which is associated with cones of Pinus nigra in Italy.

Movement in Trade/Transport

In trade, the pathogen could be moved on or in cones, seed, any above- or below-ground organ of colonized seedlings or larger trees or their parts, logs, green lumber, and chips, bark or mulch. The ability of S. sapinea to persist asymptomatically on or in trees and tree parts provides additional potential for movement.

Plant Trade

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Impact

Top of page Whether or not losses have been expressed in economic terms, significant damage has been caused by S. sapinea in a variety of situations. Palmer and Nicholls (1985) reported loss of 35% of 1-year-old red pine seedlings in a Wisconsin nursery (loss of more than 1 million seedlings). In the same state, mortality of newly planted or established red pine saplings during a drought year was as great as 95% in some plantations. Lower stems and root collars frequently yielded S. sapinea, which proliferates to rapidly girdle and kill many trees under these conditions (Stanosz and Cummings Carlson, 1996; Stanosz et al., 2001). Nicholls and Ostry (1990) reported tree mortality in Pinus banksiana and P. resinosa plantations ranging from 2 to 51% in Minnesota and Wisconsin, and indicated that S. sapinea was consistently associated with dead trees. Trees in windbreaks also have been severely damaged in central USA (Peterson and Wysong, 1968).

Losses in the production of Pinus radiata in the southern hemisphere have been reported in more detail. Zwolinski et al. (1990a) quantified the losses resulting from a post-hail outbreak of dieback induced by S. sapinea affecting approximately 2000 ha of mostly P. radiata in the Cape Province of South Africa. The timber loss in compartments prematurely harvested was about 28% of the volume and 55% of the value of potential production. The percentage volume loss increased with plantation age, with the greatest losses recorded on good quality sites. Great losses were also documented for a P. radiata stand affected by S. sapinea in New Zealand (Currie and Toes, 1978). There was a close association between the severity of dieback, tree malformation, and loss in merchantable tree volume. A reduction of 63% in merchantable tree volume was estimated. In contrast, despite a high incidence of top death in some (usually younger) stands of P. radiata in north-eastern Victoria, Australia, the overall effect on tree growth and on volume and value of merchantable wood was small (Wright and Marks, 1970). The volume of degraded wood in this study ranged from 0.5 to 5.5% of the possible volume.

Economic Impact

Top of page Whether or not losses have been expressed in economic terms, significant damage has been caused by S. sapinea in a variety of situations. Palmer and Nicholls (1985) reported loss of 35% of 1-year-old red pine seedlings in a Wisconsin nursery (loss of more than 1 million seedlings). In the same state, mortality of newly planted or established red pine saplings during a drought year was as great as 95% in some plantations. Lower stems and root collars frequently yielded S. sapinea, which proliferates to rapidly girdle and kill many trees under these conditions (Stanosz and Cummings Carlson, 1996; Stanosz et al., 2001). Nicholls and Ostry (1990) reported tree mortality in Pinus banksiana and P. resinosa plantations ranging from 2 to 51% in Minnesota and Wisconsin, and indicated that S. sapinea was consistently associated with dead trees. Trees in windbreaks also have been severely damaged in central USA (Peterson and Wysong, 1968).

Losses in the production of Pinus radiata in the southern hemisphere have been reported in more detail. Zwolinski et al. (1990a) quantified the losses resulting from a post-hail outbreak of dieback induced by S. sapinea affecting approximately 2000 ha of mostly P. radiata in the Cape Province of South Africa. The timber loss in compartments prematurely harvested was about 28% of the volume and 55% of the value of potential production. The percentage volume loss increased with plantation age, with the greatest losses recorded on good quality sites. Great losses were also documented for a P. radiata stand affected by S. sapinea in New Zealand (Currie and Toes, 1978). There was a close association between the severity of dieback, tree malformation, and loss in merchantable tree volume. A reduction of 63% in merchantable tree volume was estimated. In contrast, despite a high incidence of top death in some (usually younger) stands of P. radiata in north-eastern Victoria, Australia, the overall effect on tree growth and on volume and value of merchantable wood was small (Wright and Marks, 1970). The volume of degraded wood in this study ranged from 0.5 to 5.5% of the possible volume.

Environmental Impact

Top of page Information on environmental impacts to natural environments is lacking.

Diagnosis

Top of page Tentative diagnosis of S. sapinea is accomplished by recognition of pycnidia with conidia (Punithalingam and Waterston, 1970; Sutton, 1980). Pycnidia commonly occur on or in colonized needles, shoots, cones and bark of woody stems and roots. It is possible to isolate S. sapinea from colonized tissues and from conidia streaked onto culture media. Isolation has been facilitated by use of an amended malt extract medium (20 g Difco agar, 10 g Difco malt extract, 50 mg rose bengal, 10 mg active ingredient (a.i.) benodanil, 1 mg a.i. chlorothalonil, 1 mg o-phenylphenol and 1 L water) (Swart et al., 1987b). Water agar amended with tannic acid has also been used to efficiently culture S. sapinea from asymptomatic shoots (20 g Difco agar, 5 g tannic acid and 1 L water) (Blodgett et al., 2003). Pycnidia and conidia form in colonies produced on a water agar, malt extract agar, potato dextrose agar and other media, and on autoclaved conifer needles placed on the surface of culture media. Incubation of cultures in the light enhances the production of pycnidia.

The analysis of molecular markers allows confirmation of S. sapinea. Differences in ITS and 5.8S rDNA sequences among S. sapinea and closely related species are small (Zhou and Stanosz, 2001). Comparison of inter simple sequence repeat fingerprints of genomic DNA, however, allows differentiation of S. sapinea from Diplodia scrobiculata (formerly differentiated as the B morphotype or B group of S. sapinea) (De Wet et al., 2003) as well as other species of Botryosphaeria and related anamorphic fungi with pigmented conidia (Zhou et al., 2001). Restriction enzyme analysis of ribosomal DNA sequences also differentiated isolates of S. sapinea from those of D. scrobiculata (Hausner et al., 1999). Identification of isolates as S. sapinea or D. scrobiculata can also be accomplished by polymerase chain reaction amplification of random amplified polymorphic DNA markers specific to each species (Stanosz et al., 1999).

Detection and Inspection

Top of page Although sometimes recognizable as characteristic, symptoms vary and are not unique, and S. sapinea may be present in tree parts also damaged by other fungal pathogens, insects or abiotic agents. Discoloration of wood colonized in living trees or after felling is also not distinctive.

Similarities to Other Species/Conditions

Top of page Identical shoot blight symptoms can be induced on a variety of conifer hosts (Blodgett and Stanosz, 1997; Blodgett and Stanosz, 1999) by the recently described, closely related, and morphologically similar pathogen Diplodia scrobiculata (De Wet et al., 2003) that was formerly differentiated as the B morphotype or B group of S. sapinea (Palmer et al., 1987). In addition, symptoms caused by other fungal pathogens of shoots (e.g., Sirococcus conigenus), by insects (e.g., the pine shoot moth Dioryctria resinosella) and abiotic agents (e.g., frost) can be similar. Sapwood staining caused by S. sapinea is not so distinctive as to easily be differentiated from that caused by other fungi.

Prevention and Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Phytosanitary Measures

Specific information is lacking regarding the effectiveness of measures to disinfest seed, or treat logs or lumber, to prevent movement of S. sapinea.

Cultural Control and Sanitary Methods

The removal and destruction of colonized shoots, branches and cones can prevent further invasion of a diseased tree and reduce the availability of inoculum for further spread. Host species should not be used for windbreaks in nurseries and it may be desirable to remove significantly damaged trees from production areas. Excessive pruning should be avoided and pruning and shearing should be limited to dry weather when inoculum is less available. The association of disease with water stress (Nicholls and Ostry, 1990; Blodgett et al., 1997a, b) and altered nutrition (De Kam et al., 1991; Van Dijk et al., 1992; Stanosz and Trobaugh, 1996) suggests that maintaining favourable moisture status and avoiding excesses in nitrogen may reduce the incidence and/or severity of disease. Less susceptible or non-host species should be considered for sites with a history of unacceptable damage.

Host-Plant Resistance

The incidence and severity of symptoms varies among host species. The most damaged species are found among the two- and three-needled 'hard pines' (subgenus Diploxylon); five-needled 'soft pines' (subgenus Haploxylon) and non-pine hosts are generally less susceptible. Within the former group, non-wounded Pinus resinosa seedlings inoculated with conidia in greenhouse trials exhibited a lower incidence and less severe symptoms than Pinus banksiana seedlings (Blodgett and Stanosz, 1997). Ranked from greatest to least severity of symptoms in response to wounding and inoculation of terminal shoots with S. sapinea were Pinus sylvestris, P. resinosa, Picea pungens, Pinus mugo, Pseudotsuga menziesii and Abies balsamea (Blodgett and Stanosz, 1999). Differences in responses of pine species cultivated in South Africa to inoculation with S. sapinea were quantified by Swart et al. (1988). In a growth chamber experiment, inoculated seedlings of Pinus kesiya, P. pinaster and P. radiata exhibited greater frequencies of dead shoots than those of P. elliottii, P. patula and P. taeda. On trees inoculated in the field, a greater frequency of shoot death and longer cambial lesions occurred for P. radiata than for P. elliottii and P. pinaster.

Variation in host response to S. sapinea has also been observed within species. Burdon et al. (1982) studied responses of inoculated progenies of parents selected for freedom from S. sapinea-associated shoot dieback on a site of very high disease incidence. As a group these progenies showed a lower incidence of disease than control seedlots, and there was also considerable variation among these progenies. Gerhold et al. (1994) noted differences in response to inoculation among varieties of P. sylvestris seedlings. Variation in disease tolerance between provenances and among families of Pinus greggii following natural infection by S. sapinea has also been reported (Smith et al., 2002).

Chemical Control

Fungicide applications have reduced the incidence of shoot blight and may be appropriate for nurseries, Christmas tree plantations, ornamental plantings and windbreaks (Van Der Westhuizen, 1968; Schweitzer and Sinclair, 1976; Peterson, 1977; Palmer et al., 1986; Stanosz and Smith, 1996). Stanosz and Smith (1996) found similar efficacy of thiophanate methyl and chlorothalonil on Pinus resinosa seedlings. However, asymptomatic persistence of virulent strains of S. sapinea can occur on or in hosts in spite of fungicide use (Stanosz et al., 1997). Proliferation of S. sapinea in raw logs and freshly sawn lumber has been suppressed by treatment with methyl bisthiocyanate and 2-n-octyl-4-isothiazolin-3-one (Kreber et al., 2001).

References

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