Seiridium cardinale
(cypress canker)

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Identity

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Preferred Scientific Name

• Seiridium cardinale (W.W. Wagener) B. Sutton & I.A.S. Gibson

Preferred Common Name

• cypress canker

Other Scientific Names

• Coryneum cardinale W.W. Wagener

International Common Names

• English: canker of cypress; cypress blight
• Spanish: cancro de la corteza del ciprés; cancro del ciprés
• French: chancre cortical du cyprès; chancre du cyprès
• Portuguese: cancro cortical dos ciprestes

Local Common Names

• Germany: Zypresse Krebs
• Italy: cancro corticale del cipresso; cancro del cipresso

EPPO code

• SEIRCA (Seiridium cardinale)

Summary of Invasiveness

Top of page The high pathogenicity of S. cardinale, wide host range in the Cupressaceae family, relative stability of its virulence, abundant production of asexual spores, its adaptation to various environments and the possibility of long-distance transport by vectors or trade of infected propagation material, have allowed this fungus to spread widely and to cause pandemics in several continents.

Taxonomic Tree

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• Domain: Eukaryota
•     Kingdom: Fungi
•         Phylum: Ascomycota
•             Subphylum: Pezizomycotina
•                 Class: Sordariomycetes
•                     Subclass: Sordariomycetidae
•                         Order: Xylariales
•                             Family: Amphisphaeriaceae
•                                 Genus: Seiridium
•                                     Species: Seiridium cardinale

Notes on Taxonomy and Nomenclature

Top of page The fungus responsible for a destructive outbreak of canker disease on Cupressus macrocarpa and C. sempervirens in California (USA) was first described by Wagener in 1939 as Coryneum cardinale. It was later reassigned to the anamorph genus Seiridium Sutton and Gibson. So far, the teleomorph (tentatively Ascomycetes: Amphisphaeriaceae) has not been found. No subspecific entity or forma specialis of the fungus has been reported (Wagener, 1939; Sutton and Gibson, 1972; Boesewinkel, 1983; Graniti, 1986).

Description

Top of page The subperidermal acervular conidiomata of C. cardinale appear as minute, black pustular bodies scattered or clustered on infected stems, branches and cones of affected trees, and dehisce by rupture of the upper wall. Often black conidial masses spread from cankers over the bark.

Conidia are formed at the apices of hyaline, holoblastic, annellidic conidiogenous cells and subsequent proliferations. Conidia are oblong-fusiform, smooth, 17-34 (mostly 21-26) x 7-12 (mostly 8-10) µm (length/width ratio: 2.5-3), straight, sometimes slightly curved, 5-distoseptate. The thick-walled four median cells are of the same brown or dark colour, slightly collapsed when conidia are not fully turgid. The two thin-celled end cells are hyaline, the apical cell is campanulate, and the basal one truncate. The apical end cell bears a very short (approximately 1 µm long) hyaline appendage; the basal end cell often bears a similar, central appendage.

A transient production of hyaline, filiform spermatia may occur within the acervuli (Motta, 1979).

For further details, see Wagener, 1939; Sutton and Gibson, 1972; Sutton, 1975; Boesewinkel, 1983; Graniti, 1986, 1998a; Nag Raj, 1994.

Distribution

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After the introduction of cypress canker in France and Italy around the middle of the last century (Barthelet and Vinot, 1944; Grasso, 1951), the wide occurrence of susceptible hosts and climatic conditions favourable to growth and dissemination of the pathogen, facilitated its establishment and spread in the Mediterranean area (Solel et al., 1983; Xenopoulos and Diamandis, 1985; Graniti, 1986, 1998a; Raddi et al., 1987; Luisi, 1990, Panconesi, 1990).

There is an old record for New South Wales, Australia (Hutton, 1949), however this is not supported by any more recent literature.

The list of countries includes records of specimens from the IMI Herbarium retained at CABI Bioscience, UK Centre, Egham; dates of collection are noted (Herb. IMI, various dates).

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.

History of Introduction and Spread

Top of page An outbreak of destructive cypress blight was first reported from northern California, USA, in 1939, but the pathogen (S. cardinale) had probably been introduced into the area more than a decade earlier (Wagener, 1928, 1939, 1948, 1964). The main effect of this epidemic was on the highly susceptible Monterey cypress, Cupressus macrocarpa and, to a lesser extent, on the European C. sempervirens and on some species of American and exotic Cupressaceae. In the same years the disease was reported from New Zealand (Birch, 1933), and subsequently spread into Europe (Barthelet and Vinot, 1944), Asia Minor, South America, Australia, Japan and South Africa. To date, the disease has become established in the boreal latitudes between 30° and 40°N and in some austral areas between 30° and 50°S (CABI/EPPO, 2003)

The origin of S. cardinale in producing the first epidemics remains uncertain. A virulent strain able to infect susceptible cypress trees may have arisen from local populations of weakly pathogenic Seiridium species in the areas where the disease was first recorded (Wagener, 1964). The most likely hypothesis is that the first epidemics originated from accidental introduction of the pathogen into California, USA, or New Zealand on imported nursery stocks of ornamental cypress trees.

Risk of Introduction

Top of page S. cardinale is a highly dangerous pathogen, able to cause serious epidemics to susceptible Cupressaceae in temperate areas of the world. Although the most common vehicle for the worldwide diffusion of cypress canker has been through the international trade in infected nursery stock, S. cardinale has not been included in the EPPO lists of quarantine organisms (EPPO, 1987).

The risk of introduction of the pathogen into hitherto free areas is not limited to accidental transport or trade of infected seeds, seedlings, potted plants and nursery stock, but also includes the trade of infected corticated, and even decorticated, timber.

Habitat

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No natural or experimental host species of S. cardinale is known out of the family Cupressaceae. Canker disease may affect groups of trees in natural forests, woods, stands, plantations, and rows of windbreaks, as well as single ornamental cypress trees in parks, gardens, cemeteries and historical places. Nurseries and propagation plots are also affected.

Habitat List

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Category	Sub-Category	Habitat	Presence	Status
Terrestrial
	Terrestrial – Managed	Cultivated / agricultural land	Present, no further details	Harmful (pest or invasive)
		Protected agriculture (e.g. glasshouse production)	Present, no further details	Harmful (pest or invasive)
		Managed forests, plantations and orchards	Present, no further details	Harmful (pest or invasive)
		Managed grasslands (grazing systems)	Present, no further details	Harmful (pest or invasive)
		Disturbed areas	Present, no further details	Harmful (pest or invasive)
		Rail / roadsides	Present, no further details	Harmful (pest or invasive)
		Urban / peri-urban areas	Present, no further details	Harmful (pest or invasive)
	Terrestrial ‑ Natural / Semi-natural	Natural forests	Present, no further details	Harmful (pest or invasive)
		Natural grasslands	Present, no further details	Harmful (pest or invasive)
		Riverbanks	Present, no further details	Harmful (pest or invasive)
		Wetlands	Present, no further details	Harmful (pest or invasive)
Littoral
		Coastal areas	Present, no further details	Harmful (pest or invasive)

Hosts/Species Affected

Top of page S. cardinale may infect and cause disease to many species, varieties and hybrids of Cupressaceae, both native and cultivated. Susceptibility to S. cardinale canker disease varies among and within the host species.

Inoculation tests on a number of known and potential hosts in various countries and environments indicated that Cupressus macrocarpa is highly susceptible, C. sempervirens, Thuja plicata and Cupressocyparis leylandii are less susceptible; Cupressus arizonica, C. lusitanica, C. forbesii, Chamaecyparis lawsoniana, T. orientalis [Platycladus orientalis] and other species show a range of resistance, whereas Cupressus bakeri, C. torulosa, C. funebris [Chamaecyparis funebris], C. cashmeriana and other Asiatic species of Cupressus were resistant or highly resistant (Smith, 1938; Wagener, 1939, 1948; Wolf, 1939; Wolf and Wagener, 1948; Grasso, 1952; Strouts, 1973; Faddoul, 1973; Raddi and Panconesi, 1977; Ponchet and Andréoli, 1979; Grasso et al., 1979; Grasso and Ponchet, 1980; Andréoli, 1979; Beresford and Mulholland, 1982; Mathon, 1982; van der Werff, 1988; Valdivieso et al., 1988; Panconesi, 1990; Andréoli and Ponchet, 1991; Xenopoulos, 1991a, 1991b; Spanos, 1995; Spanos et al., 1997a; Teissier du Cros, 1999; Ducrey et al., 1999).

Relative susceptibility of potential hosts to the pathogen has been tested in several countries under natural, greenhouse and laboratory conditions. Degree of susceptibility or resistance of the host to a particular strain of S. cardinale, a mixture of strains, or samples representing large populations of the pathogen, is usually assessed by inoculating cypress seedlings in the greenhouse or young trees in the nursery or field. Such tests, however, may take 1-2 years and up to 8 years for reliable results to be obtained, depending on genotype and age of the tree, and on environmental conditions (Panconesi, 1990).

Susceptibility of cypress clones or virulence of S. cardinale strains can be comparatively assessed by the size of the necrotic lesion at cambium level, as measured on decorticated stems of inoculated seedlings (Ponchet and Andréoli, 1984).

Correlations between responses of in vitro or in greenhouse inoculated seedlings, micropropagated shoots, explants or tissue cultures and known levels of field resistance have been reported. Their application in resistance breeding programmes could be advantageous in terms of accuracy and speed, especially if associated with responses to toxin treatment.

Early screening methods to assay cypress species or varieties, clones or progenies for resistance to S. cardinale, or low sensitivity to their toxins, have been set up. For example, either cypress explanta or callus cultures could be used to screen cypress genotypes prior to field evaluation. Direct inoculation of S. cardinale on callus cultures, inhibition of fungal growth by cypress callus in dual cultures, ion leakage or ethylene evolution from explanta treated with S. cardinale toxins may provide information about the susceptibility of clones to the pathogen or sensitivity to its toxic metabolites (Tonon, 1994; Tonon et al., 1995; Spanos and Woodward, 1997). The response of callus or cell cultures to seiridins could be used to screen cypress germplasm in vitro (Sparapano et al., 1986; Sparapano and Evidente, 1995).

Expression of resistance responses to S. cardinale in micropropagated cypress shoots has been evaluated histologically. Accumulation of oxidized phenolics or deposition of suberin and lignin in cell walls of foliar epidermis and hypodermis could be used to detect genotypes resistant to the pathogen (Spanos et al., 1997a).

Host Plants and Other Plants Affected

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Growth Stages

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

Symptoms

Top of page Cankers on stem and branches

Infection by S. cardinale on susceptible host trees induces both local and systemic symptoms.

The first sign of cypress blight by S. cardinale is a browning or a reddening of the live bark of stem or branches, at the point of entry of the pathogen. Discoloration is followed by a slight depression of the infected area, longitudinal cracking or fissuring, and resinous exudation. Subsequently, lenticular or elongated cankers develop on the bark around the infection site, where a necrosis of the infected bark tissue occurs, and these may girdle the branches or the stem of young plants. Outgrowths of bark tissues, histological abnormalities and plant cell necrosis may occur around the diseased areas. On trunk and large branches of adult trees, the enlargement of cankers is a slow process. Consistent flows of resin exuding from cracks formed on the cankered area can be seen on the outside of the cankers, which may extend to infected stems and branches. Usually, sectors of the tree on the side of the cankers decline and die.

Cuttings made through the inner bark, the cambium and the first few rings of sapwood can reveal a brown or reddish discoloration. Intensity of discoloration is variable and may assume a typical red-violet colour (hence, the specific epithet 'cardinale' given to the pathogen).

Foliage chlorosis and dieback of branches and top of trees

On trees of susceptible species, e.g. Cupressus macrocarpa and C. sempervirens, crown symptoms are clearly associated with presence of cankers. A diffuse yellowing or reddening first appears on the foliage of twigs, branches, and apical parts of the affected trees, subsequently turning to brown or reddish-brown as the dieback progresses. The leaves of affected branches become dry with time, and then slowly drop to the ground. Fading, drying and dieback of branches and treetops are the most conspicuous symptoms of the disease. The spread of one, several, or many infections on a single tree can kill the whole tree within a relatively short time, depending on its age, susceptibility and the environment.

On relatively resistant clones of Cupressus sempervirens, on C. arizonica, and even on more resistant species such as C. torulosa and C. lusitanica, infection can develop slowly. With resistant hosts, eventually the cankers can be compartmentalized and sealed off by the plant defence reactions (Ponchet and Andréoli, 1990; Ponchet et al., 1990).

List of Symptoms/Signs

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Biology and Ecology

Top of page Genetics

Although a teleomorph is unknown for S. cardinale, heterokaryosis is a common feature of this mitosporic fungus, and no evidence of vegetative incompatibility was found among strains (Sánchez and Gibbs, 1995); consequently, the occurrence of natural variants of the pathogen cannot be ruled out. However, current data do not support a condition of high variability in S. cardinale. Several works indicated that there is little variation in virulence for this pathogen (Andréoli et al., 1984; Panconesi, 1990; Xenopoulos, 1991b; Spanos, 1995).

The disease caused by S. cardinale on its hosts is markedly influenced by local ecological conditions. Canker disease is more common and severe in non-optimal climatic environments for growth of cypress, e.g. in the northwestern areas of the Mediterranean region (Quezal, 1985) than in the southeastern areas, where C. sempervirens is native (Santini et al., 1997a; Santini and Di Lonardo, 2000).

Physiology

Leaf symptoms on trees affected by S. cardinale may develop on the branches of affected trees regardless of the girdling effect of the cankers, for example on foliage distal from where the fungus can be isolated. In the infected bark, necrosis and disruption of host cells, outgrowths of tissues and other histological abnormalities may occur in advance of hyphal growth (Mutto and Panconesi, 1987; Ponchet and Andréoli, 1989, 1990).

This suggests that some extracellular metabolites produced by the fungus, other than those involved in breaking down the apoplastic structures of the host (cell wall-degrading enzymes such as polygalatturanases, xylanases, cellulases, Magro et al., 1982), such as toxins, play a role in pathogenesis.

Toxin Production

The nature and appearance of symptoms caused by infection of S. cardinale to its hosts, as well as the necrotic processes affecting bark and leaf tissues, suggest that toxins are produced in the cypress bark or wood colonized by the pathogen, and are possibly involved in pathogenesis. These substances may diffuse to adjacent tissues, and eventually translocate to distal parts and leaves via the transpiration stream. Out of 100 isolates of S. cardinale collected in Italy, 97 were toxigenic (Sparapano et al., 1995b).

Several phytotoxic metabolites produced by S. cardinale in culture were isolated and chemically characterized. The major toxins were two D<(sup)a,b> butenolides (seiridin and iso-seiridin), followed by three cyclic sesquiterpenes (seiricardines A, B and C) and two minor seiridins (Sparapano et al., 1986; Graniti and Sparapano, 1990; Ballio et al., 1991; Evidente and Sparapano, 1994; Graniti, 1998a).

At low concentrations (50 mM) seiridins enhance plant cell growth and can replace kinetin in tissue culture media. Assayed at higher concentrations (150 mM), seiridins induce leaf chlorosis and necrosis. A subperidermal injection of 2 ml of a 0.2-0.3 mg/ml solution of seiridin into the stem of susceptible cypress seedlings caused extensive dieback and death of the seedlings within 6-8 months (Sparapano et al., 1995b; Sparapano and Evidente, 1995). These symptoms were reminiscent of those shown by Seiridium-infected seedlings. Seiridins also showed antibacterial activity. The susceptibility of species of Cupressus to S. cardinale correlated with their sensitivity to seiridins. Inoculations with highly toxigenic isolates of S. cardinale killed only 5% of C. arizonica seedlings within 4 months compared to 30% of C. sempervirens and 75% of C. macrocarpa seedlings (Sparapano et al., 1994b).

Although minor metabolites, seiricardines as components of an array of toxins, may contribute to the overall toxicity of the pathogen. Injection of 3 ml of a 0.1 mg/ml solution of seiricardines A and B into the stem of young cypress trees induced hypertrophic reactions of bark tissue, longitudinal lesions on stems, and a reddish discoloration of distant leaves. All seiricardines showed fungistatic activity in vitro (Ballio et al., 1991; Evidente et al., 1993).

Reproductive Biology

Under favourable environmental conditions, production of conidia from acervular conidiomata formed on the surface of cankers on stem and branches, as well as on other parts of the affected tree such as the cones (galbuli), is able to assure the availability of fresh inoculum throughout the year. Moreover, conidia of S. cardinale retain their germinability and pathogenicity for more than 1 year (Wagener, 1939, 1948; Panconesi and Ongaro, 1982; Panconesi and Raddi, 1991b; Panconesi et al., 1993).

Pathogenesis

Penetration of S. cardinale hyphae through natural openings, i.e. stomata of leaves (or shoots) into the substomatal chamber, followed by invasion and deterioration of the mesophyll tissue, and lenticels, has been demonstrated experimentally. Penetration through the cuticle of leaves or young shoots is also possible; however, S. cardinale is unable to penetrate the periderm and lignified structures directly (Intini and Panconesi, 1976; Ponchet and Andréoli, 1989; Spanos et al., 1997a, 1999).

In the field and in the nursery, infection of S. cardinale on its hosts usually occurs through wounds produced by various agents: strong winds, frost, hail, insects, small animals and pruning. On young trees, infections are frequent at the insertion of shoots on the stem or branches, where wounds often occur and conidia carried by rain are laid. Actually, cypress canker has caused serious losses to cypress plantations and windbreaks in some Greek islands where winds are strong and recurrent (Xenopolous, 1991a) or in southern France and central Italy, where late frosts frequently occur (Dugelay, 1957; Moriondo, 1967).

After penetration, the pathogen grows within the bark, where a necrotic lesion develops. Spread of the mycelium is relatively rapid in the cortical parenchyma and less in the secondary phloem. Subsequently, the pathogen extends through the vascular cambium into the medullary rays and outermost layers of sapwood. Eventually, all bark tissues turn brown and die (Moriondo, 1972; Mutto and Panconesi, 1987; Ponchet and Andréoli, 1984, 1989; Madar and Liphschitz, 1989; Spanos et al., 1999). Cell necrosis of the cankered bark progresses steadily, with some seasonal variation, until the branches or stem are girdled. Relatively abundant flows of resin are produced by actively growing cankers, i.e. until they are able to enlarge. Even when fungal inoculum is placed deep into the stem, it can spread to the bark and give rise to cankers (Panconesi et al., 1995). The older bark is more resistant than younger bark to growth of the pathogen (Spanos et al., 1997a). Disorganization of xylem elements and occlusion of pit vessels with consequent reduction of water flow were observed in the xylem from branches of cypress trees inoculated with S. cardinale (Madar et al., 1990).

Host reaction to infection includes a range of cellular responses leading to cell wall incrustation by suberin and lignin, accumulation of oxidized polyphenolic compounds, and resinosis. Lignification, suberization and cell wall thickening have been observed in response to challenge by S. cardinale (Spanos and Woodward, 1997; Spanos et al., 1997a). Healing processes taking place in the surrounding tissues contribute to the formation of cankers. The different consistency of necrotic and reacting tissues and the consequent tension originate cracks and fissures on the bark through which resin can exude.

Resinosis as well as occlusions of the xylem elements most likely play a role in the plant's defence against a toxigenic pathogen that is invading the bark with potential systemic activity (Graniti, 1994; Sparapano et al., 1995b). The composition of foliage resin has been found to be different in healthy and S. cardinale-infected trees (Schiller and Madar, 1991).

Defence processes in infected trees take the form of separation of healthy bark tissue from the diseased one by the formation of a wound periderm through neophellogenic activity. The total thickness of this new periderm (more than 100 mm) was related to clonal resistance to S. cardinale (Ponchet and Andréoli, 1989), whereas in susceptible clones, a thinner periderm may be overcome by the pathogen, leading to the formation of a diffuse canker. In experiments with resistant cypress clones, development of boundary zones including 4-6 layers of cells with ligno-suberized walls within the diseased cypress bark tended to restrict and to isolate the tissues invaded by the pathogen, thus preventing its further spread. In susceptible clones, only 2-4 layers of suberized cells were formed in discontinuous bands around infection sites. These reactions involve a series of processes that can be detected histologically, allowing differentiation of resistant or tolerant species or clones from susceptible ones (Ponchet and Andréoli, 1990; Spanos et al., 1999).

The outer layers of the sapwood adjacent to cankers, as well as the medullar rays, may be colonized by S. cardinale, which can survive for a long period in the woody tissues of cypress without loss of pathogenicity (Faddoul, 1973; Mutto and Panconesi, 1987; Ponchet and Andréoli, 1989, 1990; Madar et al., 1990; Panconesi et al., 1995a).

Environmental Requirements

Conidia of S. cardinale can germinate, and mycelium grow in vitro, from 5-6°C up to a maximum of approximately 35°C, with optimal values around 25°C. Under natural environmental conditions, however, the disease develops with temperatures up to 30°C, although infection is optimal around 25°C (Graniti and Frisullo, 1990). Actually, growth of the pathogen in host tissues is slow or is even arrested during the hottest months of the year (Panconesi, 1990; Ponchet et al., 1990).

Relative humidity close to saturation is required for infection (at 80% RH about half of the conidia of the pathogen are unable to germinate). Rains are effective in spreading the inoculum and favouring penetration of the infecting hyphae through wounds. As a consequence, the incidence and severity of cypress blight may be high or even very high in areas where climatic factors, particularly rain and high relative humidity during the infection season (autumn through spring), favour the production and dissemination of inoculum, and where frost or strong winds produce wounds and lesions on cypress trees. Some cypress plantations close to a devastated area of high incidence may escape the disease for lack of just one predisposing factor, e.g. strong winds or high humidity.

Associations

S. cardinale is often associated with other dematiaceous fungi on cankered tissue of cypress bark, e.g. Pestalotiopsis funerea and P. monochaetioides; these are not primary pathogens however (Sánchez and Gibbs, 1995).

Natural enemies

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Notes on Natural Enemies

Top of page No natural enemies are known for S. cardinale, except competitors (such as species of Pestalotiopsis colonizing bark cankers) or antagonistic fungi (Trichoderma viride).

Means of Movement and Dispersal

Top of page Natural Dispersal

Under moist conditions, conidiomata of S. cardinale open wide on the surface of the cankers, thus exposing black slimy conidial masses. When dry, fragments of this material can be released into the environment by strong winds. Usually, however, conidia extruded from conidiomata are dispersed by rain over short distances, mostly in a downward direction, and then spread laterally by windborne conidia-laden droplets (Panconesi and Ongaro, 1982).

Vector Transmission

Long-distance spread of inoculum, even to isolated areas, is assured by insects and probably birds, which can carry inocula up to the tops of the tree. Insects, especially cork-borers, are highly efficient vectors. Twig-mining beetles such as Phloeosinus aubei, P. thujae and P. armatus are common in the Mediterranean area, and they can spread the disease either by carrying the inoculum from cankered trees into young shoots of healthy trees, or by opening wounds in the cypress bark through which rain-carried conidia enter and initiate infection (Wagener, 1939; Covassi et al., 1975; Mendel et al., 1983; Mendel, 1984; Sumer, 1987; Covassi, 1991; Tiberi and Battisti, 1998). On cones and seeds, the seed bug Orsillus maculatus and the seed chalcid Megastigmus wachtli may contribute to spread the disease (Tiberi and Battisti, 1998; Battisti and Roques, 1999; Roques and Battisti, 1999). Another insect vector of S. cardinale present in California, USA, is the cypress bark moth Cydia cupressana [Enarmonia cupressana] (Frankie and Koelher, 1971; Frankie and Parameter, 1972).

Seedborne Spread

The disease can be transmitted by contaminated or infected seed, both from cankered or healthy-looking trees.

Agricultural Practices

Infections by S. cardinale are favoured by any agricultural practice producing wounds.

Movement in Trade

The worldwide distribution of the disease has probably been favoured by the international trade of infected nursery stock, especially of ornamental species of Cupressaceae.

Seedborne Aspects

Top of page Incidence

Conidiomata of S. cardinale are frequently produced on cypress galbuli (Grasso, 1969). Seeds may also carry conidia on their surface or become infected by the pathogen with final formation of conidiomata (Motta and Saponaro, 1983; Saponaro and Motta, 1981, 1984; Motta, 1986).

Spraying a conidial suspension on recently fertilized ovules of C. sempervirens, C. macrocarpa and Thuja orientalis [Platycladus orientalis] resulted in a high disease incidence on mature seeds, and their germinability was sharply reduced (Motta, 1984).

Effect on Seed Quality

Cones infected by S. cardinale produce fewer filled seeds and more empty seeds than healthy cones. Seed damage by insects, such as the seed bug Orsellus maculatus and the seed chalcid Megastigmus wachtli, facilitates infection by S. cardinale (Tiberi and Battisti, 1998; Battisti et al., 2000). Seeds attacked by S. cardinale loose their germinability.

Pathogen Transmission

In a survey carried out with seeds from nine species of Cupressaceae from Italy and France, 0.5% to 70% of seeds were either surface-contaminated or infected by the pathogen even when collected from healthy-looking trees (Saponaro and Motta, 1984).

Seed Health Tests

The blotter method is commonly used for cypress seed testing (Saponaro and Motta, 1984). X-ray analysis has been used to assess cypress seed quality and the damage caused by insects and pathogenic fungi, including S. cardinale (Battisti et al., 2000).

Seed Treatments

Slurry dressing or immersion of seeds in an aqueous suspension of benomyl or thiophanate-methyl reduced infection from 47% (untreated) to 0-1% (Motta, 1984).

Plant Trade

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Wood Packaging

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Impact Summary

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Impact

Top of page Infection of susceptible cypress trees by S. cardinale under favourable environmental conditions is fatal. Death of the tree may take up to a few months or even years, depending on the species, clone, age, and environmental factors. In the Mediterranean region, where climatic conditions are favourable to the pathogen, the epidemic of cypress blight is so advanced that it has threatened to become an ecological disaster (Graniti, 1993, 1998a). Actually, about 85% of the existing population of C. sempervirens in Italy, estimated on seedlings from commercial seed, was found susceptible to the disease (Raddi and Panconesi, 1981b). In a similar survey carried out in Greece (Xenopoulos, 1990) with seedlings from natural stands, the percentages of susceptible cypress trees ranged from 97.2 (Crete) and 92.7 (Rhodes) to 88.6 (Samos).

Heavy economic losses have been caused by cypress canker to the ornamental trees industry, especially in districts like Provence in France and Tuscany in Italy, where nurseries are an important economic activity and cypresses represent a major part of the marketable production.

Moreover, cypress trees grow easily in poor, arid soils, and thus are almost irreplaceable in replanting degraded hilly areas and in reforestation. Several species of cypress are widely used as efficient windbreaks for citrus and other subtropical crops. Finally, cypress groves produce a highly valued timber.

Since its introduction, S. cardinale has caused destructive and recurrent epidemics that have devastated forests, natural stands, plantations, windbreaks and ornamental cypress trees in several countries of various parts of the world. The first epidemics in California, USA, resulted in a loss of about 30,000 trees of Cupressus macrocarpa and C. sempervirens (Wagener, 1939, 1948, 1964).

In central Italy (Tuscany), where the disease was first recorded more than 50 years ago, the most susceptible trees were killed in the first decades after introduction. The average incidence of canker on residual cypress plantations was estimated at 23.3% in 1995 (Pivi, 1995) and is currently 23-27%; but it has reached 75% in some groves around Florence (Panconesi, 1991; Panconesi and Raddi, 1998). A 1978 survey in the district of Florence showed that some 720,000 of the approximately 4 million cypress trees in the area (i.e., 18%) were either dead or severely affected by the disease (Poggesi, 1979). This figure would have been even higher (close to 1 million trees), if all diseased trees with only light infections (about 6%), which would die subsequently, had been considered. Further assessments were not made in the same area in the following years; meanwhile, the disease has progressed. A 7200-tree cypress grove near Florence was sampled every year to assess the disease incidence during the period 1981-1993. The relative figures were 31.3% (1981) and 50.6% (1993) incidence, representing a 19.3% increase in 12 years (Panconesi and Raddi, 1991b, 1998).

In Greece, the highest incidences were recorded in the areas around Kyrgia (70%), in the valley of Megalopolis, western Peloponnesus (90%), and around Karistos (98%), a windy valley of Euboea island, where cypresses are used extensively as windbreaks (Xenopoulos and Diamandis, 1985; Xenopoulos, 1991; Panconesi and Raddi, 1991). The annual increase of the disease in some stands in the Peloponnesus, with an initial attack of 20%, ranged from 5% to 20% (Xenopoulos, 1991a).

By contrast, the spread and severity of the cypress canker caused by S. cardinale have been low or virtually negligible in the warmest areas of the Mediterranean region, such as North Africa; however, in these areas, Lepteutypa cupressi represents a potential threat.

Economic Impact

Top of page Infection of susceptible cypress trees by S. cardinale under favourable environmental conditions is fatal. Death of the tree may take up to a few months or even years, depending on the species, clone, age, and environmental factors. In the Mediterranean region, where climatic conditions are favourable to the pathogen, the epidemic of cypress blight is so advanced that it has threatened to become an ecological disaster (Graniti, 1993, 1998a). Actually, about 85% of the existing population of C. sempervirens in Italy, estimated on seedlings from commercial seed, was found susceptible to the disease (Raddi and Panconesi, 1981b). In a similar survey carried out in Greece (Xenopoulos, 1990) with seedlings from natural stands, the percentages of susceptible cypress trees ranged from 97.2 (Crete) and 92.7 (Rhodes) to 88.6 (Samos).

Heavy economic losses have been caused by cypress canker to the ornamental trees industry, especially in districts like Provence in France and Tuscany in Italy, where nurseries are an important economic activity and cypresses represent a major part of the marketable production.

Moreover, cypress trees grow easily in poor, arid soils, and thus are almost irreplaceable in replanting degraded hilly areas and in reforestation. Several species of cypress are widely used as efficient windbreaks for citrus and other subtropical crops. Finally, cypress groves produce a highly valued timber.

Since its introduction, S. cardinale has caused destructive and recurrent epidemics that have devastated forests, natural stands, plantations, windbreaks and ornamental cypress trees in several countries of various parts of the world. The first epidemics in California, USA, resulted in a loss of about 30,000 trees of Cupressus macrocarpa and C. sempervirens (Wagener, 1939, 1948, 1964).

In central Italy (Tuscany), where the disease was first recorded more than 50 years ago, the most susceptible trees were killed in the first decades after introduction. The average incidence of canker on residual cypress plantations was estimated at 23.3% in 1995 (Pivi, 1995) and is currently 23-27%; but it has reached 75% in some groves around Florence (Panconesi, 1991; Panconesi and Raddi, 1998). A 1978 survey in the district of Florence showed that some 720,000 of the approximately 4 million cypress trees in the area (i.e., 18%) were either dead or severely affected by the disease (Poggesi, 1979). This figure would have been even higher (close to 1 million trees), if all diseased trees with only light infections (about 6%), which would die subsequently, had been considered. Further assessments were not made in the same area in the following years; meanwhile, the disease has progressed. A 7200-tree cypress grove near Florence was sampled every year to assess the disease incidence during the period 1981-1993. The relative figures were 31.3% (1981) and 50.6% (1993) incidence, representing a 19.3% increase in 12 years (Panconesi and Raddi, 1991b, 1998).

In Greece, the highest incidences were recorded in the areas around Kyrgia (70%), in the valley of Megalopolis, western Peloponnesus (90%), and around Karistos (98%), a windy valley of Euboea island, where cypresses are used extensively as windbreaks (Xenopoulos and Diamandis, 1985; Xenopoulos, 1991; Panconesi and Raddi, 1991). The annual increase of the disease in some stands in the Peloponnesus, with an initial attack of 20%, ranged from 5% to 20% (Xenopoulos, 1991a).

By contrast, the spread and severity of the cypress canker caused by S. cardinale have been low or virtually negligible in the warmest areas of the Mediterranean region, such as North Africa; however, in these areas, Lepteutypa cupressi represents a potential threat.

Environmental Impact

Top of page The devastation of planted and ornamental cypress trees has caused not only serious economic losses, but also other grim consequences for the environment and social life, including tourism. This holds true where cypress is not only a key component of the landscape and an irreplaceable decoration for monuments and historical places, like Florence in Italy and Olympia in Greece, but an integral part of the nation's history.

Diagnosis

Top of page A correct diagnosis of cypress canker and a proper identification of the pathogen are a prerequisite for determining actions to be taken. Identification of cypress blight does not present a problem for an experienced plant pathologist in areas where one or few cypress species or clones are grown, and where S. cardinale is the sole or the prevailing pathogenic species of Seiridium. When several species of Cupressaceae, often showing non-specific symptoms, are mixed in groves or parks, or when more than one pathogen is present, identification is more difficult and diagnosis is usually based both on microscopic examination of conidiomata or other reproductive structures formed in vivo, and by isolation and determination of the pathogen in culture. This is not always easy because the presence of the pathogen can be masked by other fungi (e.g. species of Pestalotiopsis) colonizing cankers.

Identification of S. cardinale is possible by microscopic examination of mitospores (conidia) produced on the surface of cankers or in culture. The six-celled conidia of S. cardinale are discernible from those of related species of Coelomycetes by the absence of long appendages at one or both conidial ends. Other methods, cultural, serological, chemical and molecular are available.

Detection and Inspection

Top of page The first symptom of the disease is noticeable from a distance as a change in colour of the foliage, which turns yellow and eventually brownish-red in dead trees. A diffuse foliar yellowing or reddening of twigs, branches and apical parts of the affected trees is a common characteristic of the disease. The flow of resin exuding from the cankers makes it easy to localize stem cankers hidden by the dense foliage of several cypress species. Such a resinous exudation, which is not present in cankers caused by other pathogens (e.g. Diaporthe occulta [D. eres]), may be abundant on the bark of the trunk or branches. Fading and dieback of twigs, branches and treetops are noticeable at distance, and these symptoms may facilitate a disease survey. Potential losses from disease in a cypress forest or plantation can be assessed from the air.

For disease assessment, either extension or size of cankers on stem or branches, and rating by visual scales of leaf damage and severity of dieback, are commonly used. As necrosis may extend from the cankered bark to the first layers of sapwood, the necrotic area can be seen (and measured) as a brown lesion of the wood surface in decorticated stems or trunks.

Similarities to Other Species/Conditions

Top of page Two more species with anamorphs in the genus Seiridium are known to cause canker diseases on various Cupressaceae: Lepteutypa cupressi (anamorph: Seiridium cupressi) and Seiridium unicorne (Swart, 1973; Sutton, 1975, 1980; Boesewinkel, 1983; Graniti, 1986; Graniti and Frisullo, 1990).

Lepteutypa cupressi caused serious losses to cypress plantations, especially to Cupressus macrocarpa, in Kenya in the 1940s (Nattrass and Ciccarone, 1947; Ciccarone, 1949; Nattrass et al., 1963), then in New Zealand (Boesewinkel, 1983) and in Australia. In the Mediterranean area, it was found in a natural forest of C. sempervirens on the Greek island of Kos (Graniti, 1986, 1998a; Xenopoulos, 1991a) and subsequently eradicated. Inoculation experiments with L. cupressi on susceptible hosts showed highest pathogenicity at 20-25°C. At 30°C the pathogen produces little disease (Graniti and Frisullo, 1990). After infection, L. cupressi progresses slowly during winter and faster during spring and early summer, with little or no growth at 35°C. On infected trees, the necrotic process continues even in the hottest months of the year, whereas that of S. cardinale is slowed. Hence, L. cupressi could potentially become established in the warmest Mediterranean areas (Panconesi, 1990).

Seiridium unicorne is a widespread and plurivorous fungus, which is common, but not serious, in several parts of the world (Portugal: Caetano et al., 1991; USA: Tisserat et al., 1991; New Zealand: van der Werff, 1988). Destructive epidemics of S. unicorne have not been reported. However, it has caused an epidemic of canker disease to the Hinoki cypress (Chamaecyparis obtusa) in Japan with serious losses to young plantations (Tabata, 1991).

S. cardinale can be distinguished from S. cupressi and S. unicorne on the basis of morphological and cultural traits, and this has been confirmed by physiological, pathogenic, toxicological and enzymatic polymorphism data (Boesewinkel, 1983; Graniti, 1986, 1998a; Graniti and Frisullo, 1990; Ponchet et al., 1990; Nag Raj, 1994; Raddi et al., 1994). In the past, some contrasting views were put forward, based in part on data from non-authenticated isolates, according to which, cypress canker is due to two species (with either presence or absence of long conidial appendages) or to only one species of variable morphology (Swart, 1973; Chou, 1989; Viljoen et al., 1993). More recently, distinction of three species of Seiridium affecting cypress trees was confirmed by phylogenetic and molecular data (PCR and SSCP or RFLP analysis of rDNA sequences: Moricca and Raddi, 1999, 2000; Moricca et al., 2001; histone and partial b-tubulin sequences: Barnes et al., 2001).

Fungi other than species of Seiridium are known to cause canker diseases on cypress in several countries. Among them, Sphaeropsis sapinea f.sp. cupressi (Solel et al., 1987; Frisullo and Graniti, 1990; Swart et al., 1993; Linde et al., 1997; Frisullo et al., 1997; Xenopoulos and Tsopelas, 2000); Botryosphaeria stevensii (Frisullo and Graniti, 1990); Diaporthe occulta [D. eres] (Farr et al., 1989); Lasiodiplodia theobromae (Bruck et al., 1990).

Dieback of shoots, a diffuse reddening and drying of foliage, and a general decline of trees can be caused by other adverse factors, e.g. frost damage and infestation by the aphid Cinara cupressi. The latter caused serious damage in central and southern Italy in the 1970s (Covassi and Binazzi, 1979; Binazzi et al., 1998).

Prevention and Control

Top of page Cultural Control and Sanitary Measures

Sanitation is the most efficient method to control epidemic spread of the disease. Localization of infected individual trees, their felling, and destruction of disease foci at their first appearance in a previously uncontaminated area are fundamental measures for disease eradication. In areas where the disease is already established, early pruning of any limbs or tops showing symptoms, removal of the affected organs in the partially affected crowns, and the felling of heavily infected or dead trees is recommended in order to reduce the sources of inoculum and to avoid spread of vectors to healthy trees. All the infected material, i.e. the pruned branches, and the bark removed from the stem of trees should be collected and burned.

Sanitation for single or small groups of trees is possible only if the infection is not too extensive. Only partially infected trees benefit from surgery, whereas severely damaged trees need replacing with resistant clones. The surgical removal of incipient cankers from the branches or stems of trees is followed by fungicide (benomyl or carbendazim) painting of exposed wounds and subsequent protection with a resin dressing (Marchetti and Zechini D'Aulerio, 1983). Finally, the whole tree or at least the area around the cankers is sprayed with a systemic fungicide. If necessary, these interventions should be repeated once or twice in the following years. They may save individual trees. In central Italy, 10 years of sanitation efforts in one area resulted in 5.1% diseased trees compared with 20.6% in untreated areas (Moricca and Raddi, 2000).

These sanitary measures, which are applied to ornamental trees in gardens, parks and avenues, especially in urban and peri-urban areas, may be too expensive (Puleri, 1996) or difficult to apply, and also require technical and organizational efforts, when belts of windbreaks, large plantations and cypress woods are concerned. In cypress forests and groves, the process of sanitation is to fell and remove all the affected trees quickly. Timber of felled trunks can be recovered, provided that bark and branches are removed and burned.

Cypress groves for seed production can be efficiently reclaimed by repeated and drastic application of the above sanitary measures in order to remove all the affected (and most susceptible) trees. One of the consequences of these measures is that the surviving trees not only produce relatively healthy seed, but also pollen endowed with genetic resistance to the disease, which may contribute to the improvement of seed quality.

Sanitation is currently applied in cypress nurseries and propagation plots. General information and details on the sanitation procedures, surgical and pruning methods are given in: Raddi and Panconesi, 1981a, 1981b; Nembi and Panconesi, 1982; Strouts, 1988; Parrini and Panconesi, 1991; Madar et al., 1991; Self and Chou, 1994; Vetralla et al., 1995; Panconesi and Raddi, 1998; Danti, 2001. For problems in urban and peri-urban areas, see: Graniti, 1998b, Andréoli, 1999; Moricca and Raddi, 2000.

Chemical Control

A number of protectant (dichlofluanide, chlorothalonil or, to a lesser extent, copper-based preparations) and systemic fungicides, including benomyl, carbendazim and thiophanate-methyl, better if applied as mixed or alternate treatments, have shown to be effective to control S. cardinale (Raddi and Panconesi, 1981a, 1981b, Mathon, 1982; McCain, 1984; Ponchet, 1986; Panconesi and Raddi, 1986; Moricca and Raddi, 2000).

Due to the long infection period and to the height of trees, chemical control of cypress canker by spraying trees with fungicides may be uneconomic or impractical except for nurseries or valuable ornamental plantings. Repeated applications of fungicides, from 2-3 to 4-6 times per year, particularly during the mild seasons and after pruning, are effective to prevent the disease or to stop the progress of the pathogen in recently-infected (within 10 days of infection) bark tissue. These sprays, however, have little or no value if applied as curative treatments to trees that are already diseased (Panconesi and Raddi, 1986). Problems may arise when chemical control of cypress canker is carried out in urban environment (Graniti, 1998b; Danti, 2001). Protection of pruning wounds with a systemic fungicide and with a sealing slurry or dressing is a current practice in nurseries and young plantations of ornamental trees.

Biological Control

Growth of S. cardinale was strongly inhibited by Trichoderma viride (Magro et al., 1984; Marchetti et al., 1986). The possibility of controlling infections of the pathogen with the aid of T. viride or other antagonistic microorganisms has been envisaged. Application of wet soil containing natural populations of T. viride to bark cankers favoured the healing of lesions on young cypress trees (Marchetti et al., 1986).

Host-Plant Resistance

Several investigations have shown that a high variability of susceptibility or resistance to S. cardinale exists in natural forests as well as in plantations of Cupressus sempervirens. Variability ranged from quite resistant to highly susceptible trees, indicating that resistance is a population characteristic, with mechanisms under polygenic control. Pollen is partly responsible for the resistance displayed by the progeny. Such a condition has helped breeders to select resistant clones, and to afford the genetic improvement of cypress species for resistance to the canker disease (Raddi and Panconesi, 1981a, 1981b, 1991, 1998; Xenopoulos, 1990; Raddi et al., 1998; Santini and Di Lonardo, 2000).

The most effective means of controlling cypress canker is the adoption of resistant clones, hybrids or species. Considerable efforts have been made in the past decades to develop a common strategy in the Mediterranean area (Grasso and Raddi, 1979; Raddi, 1984; Ponchet, 1986, 1990; Panconesi, 1991).

The main aims of this strategy have been: identification of cypresses resistant to the canker disease; large-scale production of selected cypress seed, which can produce a high percentage of resistant seedlings for replanting and reforestation; intraspecific crosses betweens resistant clones of cypress; interspecific crosses with resistant cypress species (Raddi and Panconesi, 1981a, 1981b, 1991; Teissier du Cros et al., 1991; Raddi and Panconesi, 1998; Santini et al., 1997b; Raddi et al., 1990, 1998). The following species of Cupressus have been considered in some breeding programmes for resistance: C. arizonica, C. bakeri, C. funebris [Chamaecyparis funebris], C. duclouxiana, C. torulosa, C. cashmeriana, C. lusitanica, C. abramsiana, C. guadalupensis, C. macnabiana, C. goveniana, C. dupreziana [C. sempervirens var. dupreziana] (Ponchet and Andréoli, 1979, 1993; Raddi et al., 2000).

Several clones of S. sempervirens have been selected (and some of them patented) for resistance to cypress canker, and are now commercially available, mostly as windbreaks or ornamentals. The same clones also exhibit rapid growth and tolerance of frost (Panconesi and Raddi, 1990, 1991a; Santini et al., 1997b). Other resistant clones, particularly adapted to urban landscape, were also selected (Andréoli, 1999).

For large-scale production of resistant clones, micropropagation and techniques for obtaining shoot cuttings were developed (Siniscalco and Pavolettoni, 1994; Capuana and Lambardi, 1995; Spanos, 1995; Spanos et al., 1997b). In nurseries, grafting vegetative propagation is generally used. Young trees (ramets) of clones of Italian cypress selected for resistance to S. cardinale, grafted onto seed-derived rootstocks, usually maintain the growth vigour and crown shape of their mother trees (ortets) if grown in the same environment (Santini et al., 1997b). Santini et al. (2000) showed that self-rooted homospecific and heteroplastic grafts did not change the resistance of the grafted clones significantly. The most suitable rootstocks are canker-resistant clones of C. sempervirens or clones of more resistant species, e.g. C. glabra, propagated by rooted cutting (Andréoli et al., 1966).

Work is now in progress to produce multiclonal varieties, i.e. mixed populations of several clones of C. sempervirens, each endowed with different resistance to S. cardinale, to be used for windbreaks or new plantations (Raddi and Panconesi, 1991; Raddi et al., 1998).

A particular problem in replanting cypress clones selected for resistance to canker disease, particularly in the urban environment, is the risk of pollinosis. Long-term breeding programmes are in progress, which include identification of clones with low and brief production of pollen, and a low content of allergens (Raddi et al., 2000).

Control of Vectors

Insects able to spread S. cardinale, such as the cypress bark borer beetles Phloeosinus aubei and the seed bug Orsillus maculatus, have to be kept under control. Removal of branches or trees killed or severely infected by S. cardinale, use of insecticide-treated trap-logs (Mendel, 1983) and insecticide sprays, especially in the nursery, are recommended. Use of pheromone traps has also been envisaged (Tiberi and Battisti, 1998).

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Xenopoulos S; Tsopelas P, 2000. Sphaeropsis canker, a new disease of cypress in Greece. Forest Pathology, 30(3):121-126; 12 ref.

Xenopoulos SG, 1991. Pathogenic variability of various isolates of Seiridium cardinale, S. cupressi and S. unicorne inoculated on selected Cupressus clones and seedlings. European Journal of Forest Pathology, 21(3):129-135

Xenopoulos SG, 1991. The cypress health state in Greece and new prospect from current research. In: Panconesi A, ed. Il Cipresso. Proposte di valorizzazione ambientale e produttiva nei paesi mediterranei della Comunità Economica Europea. Firenze, Italy: CNR Regione Toscana CEE, 61-70.

Distribution Maps

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